@article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/105373, title ="A Systematic Nomenclature for the Drosophila Ventral Nerve Cord", author = "Court, Robert and Namiki, Shigehiro", journal = "Neuron", volume = "107", number = "6", pages = "1071-1079", month = "September", year = "2020", doi = "10.1016/j.neuron.2020.08.005", issn = "0896-6273", url = "https://resolver.caltech.edu/CaltechAUTHORS:20200914-111809468", note = "© 2020 The Authors. Published by Elsevier Under a Creative Commons license - Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0). \n\nReceived 13 February 2020, Revised 30 June 2020, Accepted 5 August 2020, Available online 14 September 2020. \n\nWe thank Gerald M. Rubin, Janine Stevens, the Visiting Science and Conference Programs of the Howard Hughes Medical Institute’s Janelia Research Campus for hosting the workshop. This work was initially conceived of as part of the Descending Interneuron Project Team at Janelia. This work was also supported, in part, by grants EP/F500385/1 and BB/F529254/1 for the University of Edinburgh School of Informatics Doctoral Training Centre in Neuroinformatics and Computational Neuroscience (http://www.anc.ed.ac.uk/dtc) from the UK Engineering and Physical Sciences Research Council (EPSRC), UK Biotechnology and Biological Sciences Research Council (BBSRC), and the UK Medical Research Council (MRC). Finally, by the Wellcome Trust as part of the “Virtual Fly Brain: a global informatics hub for Drosophila neurobiology” WT105023MA. \n\nAuthor Contributions. Conceptualization, W.K., J.W.T., and D.S.; Software, R.C.; Validation, All; Resources, D.S., R.C., and J.B.; Data Curation, R.C., M.C., and J.D.A; Writing—Original Draft, D.S. and R.C.; Writing—Review & Editing, M.C., M.D., R.K.M., A.M.S., J.H.S., T.S., J.C.T., J.W.T., and D.W.W.; Visualization, D.S. and R.C.; Funding Acquisition, All. \n\nResource Availability. Lead Contact: Further information and requests for data and resources should be directed to and will be fulfilled by the Lead Contact, David Shepherd (d.shepherd@bangor.ac.uk). \n\nMaterials Availability. This study did not generate any new reagents. \n\nData and Code Availability. All anatomical datasets and segmented domains have been deposited at Virtual Fly Brain (https://github.com/VirtualFlyBrain/DrosAdultVNSdomains/tree/master/Court2017/template) and are openly available. \n\nThe authors declare no competing interests.", revision_no = "27", abstract = "Drosophila melanogaster is an established model for neuroscience research with relevance in biology and medicine. Until recently, research on the Drosophila brain was hindered by the lack of a complete and uniform nomenclature. Recognizing this, Ito et al. (2014) produced an authoritative nomenclature for the adult insect brain, using Drosophila as the reference. Here, we extend this nomenclature to the adult thoracic and abdominal neuromeres, the ventral nerve cord (VNC), to provide an anatomical description of this major component of the Drosophila nervous system. The VNC is the locus for the reception and integration of sensory information and involved in generating most of the locomotor actions that underlie fly behaviors. The aim is to create a nomenclature, definitions, and spatial boundaries for the Drosophila VNC that are consistent with other insects. The work establishes an anatomical framework that provides a powerful tool for analyzing the functional organization of the VNC.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/104029, title ="Flies Remember Multiple Food Locations in the Absence of External Cues", author = "Behbahani, A. H. and Rak, A. K.", journal = "Integrative and Comparative Biology", volume = "60", number = "S1", pages = "E15", month = "March", year = "2020", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20200625-074412672", note = "© 2020 Society for Integrative and Comparative Biology. \n\nPublished: 12 March 2020.", revision_no = "6", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/101374, title ="Genome editing in non-model organisms opens new horizons for comparative physiology", author = "Dickinson, Michael H. and Vosshall, Leslie B.", journal = "Journal of Experimental Biology", volume = "223", number = "Suppl 1", pages = "1", month = "February", year = "2020", doi = "10.1242/jeb.221119", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20200219-103200881", note = "© 2020 Published by The Company of Biologists Ltd.", revision_no = "9", abstract = "For almost 100\u2005years, biologists have made fundamental discoveries using a handful of model organisms that are not representative of the rich diversity found in nature. The advent of CRISPR genome editing now opens up a wide range of new organisms to mechanistic investigation. This increases not only the taxonomic breadth of current research but also the scope of biological problems that are now amenable to study, such as population control of invasive species, management of disease vectors such as mosquitoes, the creation of chimeric animal hosts to grow human organs and even the possibility of resurrecting extinct species such as passenger pigeons and mammoths. Beyond these practical applications, work on non-model organisms enriches our basic understanding of the natural world. This special issue addresses a broad spectrum of biological problems in non-model organisms and highlights the utility of genome editing across levels of complexity from development and physiology to behaviour and evolution.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/99214, title ="Flies Regulate Wing Motion via Active Control of a Dual-Function Gyroscope", author = "Dickerson, Bradley H. and de Souza, Alysha M.", journal = "Current Biology", volume = "29", number = "20", pages = "3517-3524", month = "October", year = "2019", doi = "10.1016/j.cub.2019.08.065", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20191010-123834351", note = "© 2019 Elsevier Ltd. \n\nReceived 24 June 2019, Revised 22 August 2019, Accepted 23 August 2019, Available online 10 October 2019. \n\nWe thank Gwyneth Card, Erica Ehrhardt, and Wyatt Korff for sharing SS36076, SS41075, and SS43980. We also thank Anne von Philipsborn for providing us with UAS-Chrimson; VT22025-p65.ADZ VT29310-GAL4.DBD for the tp1-SG experiments. We are grateful to Thad Lindsay and Ivo Ros for help with setting up imaging experiments. This work was supported by grants from the NSF (DBI-1523434 to B.H.D.) and the NINDS-NIH (U01NS090514 and U19NS104655 to M.H.D.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. \n\nAuthor Contributions: Conceptualization, B.H.D. and M.H.D.; Methodology, B.H.D., A.M.d.S., A.H., and M.H.D.; Investigation, B.H.D., A.M.d.S., and A.H.; Writing – Original Draft, B.H.D. and M.H.D.; Writing – Review & Editing, B.H.D. and M.H.D.; Funding Acquisition, B.H.D. and M.H.D.; Resources, M.H.D.; Supervision, M.H.D. \n\nThe authors declare no competing interests.", revision_no = "19", abstract = "Flies execute their remarkable aerial maneuvers using a set of wing steering muscles, which are activated at specific phases of the stroke cycle [1, 2, 3]. The activation phase of these muscles—which determines their biomechanical output [4, 5, 6]—arises via feedback from mechanoreceptors at the base of the wings and structures unique to flies called halteres [7, 8, 9]. Evolved from the hindwings, the tiny halteres oscillate at the same frequency as the wings, although they serve no aerodynamic function [10] and are thought to act as gyroscopes [10, 11, 12, 13, 14, 15]. Like the wings, halteres possess minute control muscles whose activity is modified by descending visual input [16], raising the possibility that flies control wing motion by adjusting the motor output of their halteres, although this hypothesis has never been directly tested. Here, using genetic techniques possible in Drosophila melanogaster, we tested the hypothesis that visual input during flight modulates haltere muscle activity and that this, in turn, alters the mechanosensory feedback that regulates the wing steering muscles. Our results suggest that rather than acting solely as a gyroscope to detect body rotation, halteres also function as an adjustable clock to set the spike timing of wing motor neurons, a specialized capability that evolved from the generic flight circuitry of their four-winged ancestors. In addition to demonstrating how the efferent control loop of a sensory structure regulates wing motion, our results provide insight into the selective scenario that gave rise to the evolution of halteres.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/92143, title ="Visual-olfactory integration in the human disease vector mosquito, Aedes aegypti", author = "Vinauger, Clément and van Breugel, Floris", journal = "Current Biology", volume = "29", number = "15", pages = "2509-2516", month = "August", year = "2019", doi = "10.1016/j.cub.2019.06.043", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190108-134557907", note = "© 2019 Elsevier Ltd. \n\nReceived 7 January 2019, Revised 21 March 2019, Accepted 13 June 2019, Available online 18 July 2019. \n\nComments from three anonymous reviewers greatly improved the manuscript and analyses. We thank B. Nguyen for mosquito colony maintenance; J. Tuthill, A. Mamiya, and P. Weir for comments and help with the arena and imaging experiments; G. Wolff for comments and imaging assistance; and D. Alonso San Alberto for technical support. We acknowledge the support of the Air Force Office of Scientific Research under grants FA9550-14-1-0398 and FA9550-16-1-0167, NIH under grants 1RO1DCO13693 and 1R21AI137947, an Endowed Professorship for Excellence in Biology (J.A.R.), and the University of Washington Innovation Award. O.S.A. was supported in part by NIH grants 5K22AI113060 and 1R21AI123937.\n\nAuthor Contributions:\nC.V., F.V.B., A.L.F., M.H.D., and J.A.R. conceived the study. C.V., F.V.B., L.T.L., and K.K.S.T. participated in the execution and analysis of the arena assays. O.S.A. generated the GCaMP6 mosquitoes. J.A.R. conducted the imaging assays, and C.V., F.V.B., and J.A.R. analyzed the imaging data. C.V., F.V.B., and J.A.R. wrote the paper, and all authors edited the manuscript.\n\nDeclaration of Interests:\nThe authors declare no competing interests.", revision_no = "31", abstract = "Mosquitoes rely on the integration of multiple sensory cues, including olfactory, visual, and thermal stimuli, to detect, identify, and locate their hosts [1, 2, 3, 4]. Although we increasingly know more about the role of chemosensory behaviors in mediating mosquito-host interactions [1], the role of visual cues is comparatively less studied [3], and how the combination of olfactory and visual information is integrated in the mosquito brain remains unknown. In the present study, we used a tethered-flight light-emitting diode (LED) arena, which allowed for quantitative control over the stimuli, and a control theoretic model to show that CO_2 modulates mosquito steering responses toward vertical bars. To gain insight into the neural basis of this olfactory and visual coupling, we conducted two-photon microscopy experiments in a new GCaMP6s-expressing mosquito line. Imaging revealed that neuropil regions within the lobula exhibited strong responses to objects, such as a bar, but showed little response to a large-field motion. Approximately 20% of the lobula neuropil we imaged were modulated when CO2 preceded the presentation of a moving bar. By contrast, responses in the antennal (olfactory) lobe were not modulated by visual stimuli presented before or after an olfactory stimulus. Together, our results suggest that asymmetric coupling between these sensory systems provides enhanced steering responses to discrete objects.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/98869, title ="The effects of target contrast on Drosophila courtship", author = "Agrawal, Sweta and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "222", number = "16", pages = "Art. No. jeb203414", month = "August", year = "2019", doi = "10.1242/jeb.203414", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190926-090305792", note = "© 2019 Published by The Company of Biologists Ltd. \n\nReceived 14 March 2019; Accepted 11 July 2019. \n\nWe thank D. Anderson for providing the P1 split-GAL4 line and A. Sustar for her help with backcrossing all fly lines into a Canton-S background. We also thank S. Safarik for his help with technical details relating to the Flyatar apparatus, and Kristin Branson, Alice Robie and Juan Rodriguez-Gonzalez for the Duotrax software used to track wings. \n\nThe authors declare no competing or financial interests. \n\nAuthor contributions: Conceptualization: S.A., M.H.D.; Methodology: S.A., M.H.D.; Software: S.A.; Validation: S.A.; Formal analysis: S.A.; Investigation: S.A.; Resources: M.H.D.; Data curation: S.A.; Writing - original draft: S.A.; Writing - review & editing: S.A., M.H.D.; Visualization: S.A., M.H.D.; Supervision: M.H.D.; Funding acquisition: M.H.D. \n\nThis material is based upon work supported by the Paul G. Allen Family Foundation and the National Science Foundation Graduate Research Fellowship Program under grant no. DGE-0718124. \n\nData availability: Data are available from the Dryad Digital Repository (Agrawal and Dickinson, 2019): https://doi.org/10.5061/dryad.k74670v \n\nSupplementary information: Supplementary information available online at http://jeb.biologists.org/lookup/doi/10.1242/jeb.203414.supplemental", revision_no = "12", abstract = "Many animals use visual cues such as object shape, color and motion to detect and pursue conspecific mates. Contrast is another possibly informative visual cue, but has not been studied in great detail. In this study, we presented male Drosophila melanogaster with small, fly-sized, moving objects painted either black, white or gray to test whether they use contrast cues to identify mates. We found that males frequently chased gray objects and rarely chased white or black objects. Although males started chasing black objects as often as gray objects, the resulting chases were much shorter. To test whether the attraction to gray objects was mediated via contrast, we fabricated black and gray behavioral chambers. However, wild-type males almost never chased any objects in these darkly colored chambers. To circumvent this limitation, we increased baseline levels of chasing by thermogenetically activating P1 neurons to promote courtship. Males with thermogenetically activated P1 neurons maintained a similar preference for gray objects despite elevated levels of courtship behavior. When placed in a black chamber, males with activated P1 neurons switched their preference and chased black objects more than gray objects. We also tested whether males use contrast cues to orient to particular parts of the female's body during courtship. When presented with moving objects painted two colors, males positioned themselves next to the gray half regardless of whether the other half was painted black or white. These results suggest that males can use contrast to recognize potential mates and to position themselves during courtship.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90223, title ="Diverse food-sensing neurons trigger idiothetic local search in Drosophila", author = "Corfas, Román A. and Sharma, Tarun", journal = "Current Biology", volume = "29", number = "10", pages = "1660-1668", month = "May", year = "2019", doi = "10.1016/j.cub.2019.03.004", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181010-085017891", note = "© 2019 Elsevier Ltd. \n\nReceived 10 October 2018, Revised 21 January 2019, Accepted 6 March 2019, Available online 2 May 2019. \n\nWe wish to thank Francesca V. Ponce for helpful discussions and assistance with preparing the synthetic food medium. Rubi Salgado assisted with fly rearing. Annie Rak helped with conducting the PER experiments. Ysabel M. Giraldo and Katherine J. Leitch provided advice on statistical analysis. Floris van Breugel and Theodore H. Lindsay helped implement the software used for tracking and closed-loop optogenetic stimulation. William B. Dickson created the software for closed-loop virtual fictive food sites, fabricated the balls for the spherical treadmill, and assisted in data analysis. Kristin Scott and John Carlson kindly provided us with flies. Research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under award U19NS104655. \n\nAuthor Contributions: R.A.C. conducted all experiments, except those in Figure 4, which were performed by T.S. R.A.C. analyzed all data and prepared all figures. R.A.C. and M.H.D. conceived of experiments and wrote the paper. \n\nThe authors declare no competing interests.", revision_no = "57", abstract = "Foraging animals may benefit from remembering the location of a newly discovered food patch while continuing to explore nearby [1, 2]. For example, after encountering a drop of yeast or sugar, hungry flies often perform a local search [3, 4]. That is, rather than remaining on the food or simply walking away, flies execute a series of exploratory excursions during which they repeatedly depart and return to the resource. Fruit flies, Drosophila melanogaster, can perform this food-centered search behavior in the absence of external landmarks, instead relying on internal (idiothetic) cues [5]. This path-integration behavior may represent a deeply conserved navigational capacity in insects [6, 7], but its underlying neural basis remains unknown. Here, we used optogenetic activation to screen candidate cell classes and found that local searches can be initiated by diverse sensory neurons. Optogenetically induced searches resemble those triggered by actual food, are modulated by starvation state, and exhibit key features of path integration. Flies perform tightly centered searches around the fictive food site, even within a constrained maze, and they can return to the fictive food site after long excursions. Together, these results suggest that flies enact local searches in response to a wide variety of food-associated cues and that these sensory pathways may converge upon a common neural system for navigation. Using a virtual reality system, we demonstrate that local searches can be optogenetically induced in tethered flies walking on a spherical treadmill, laying the groundwork for future studies to image the brain during path integration.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/94242, title ="Descending control of flight behavior in flies", author = "Namiki, S. and Ros, I.", journal = "Integrative and Comparative Biology", volume = "59", number = "S1", pages = "E166", month = "March", year = "2019", doi = "10.1093/icb/icz003", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190328-095719717", note = "© 2019 Oxford University Press. \n\nPublished: 11 February 2019.", revision_no = "14", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/94233, title ="Fruit flies must overcome inertial torques to modulate wing pitch", author = "Behbahani, A. H. and Melis, J. M.", journal = "Integrative and Comparative Biology", volume = "59", number = "S1", pages = "E14", month = "March", year = "2019", doi = "10.1093/icb/icz003", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190328-090148487", note = "© 2019 Oxford University Press. \n\nPublished: 11 February 2019.", revision_no = "10", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/94230, title ="Seasonality in Drosophila Sun Navigation", author = "Dan, M. and Giraldo, Y. M.", journal = "Integrative and Comparative Biology", volume = "59", number = "S1", pages = "E296", month = "March", year = "2019", doi = "10.1093/icb/icz004", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190328-082132500", note = "© 2019 Oxford University Press. \n\nPublished: 11 February 2019.", revision_no = "7", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/92817, title ="Celestial navigation in Drosophila", author = "Warren, Timothy L. and Giraldo, Ysabel M.", journal = "Journal of Experimental Biology", volume = "222", number = "S1", pages = "Art. No. jeb186148", month = "February", year = "2019", doi = "10.1242/jeb.186148", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190211-082112368", note = "© 2019 Published by The Company of Biologists Ltd. \n\nWe thank Peter Weir for comments on the manuscript. \n\nThe authors declare no competing or financial interests. \n\nThis work was funded by grants from the National Science Foundation (IOS 1547918), National Institutes of Health (U19NS104655) and the Simons Foundation (71582123) to M.H.D., as well as a National Institutes of Health NRSA postdoctoral fellowship (F32GM109777) to Y.M.G. Deposited in PMC for release after 12 months.", revision_no = "17", abstract = "Many casual observers typecast Drosophila melanogaster as a stationary pest that lurks around fruit and wine. However, the omnipresent fruit fly, which thrives even in desert habitats, likely established and maintained its cosmopolitan status via migration over large spatial scales. To perform long-distance dispersal, flies must actively maintain a straight compass heading through the use of external orientation cues, such as those derived from the sky. In this Review, we address how D. melanogaster accomplishes long-distance navigation using celestial cues. We focus on behavioral and physiological studies indicating that fruit flies can navigate both to a pattern of linearly polarized light and to the position of the sun – the same cues utilized by more heralded insect navigators such as monarch butterflies and desert ants. In both cases, fruit flies perform menotaxis, selecting seemingly arbitrary headings that they then maintain over time. We discuss how the fly's nervous system detects and processes this sensory information to direct the steering maneuvers that underlie navigation. In particular, we highlight recent findings that compass neurons in the central complex, a set of midline neuropils, are essential for navigation. Taken together, these results suggest that fruit flies share an ancient, latent capacity for celestial navigation with other insects. Furthermore, they illustrate the potential of D. melanogaster to help us to elucidate both the cellular basis of navigation and mechanisms of directed dispersal on a landscape scale.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90085, title ="Distinct activity-gated pathways mediate attraction and aversion to CO₂ in Drosophila", author = "van Breugel, Floris and Huda, Ainul", journal = "Nature", volume = "564", number = "7736", pages = "420-424", month = "December", year = "2018", doi = "10.1038/s41586-018-0732-8", issn = "0028-0836", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181002-123800797", note = "© 2018 Springer Nature Limited. \n\nReceived: 22 December 2017; Accepted: 11 October 2018; Published online: 21 November 2018. \n\nWe thank A. Straw for the 3D tracking software. Several colleagues provided mutants: R. Benton (quadruple mutant), R. Stanewsky (IR25a and rescue); G. Suh (IR8a); and M. Gallio and M. Stensmyr (IR40a). R. Benton, E. Hong and J. Riffell contributed helpful comments. This work was funded by grants from NIH (NIH1RO1DCO13693-01, U01NS090514) and the Simons Foundation. \n\nReviewer information: Nature thanks S. Combes, M. Frye, L. Vosshall and R. Wilson for their contribution to the peer review of this work. \n\nAuthor Contributions: F.v.B. and M.H.D. conceived the experiments. A.H. made genetic recombinants. F.v.B. and A.H. performed experiments. F.v.B. analysed data. F.v.B. and M.H.D. wrote the manuscript. \n\nData availability: Processed data are available in a Dryad repository at https://doi.org/10.5061/dryad.2s8422f. Raw data are available from the corresponding author upon request. \n\nCode availability: Custom code is available online at https://github.com/florisvb/drosophila_co2_attraction. \n\nReporting summary: Further information on research design is available in the Nature Research Reporting Summary linked to this paper. \n\nThe authors declare no competing interests.", revision_no = "94", abstract = "Carbon dioxide is produced by many organic processes and is a convenient volatile cue for insects that are searching for blood hosts, flowers, communal nests, fruit and wildfires. Although Drosophila melanogaster feed on yeast that produce CO₂ and ethanol during fermentation, laboratory experiments suggest that walking flies avoid CO₂. Here we resolve this paradox by showing that both flying and walking Drosophila find CO₂ attractive, but only when they are in an active state associated with foraging. Their aversion to CO₂ at low-activity levels may be an adaptation to avoid parasites that seek CO₂, or to avoid succumbing to respiratory acidosis in the presence of high concentrations of CO_2 that exist in nature. In contrast to CO₂, flies are attracted to ethanol in all behavioural states, and invest twice the time searching near ethanol compared to CO₂. These behavioural differences reflect the fact that ethanol is a unique signature of yeast fermentation, whereas CO₂ is generated by many natural processes. Using genetic tools, we determined that the evolutionarily conserved ionotropic co-receptor IR25a is required for CO₂ attraction, and that the receptors necessary for CO₂ avoidance are not involved in this attraction. Our study lays the foundation for future research to determine the neural circuits that underlie both state- and odorant-dependent decision-making in Drosophila.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90638, title ="Algorithms for Olfactory Search across Species", author = "Baker, Keeley L. and Dickinson, Michael", journal = "Journal of Neuroscience", volume = "38", number = "44", pages = "9383-9389", month = "October", year = "2018", doi = "10.1523/jneurosci.1668-18.2018", issn = "0270-6474", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181105-102039199", note = "© 2018 the authors. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). \n\nReceived Aug. 8, 2018; revised Sept. 15, 2018; accepted Sept. 18, 2018. \n\nThe authors declare no competing financial interests.", revision_no = "13", abstract = "Localizing the sources of stimuli is essential. Most organisms cannot eat, mate, or escape without knowing where the relevant stimuli originate. For many, if not most, animals, olfaction plays an essential role in search. While microorganismal chemotaxis is relatively well understood, in larger animals the algorithms and mechanisms of olfactory search remain mysterious. In this symposium, we will present recent advances in our understanding of olfactory search in flies and rodents. Despite their different sizes and behaviors, both species must solve similar problems, including meeting the challenges of turbulent airflow, sampling the environment to optimize olfactory information, and incorporating odor information into broader navigational systems.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90224, title ="Imaging neural activity in the ventral nerve cord of behaving adult Drosophila", author = "Chen, Chin-Lin and Hermans, Laura", journal = "Nature Communications", volume = "9", pages = "Art. No. 4390", month = "October", year = "2018", doi = "10.1038/s41467-018-06857-z", issn = "2041-1723", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181010-090159092", note = "© 2018 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. \n\nReceived 13 March 2018; Accepted 02 October 2018; Published\n22 October 2018. \n\nData availability: The source data used for the analyses in this study are available on the Harvard Dataverse on a ‘public repository’. Analysis code and sample datasets can be found ‘here’. \n\nWe thank B.J. Dickson (Janelia Research Campus, VA) for MDN-1-Gal4 and MAN-Gal4 fly strains. We thank G. Rubin (Janelia Research Campus, VA) for DNa01-Gal4, DNb06-Gal4, DNg13-Gal4, and DNg16-Gal4 fly strains. A.C. acknowledges support from the National Institutes of Health (R01HL124091). M.H.D. acknowledges support from the National Institute of Neurological Disorders and Stroke of the National Institutes of Health (U01NS090514). P.R. acknowledges support from the Swiss National Science Foundation (31003A_175667). \n\nAuthor Contributions: C.L.C. generated strains; performed experiments; analyzed data, L.H. performed experiments; analyzed data, M.C.V. generated strains; performed experiments; analyzed data, D.F. designed and implemented the motion-compensation algorithm F.A. analyzed data, M.U. designed the motion-compensation algorithm, A.C. designed and supervised the project, M.H.D. designed and supervised the project, P.R. conceived of, designed, and supervised the project; performed experiments; analyzed data, All authors contributed to writing the paper. \n\nThe authors declare no competing interests.", revision_no = "72", abstract = "To understand neural circuits that control limbs, one must measure their activity during behavior. Until now this goal has been challenging, because limb premotor and motor circuits have been largely inaccessible for large-scale recordings in intact, moving animals—a constraint that is true for both vertebrate and invertebrate models. Here, we introduce a method for 2-photon functional imaging from the ventral nerve cord (VNC) of behaving adult Drosophila melanogaster. We use this method to reveal patterns of activity across nerve cord populations during grooming and walking and to uncover the functional encoding of moonwalker ascending neurons (MANs), moonwalker descending neurons (MDNs), and a previously uncharacterized class of locomotion-associated A1 descending neurons. Finally, we develop a genetic reagent to destroy the indirect flight muscles and to facilitate experimental access to the VNC. Taken together, these approaches enable the direct investigation of circuits associated with complex limb movements.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/89093, title ="Multifunctional Wing Motor Control of Song and Flight", author = "O’Sullivan, Angela and Lindsay, Theodore", journal = "Current Biology", volume = "28", number = "17", pages = "2705-2717", month = "September", year = "2018", doi = "10.1016/j.cub.2018.06.038", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180823-135453985", note = "© 2018 Elsevier Ltd. Under an Elsevier user license. \n\nReceived 3 March 2018, Revised 6 June 2018, Accepted 18 June 2018, Available online 23 August 2018. \n\nWe thank Barry Dickson, Carsten Duch, and Stephanie Ryglewski for the gift of split GAL4 lines; Bloomington, VDRC and DGRC stock centers for providing stocks; Begona Arias Lopez for initial work on split GAL4 combinations; Volker Berendes for help with song data analysis; and Duda Kvitsiani, Sophie Seidenbecher, and members of the Philipsborn lab for feedback on the manuscript. Part of this work was supported by a Boehringer Ingelheim Travel Grant to A.O'S., and by the National Science Foundation: USA (grant IOS 1452510 funding T.L.). This study was supported by Lundbeckfonden grant DANDRITE-R248-2016-2518. \n\nAuthor Contributions: A.O., A.P., B.E., and A.C.v.P. conducted experiments. A.O. and A.C.v.P. analyzed the data. T.L. and M.D. provided the live-imaging setup and supported live-imaging experiments. A.C.v.P. and A.O. designed experiments. A.C.v.P. wrote the paper, with input from A.O., T.L., and M.D. \n\nThe authors declare no competing interests.", revision_no = "21", abstract = "Multifunctional motor systems produce distinct output patterns that are dependent on behavioral context, posing a challenge to underlying neuronal control. Flies use their wings for flight and the production of a patterned acoustic signal, the male courtship song, employing in both cases a small set of wing muscles and corresponding motor neurons. We took first steps toward elucidating the neuronal control mechanisms of this multifunctional motor system by live imaging of muscle ensemble activity patterns during song and flight, and we established the functional role of a comprehensive set of wing muscle motor neurons by silencing experiments. Song and flight rely on distinct configurations of neuromuscular activity, with most, but not all, flight muscles and their corresponding motor neurons contributing to song and shaping its acoustic parameters. The two behaviors are exclusive, and the neuronal command for flight overrides the command for song. The neuromodulator octopamine is a candidate for selectively stabilizing flight, but not song motor patterns.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/89297, title ="Sun Navigation Requires Compass Neurons in Drosophila", author = "Giraldo, Ysabel Milton and Leitch, Katherine J.", journal = "Current Biology", volume = "28", number = "17", pages = "2845-2852", month = "September", year = "2018", doi = "10.1016/j.cub.2018.07.002", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180830-084020889", note = "© 2018 Published by Elsevier Ltd. \n\nReceived 6 June 2018, Revised 28 June 2018, Accepted 2 July 2018, Available online 30 August 2018. \n\nWe thank Tanya Wolff and Gerry Rubin for generously providing us with the split-GAL4 lines SS00131 and SS00408 prior to the publication of their manuscript describing them. Crystal Liang and Aisling Murran provided valuable assistance with data collection. This work was funded by grants from the NSF (IOS 1547918), NIH (U19NS104655), and the Simons Foundation (71582123) to M.H.D., as well as an NIH NRSA postdoctoral fellowship (F32GM109777) to Y.M.G. \n\nAuthor Contributions: P.T.W. and T.L.W. were involved in early experimental design and collected preliminary data on sun orientation behavior. Y.M.G., K.J.L., I.G.R., and M.H.D. conceived of and conducted experiments. Y.M.G. characterized sun compass behavior (Figure 1), I.G.R. conducted functional imaging experiments (Figure 2), and Y.M.G. and K.J.L. performed genetic silencing experiments (Figure 3). Y.M.G., K.J.L., I.G.R., and M.H.D. wrote the paper. All authors contributed in editing the final manuscript. \n\nThe authors declare no competing interests.", revision_no = "31", abstract = "Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2, 3, 4, 5, 6, 7, 8, 9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17, 18, 19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights—even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/92506, title ="Flow Structure and Force Generation on Flapping Wings at Low Reynolds Numbers Relevant to the Flight of Tiny Insects", author = "Santhanakrishnan, Arvind and Jones, Shannon K.", journal = "Fluids", volume = "3", number = "3", pages = "Art. No. 45", month = "September", year = "2018", doi = "10.3390/fluids3030045", issn = "2311-5521", url = "https://resolver.caltech.edu/CaltechAUTHORS:20190129-073741342", note = "© 2018 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution\n(CC BY) license (http://creativecommons.org/licenses/by/4.0/). \n\nReceived: 12 May 2018; Accepted: 13 June 2018; Published: 22 June 2018. \n\nWe would like to thank Charles Peskin and Boyce Griffith for their advice on the numerical simulations and the use of IBAMR. We would also like to thank Ty Hedrick for his continued support and assistance with filming thrips and other tiny insects. \n\nThis research was funded by an NSF (IBN-0217229) and DARPA (N00014-98-1-0855) grants to M.H.D, NSF (CBET-1511427) to L.A.M, NSF (CBET-1512071) to A.S., a National Science Foundation Graduate Research Fellowship (NSF GRFP Grant No. DGE-1144081) to S.K.J., and a graduate fellowship from the Statistical and Applied Mathematics Institute to S.K.J. \n\nAuthor Contributions: Conceptualization, L.A.M. and M.H.D.; Methodology, M.H.D., W.B.D., A.S. and L.A.M.; Software, L.A.M., W.B.D., and S.K.J.; Validation S.K.J. and A.S.; Formal Analysis, A.S. and S.K.J.; Investigation, W.B.D., M.P., A.S., V.T.K. and S.K.J.; Resources, M.H.D. and L.A.M.; Data Curation, A.S., V.T.K. and S.K.J.; Writing-Original Draft Preparation, L.A.M., A.S. and S.K.J.; Writing-Review & Editing, L.A.M., M.H.D., S.K.J., and A.S.; Visualization, A.S. and S.K.J.; Supervision, L.A.M. and M.H.D.; Project Administration, L.A.M. and M.H.D.; Funding Acquisition, L.A.M. and M.H.D. \n\nThe authors declare no conflict of interest.", revision_no = "13", abstract = "In contrast to larger species, little is known about the flight of the smallest flying insects, such as thrips and fairyflies. These tiny animals range from 300 to 1000 microns in length and fly at Reynolds numbers ranging from about 4 to 60. Previous work with numerical and physical models have shown that the aerodynamics of these diminutive insects is significantly different from that of larger animals, but most of these studies have relied on two-dimensional approximations. There can, however, be significant differences between two- and three-dimensional flows, as has been found for larger insects. To better understand the flight of the smallest insects, we have performed a systematic study of the forces and flow structures around a three-dimensional revolving elliptical wing. We used both a dynamically scaled physical model and a three-dimensional computational model at Reynolds numbers ranging from 1 to 130 and angles of attacks ranging from 0° to 90°. The results of the physical and computational models were in good agreement and showed that dimensionless drag, aerodynamic efficiency, and spanwise flow all decrease with decreasing Reynolds number. In addition, both the leading and trailing edge vortices remain attached to the wing over the scales relevant to the smallest flying insects. Overall, these observations suggest that there are drastic differences in the aerodynamics of flight at the scale of the smallest flying animals.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/87507, title ="The functional organization of descending sensory-motor pathways in Drosophila", author = "Namiki, Shigehiro and Dickinson, Michael H.", journal = "eLife", volume = "7", pages = "Art. No. e34272", month = "June", year = "2018", doi = "10.7554/eLife.34272", issn = "2050-084X", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180702-085148429", note = "© 2018 Namiki et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. \n\nReceived: 12 December 2017; Accepted: 09 May 2018; Published: 26 June 2018. \n\nWe are grateful to Gerald Rubin and Barry Dickson for providing GAL4 lines, Barett Pfeiffer and Gerry Rubin for constructs used to make the PA-GFP reagent, Julie Simpson, Heather Dionne and Teri Ngo for genetic reagents, Rob Court for initial help setting up the VNC aligner at Janelia and Hideo Otsuna for optimization of the VNC aligner and processing of VNC data, Jana Boerner for segmentation data of VNC bundles. The Janelia Fly facility (Amanda Cavallaro, Todd Laverty, Karen Hibbard, Jui-Chun Kao and others) helped in fly husbandry, and the FlyLight Project Team (https://www.janelia.org/project-team/flylight, Rebecca Johnston, Oz Malkesman, Nirmala Iyer, Kevin Zeng, Kelley Salvesen, Nick Abel, Phuson Hulamm, Reeham Motaher, Susana Tae, Rebecca Vorimo) performed brain dissections, histological preparations, and confocal imaging. We also thank Kei Ito and Masayoshi Ito for sharing information on clonal units, Jens Goldammer and Masayoshi Ito for comments on an early version of the manuscript, and Jim Truman and David Shepherd for helpful discussions on VNC anatomy. We are grateful to the FlyCircuit database from the NCHC (National Center for High-performance Computing) and NTHU (National Tsing Hua University), and to the FLYBRAIN neuron database in the University of Tokyo. This research was partially funded by the Descending Interneuron Project Team (https://www.janelia.org/project-team/fly-descending-interneuron) and the Visiting Scientist Program at The Janelia Research Campus. \n\nFunding: Howard Hughes Medical Institute. \n\nThe funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. \n\nAuthor contributions:\nShigehiro Namiki, Conceptualization, Data curation, Software, Formal analysis, Investigation, Visualization, Methodology, Writing—original draft, Writing—review and editing; Michael H Dickinson, Conceptualization, Visualization, Methodology, Writing—original draft, Writing—review and editing; Allan M Wong, Investigation, Methodology, Data acquisition; Wyatt Korff, Conceptualization, Data curation, Funding acquisition, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing; Gwyneth M Card, Conceptualization, Data curation, Supervision, Funding acquisition, Visualization, Methodology, Writing—original draft, Project administration, Writing—review and editing.", revision_no = "28", abstract = "In most animals, the brain controls the body via a set of descending neurons (DNs) that traverse the neck. DN activity activates, maintains or modulates locomotion and other behaviors. Individual DNs have been well-studied in species from insects to primates, but little is known about overall connectivity patterns across the DN population. We systematically investigated DN anatomy in Drosophila melanogaster and created over 100 transgenic lines targeting individual cell types. We identified roughly half of all Drosophila DNs and comprehensively map connectivity between sensory and motor neuropils in the brain and nerve cord, respectively. We find the nerve cord is a layered system of neuropils reflecting the fly’s capability for two largely independent means of locomotion -- walking and flight -- using distinct sets of appendages. Our results reveal the basic functional map of descending pathways in flies and provide tools for systematic interrogation of neural circuits.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/88483, title ="Flying Drosophila melanogaster maintain arbitrary but stable headings relative to the angle of polarized light", author = "Warren, Timothy L. and Weir, Peter T.", journal = "Journal of Experimental Biology", volume = "221", number = "9", pages = "Art. No. jeb177550", month = "May", year = "2018", doi = "10.1242/jeb.177550", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180801-164035833", note = "© 2018 The Author(s). Published by The Company of Biologists Ltd. \n\nReceived January 16, 2018. Accepted March 19, 2018. \n\nWe thank Nicole Iwasaki for assistance with data collection. \n\nThis work was supported by the National Science Foundation grant IBN-1352707 (to M.H.D.). \n\nAuthor contributions - Conceptualization: T.L.W., P.T.W., M.H.D.; Methodology: T.L.W., P.T.W.; Software: T.L.W., P.T.W.; Validation: T.L.W.; Formal analysis: T.L.W., P.T.W.; Investigation: T.L.W., P.T.W.; Resources: T.L.W.; Data curation: T.L.W.; Writing - original draft: T.L.W., M.H.D.; Writing - review & editing: T.L.W., P.T.W., M.H.D.; Visualization: T.L.W., P.T.W., M.H.D.; Supervision: M.H.D.; Project administration: M.H.D.; Funding acquisition: M.H.D. \n\nData availability: Data are available from the Dryad Digital Repository (Warren et al., 2018): https://doi.org/10.5061/dryad.gj706 \n\nThe authors declare no competing or financial interests.", revision_no = "12", abstract = "Animals must use external cues to maintain a straight course over long distances. In this study, we investigated how the fruit fly Drosophila melanogaster selects and maintains a flight heading relative to the axis of linearly polarized light, a visual cue produced by the atmospheric scattering of sunlight. To track flies' headings over extended periods, we used a flight simulator that coupled the angular velocity of dorsally presented polarized light to the stroke amplitude difference of the animals’ wings. In the simulator, most flies actively maintained a stable heading relative to the axis of polarized light for the duration of 15\u2005min flights. We found that individuals selected arbitrary, unpredictable headings relative to the polarization axis, which demonstrates that D. melanogaster can perform proportional navigation using a polarized light pattern. When flies flew in two consecutive bouts separated by a 5\u2005min gap, the two flight headings were correlated, suggesting individuals retain a memory of their chosen heading. We found that adding a polarized light pattern to a light intensity gradient enhanced flies' orientation ability, suggesting D. melanogaster use a combination of cues to navigate. For both polarized light and intensity cues, flies' capacity to maintain a stable heading gradually increased over several minutes from the onset of flight. Our findings are consistent with a model in which each individual initially orients haphazardly but then settles on a heading which is maintained via a self-reinforcing process. This may be a general dispersal strategy for animals with no target destination.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/85546, title ="Flying Drosophila maintain arbitrary but stable headings relative to the angle of polarized light", author = "Warren, Timothy L. and Weir, Peter T.", journal = "Journal of Experimental Biology", volume = "221", number = "9", pages = "Art. No. jeb177550", month = "May", year = "2018", doi = "10.1242/jeb.177550", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180330-151431169", note = "© 2018 Published by The Company of Biologists Ltd. \n\nReceived 16 January 2018; Accepted 19 March 2018.\n\nPublished 11 May 2018.\n\nWe thank Nicole Iwasaki for assistance with data collection.\n\nCompeting interests:\nThe authors declare no competing or financial interests.\n\nAuthor contributions:\nConceptualization: T.L.W., P.T.W., M.H.D.; Methodology: T.L.W., P.T.W.; Software: T.L.W., P.T.W.; Validation: T.L.W.; Formal analysis: T.L.W., P.T.W.; Investigation: T.L.W., P.T.W.; Resources: T.L.W.; Data curation: T.L.W.; Writing - original draft: T.L.W., M.H.D.; Writing - review & editing: T.L.W., P.T.W., M.H.D.; Visualization: T.L.W., P.T.W., M.H.D.; Supervision: M.H.D.; Project administration: M.H.D.; Funding acquisition: M.H.D.\n\nFunding:\nThis work was supported by the National Science Foundation grant IBN-1352707 (to M.H.D.).\n\nData availability:\nData are available from the Dryad Digital Repository (Warren et al., 2018): https://doi.org/10.5061/dryad.gj706.", revision_no = "17", abstract = "Animals must use external cues to maintain a straight course over long distances. In this study, we investigated how the fruit fly Drosophila melanogaster selects and maintains a flight heading relative to the axis of linearly polarized light, a visual cue produced by the atmospheric scattering of sunlight. To track flies' headings over extended periods, we used a flight simulator that coupled the angular velocity of dorsally presented polarized light to the stroke amplitude difference of the animals’ wings. In the simulator, most flies actively maintained a stable heading relative to the axis of polarized light for the duration of 15\u2005min flights. We found that individuals selected arbitrary, unpredictable headings relative to the polarization axis, which demonstrates that D. melanogaster can perform proportional navigation using a polarized light pattern. When flies flew in two consecutive bouts separated by a 5\u2005min gap, the two flight headings were correlated, suggesting individuals retain a memory of their chosen heading. We found that adding a polarized light pattern to a light intensity gradient enhanced flies' orientation ability, suggesting D. melanogaster use a combination of cues to navigate. For both polarized light and intensity cues, flies' capacity to maintain a stable heading gradually increased over several minutes from the onset of flight. Our findings are consistent with a model in which each individual initially orients haphazardly but then settles on a heading which is maintained via a self-reinforcing process. This may be a general dispersal strategy for animals with no target destination.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/86291, title ="Long-distance navigation of Drosophila melanogaster in the field", author = "Leitch, K. J. and van Breugel, F.", journal = "Integrative and Comparative Biology", volume = "58", number = "S1", pages = "E130", month = "March", year = "2018", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180508-151224245", note = "© 2018 Oxford University Press. \n\nPublished: 08 March 2018.", revision_no = "9", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/86292, title ="Mapping steering muscle activity to 3-dimensional wing kinematics in fruit flies", author = "Melis, J. M. and Lindsay, T.", journal = "Integrative and Comparative Biology", volume = "58", number = "S1", pages = "E152", month = "March", year = "2018", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180508-151329228", note = "© 2018 Oxford University Press. \n\nPublished: 08 March 2018.", revision_no = "7", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/86295, title ="Neural basis of sun-like navigation in Drosophila", author = "Giraldo, Y. M. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "58", number = "S1", pages = "E76", month = "March", year = "2018", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180508-152104550", note = "© 2018 Oxford University Press. \n\nPublished: 08 March 2018.", revision_no = "7", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/86294, title ="Super-hydrophobic diving flies and the kosmotropic waters of Mono Lake", author = "van Breugel, F. and Dickinson, M.", journal = "Integrative and Comparative Biology", volume = "58", number = "S1", pages = "E240", month = "March", year = "2018", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180508-151951814", note = "© 2018 Oxford University Press. \n\nPublished: 08 March 2018.", revision_no = "8", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/86289, title ="Visually-mediated control of Drosophila haltere kinematics modulates mechanosensory input", author = "Dickerson, B. H. and Huda, A.", journal = "Integrative and Comparative Biology", volume = "58", number = "S1", pages = "E51", month = "March", year = "2018", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180508-150645281", note = "© 2018 Oxford University Press. \n\nPublished: 08 March 2018.", revision_no = "9", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/84671, title ="Modulation of Host Learning in Aedes aegypti Mosquitoes", author = "Vinauger, Clément and Lahondère, Chloé", journal = "Current Biology", volume = "28", number = "3", pages = "333-344.e8", month = "February", year = "2018", doi = "10.1016/j.cub.2017.12.015", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180205-093035905", note = "© 2017 Elsevier Ltd. \n\nPublished: January 25, 2018. Accepted: December 7, 2017. Received in revised form: November 7, 2017. Received: September 26, 2017. \n\nWe thank B. Nguyen for mosquito colony maintenance, J. Joiner and K. Moosavi for assistance in olfactometer experiments, J. Stone for help with animal scent collections, and C. Bourgouin and M. Pereira for advice on the RNAi experiments. We thank P. Weir for comments and help with the arena experiments and B. Brunton for statistical advice. We are grateful to D. Dickens for the scanned electron microscope images of Ae. aegypti. We acknowledge the support of the Air Force Office of Sponsored Research under grant FA9550-14-1-0398 and FA9550-16-1-0167 , National Institutes of Health under grant NIH1RO1DCO13693-04 , National Science Foundation under grant IOS-1354159 , UC Riverside, MaxMind, an Endowed Professorship for Excellence in Biology (J.A.R.), the University of Washington Institute for Neuroengineering, and the Human Frontiers in Science Program under grant HFSP-RGP0022 . \n\nAuthor Contributions: C.V., C.L., and J.A.R. conceived the study. C.V. and C.L. participated in the execution and analysis of all aspects of the study. J.A.R. supervised and helped analyze the electrophysiology data presented in Figures 4 and 5. G.H.W. generated and processed the immunohistochemistry data and western blots presented in Figures 5 and S4. L.T.L. and J.E.L. helped carry out and analyze the behavioral assays presented in Figure 1, Figure 2, Figure 3, Figure 4. J.Z.P. helped design the RNAi assays. O.S.A. designed and generated the CRISPR mutant mosquitoes. M.H.D. designed the flight arena experiments presented in Figure 2. C.V., C.L., and J.A.R. wrote the paper, and all authors edited the manuscript. \n\nThe authors declare no competing financial interests.", revision_no = "25", abstract = "How mosquitoes determine which individuals to bite has important epidemiological consequences. This choice is not random; most mosquitoes specialize in one or a few vertebrate host species, and some individuals in a host population are preferred over others. Mosquitoes will also blood feed from other hosts when their preferred is no longer abundant, but the mechanisms mediating these shifts between hosts, and preferences for certain individuals within a host species, remain unclear. Here, we show that olfactory learning may contribute to Aedes aegypti mosquito biting preferences and host shifts. Training and testing to scents of humans and other host species showed that mosquitoes can aversively learn the scent of specific humans and single odorants and learn to avoid the scent of rats (but not chickens). Using pharmacological interventions, RNAi, and CRISPR gene editing, we found that modification of the dopamine-1 receptor suppressed their learning abilities. We further show through combined electrophysiological and behavioral recordings from tethered flying mosquitoes that these odors evoke changes in both behavior and antennal lobe (AL) neuronal responses and that dopamine strongly modulates odor-evoked responses in AL neurons. Not only do these results provide direct experimental evidence that olfactory learning in mosquitoes can play an epidemiological role, but collectively, they also provide neuroanatomical and functional demonstration of the role of dopamine in mediating this learning-induced plasticity, for the first time in a disease vector insect.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/84897, title ="History dependence in insect flight decisions during odor tracking", author = "Pang, Rich and van Breugel, Floris", journal = "PLOS Computational Biology", volume = "14", number = "2", pages = "Art. No. e1005969", month = "February", year = "2018", doi = "10.1371/journal.pcbi.1005969", issn = "1553-7358", url = "https://resolver.caltech.edu/CaltechAUTHORS:20180221-073540732", note = "© 2018 Pang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. \n\nReceived: July 26, 2017; Accepted: January 7, 2018; Published: February 12, 2018. \n\nData Availability Statement: All data files used in this manuscript are publicly available through the Dryad Digital Repository (https://doi.org/10.5061/dryad.n0b8m). Instructions for accessing it through the relevant codebase are given in the code repository landing page on GitHub (https://github.com/rkp8000/wind_tunnel). \n\nThis work was funded by National Institutes of Health (https://www.nih.gov) grant 5R01DC013693-02 (AF, JAR, MD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. \n\nThe authors have declared that no competing interests exist. \n\nAuthor Contributions: \nConceptualization: Rich Pang, Adrienne Fairhall.\nData curation: Floris van Breugel, Michael Dickinson.\nFormal analysis: Rich Pang, Floris van Breugel, Adrienne Fairhall.\nFunding acquisition: Michael Dickinson, Jeffrey A. Riffell, Adrienne Fairhall.\nInvestigation: Rich Pang, Floris van Breugel, Adrienne Fairhall.\nMethodology: Rich Pang, Floris van Breugel.\nProject administration: Rich Pang.\nSoftware: Rich Pang.\nSupervision: Michael Dickinson, Jeffrey A. Riffell, Adrienne Fairhall.\nVisualization: Rich Pang.\nWriting ± original draft: Rich Pang.\nWriting ± review & editing: Rich Pang, Floris van Breugel, Michael Dickinson, Jeffrey A. Riffell,\nAdrienne Fairhall.", revision_no = "33", abstract = "Natural decision-making often involves extended decision sequences in response to variable stimuli with complex structure. As an example, many animals follow odor plumes to locate food sources or mates, but turbulence breaks up the advected odor signal into intermittent filaments and puffs. This scenario provides an opportunity to ask how animals use sparse, instantaneous, and stochastic signal encounters to generate goal-oriented behavioral sequences. Here we examined the trajectories of flying fruit flies (Drosophila melanogaster) and mosquitoes (Aedes aegypti) navigating in controlled plumes of attractive odorants. While it is known that mean odor-triggered flight responses are dominated by upwind turns, individual responses are highly variable. We asked whether deviations from mean responses depended on specific features of odor encounters, and found that odor-triggered turns were slightly but significantly modulated by two features of odor encounters. First, encounters with higher concentrations triggered stronger upwind turns. Second, encounters occurring later in a sequence triggered weaker upwind turns. To contextualize the latter history dependence theoretically, we examined trajectories simulated from three normative tracking strategies. We found that neither a purely reactive strategy nor a strategy in which the tracker learned the plume centerline over time captured the observed history dependence. In contrast, “infotaxis”, in which flight decisions maximized expected information gain about source location, exhibited a history dependence aligned in sign with the data, though much larger in magnitude. These findings suggest that while true plume tracking is dominated by a reactive odor response it might also involve a history-dependent modulation of responses consistent with the accumulation of information about a source over multi-encounter timescales. This suggests that short-term memory processes modulating decision sequences may play a role in natural plume tracking.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/83384, title ="Superhydrophobic diving flies (Ephydra hians) and the hypersaline waters of Mono Lake", author = "van Breugel, Floris and Dickinson, Michael H.", journal = "Proceedings of the National Academy of Sciences of the United States of America", volume = "114", number = "51", pages = "13483-13488", month = "December", year = "2017", doi = "10.1073/pnas.1714874114 ", issn = "0027-8424", url = "https://resolver.caltech.edu/CaltechAUTHORS:20171121-074702875", note = "© 2017 National Academy of Sciences. Published under the PNAS license. \n\nEdited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved October 18, 2017 (received for review August 22, 2017). Published online before print November 20, 2017. \n\nWe thank Jocelyn Millar, who generously performed the GC-MS analysis in this paper and provided valuable feedback on hydrocarbon chemistry; Rob Phillips, who also provided helpful comments on the manuscript; Dave Marquart, who helped procure necessary permits; Aisling Farrell, who helped collect Helaeomyia petrolei from the La Brea Tar Pits; and Victoria Orphan and Sean Mullin, who helped prepare SEM specimens. This work was supported by the National Geographic Society’s Committee for Research and Exploration, Grant 9645-15. \n\nAuthor contributions: F.v.B. and M.H.D. designed research; F.v.B. and M.H.D. performed research; F.v.B. and M.H.D. contributed new reagents/analytic tools; F.v.B. analyzed data; and F.v.B. and M.H.D. wrote the paper. \n\nThe authors declare no conflict of interest. \n\nThis article is a PNAS Direct Submission. \n\nData deposition: All data in the manuscript have been uploaded to Github (https://github.com/florisvb/alkali_flies_of_mono_lake) and Open Science Framework (https://osf.io/43yhs/). \n\nThis article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1714874114/-/DCSupplemental.", revision_no = "44", abstract = "The remarkable alkali fly, Ephydra hians, deliberately crawls into the alkaline waters of Mono Lake to feed and lay eggs. These diving flies are protected by an air bubble that forms around their superhydrophobic cuticle upon entering the lake. To study the physical mechanisms underlying this process we measured the work required for flies to enter and leave various aqueous solutions. Our measurements show that it is more difficult for the flies to escape from Mono Lake water than from fresh water, due to the high concentration of Na_2CO_3 which causes water to penetrate and thus wet their setose cuticle. Other less kosmotropic salts do not have this effect, suggesting that the phenomenon is governed by Hofmeister effects as well as specific interactions between ion pairs. These effects likely create a small negative charge at the air–water interface, generating an electric double layer that facilitates wetting. Compared with six other species of flies, alkali flies are better able to resist wetting in a 0.5 M Na_2CO_3 solution. This trait arises from a combination of factors including a denser layer of setae on their cuticle and the prevalence of smaller cuticular hydrocarbons compared with other species. Although superbly adapted to resisting wetting, alkali flies are vulnerable to getting stuck in natural and artificial oils, including dimethicone, a common ingredient in sunscreen and other cosmetics. Mono Lake’s alkali flies are a compelling example of how the evolution of picoscale physical and chemical changes can allow an animal to occupy an entirely new ecological niche.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/83485, title ="Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds", author = "Goller, Benjamin and Segre, Paolo S.", journal = "Frontiers in Neuroscience", volume = "11", pages = "Art. No. 622", month = "November", year = "2017", doi = "10.3389/fnins.2017.00622", issn = "1662-453X", url = "https://resolver.caltech.edu/CaltechAUTHORS:20171128-082956969", note = "© 2017 Goller, Segre, Middleton, Dickinson and Altshuler. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. \n\nReceived: 29 June 2017; Accepted: 25 October 2017; Published: 14 November 2017. \n\nEthics Statement: This study was carried out in accordance with the recommendations of US federal regulations and the Guide for the Care and Use of Laboratory Animals, as well as the Canadian Council on Animal Care. The protocol was approved by the Institutional Animal Care and Use Committee of the California Institute of Technology and the Animal Care and Use Committee at the University of British Columbia. \n\nAuthor Contributions: BG, MD, and DA conceived and designed the experiments. BG and DA collected the data. BG, PS, KM, and DA analyzed the data and wrote the manuscript. All authors edited the manuscript. \n\nFunding: This study was supported by grants from the Natural Science and Engineering Research Council of Canada (402667, RGPIN-2016-05381) and the Human Frontier Science Program (RGP0003/2013). \n\nConflict of Interest Statement: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. \n\nAcknowledgments: We thank Bobby Chi, Lev Darkhovsky, Amy Lin, Annie Liu, and Jonathon Scott for assistance with data collection or digitization of wingbeat kinematics. We also thank Joseph Bahlman, Will Dickson, Phil Matthews, Ken Savage, and Bob Shadwick for providing technical support for the experiments. Finally, we would like to acknowledge the two reviewers for providing comments that greatly improved the manuscript.", revision_no = "13", abstract = "Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios—one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/79324, title ="Idiothetic Path Integration in the Fruit Fly Drosophila melanogaster", author = "Kim, Irene S. and Dickinson, Michael H.", journal = "Current Biology", volume = "27", number = "15", pages = "2227-2238", month = "August", year = "2017", doi = "10.1016/j.cub.2017.06.026", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170725-092327425", note = "© 2017 Elsevier Ltd. \n\nReceived 18 April 2017, Revised 26 May 2017, Accepted 9 June 2017, Available online 20 July 2017. Published: July 20, 2017. \n\nWe wish to thank Christie Huang for help with conducting these experiments, and Steve Safarik for developing our tracking software. Joel Levine kindly provided us with flies. John Tuthill, Rachel Wilson, Pavan Ramdya, and Paul Graham provided valuable feedback on this manuscript. This work was supported by the Human Frontiers of Science Program (grant RGP0022/2012) and National Institute of Neurological Disorders and Stroke of the NIH (award U01NS090514). \n\nAuthor Contributions: Conceptualization, I.S.K. and M.H.D.; Methodology, I.S.K. and M.H.D.; Investigation, I.S.K.; Formal Analysis, I.S.K.; Writing, I.S.K. and M.H.D.; Funding Acquisition, M.H.D.; Supervision, M.H.D.", revision_no = "34", abstract = "After discovering a small drop of food, hungry flies exhibit a peculiar behavior in which they repeatedly stray from, but then return to, the newly discovered resource. To study this behavior in more detail, we tracked hungry Drosophila as they explored a large arena, focusing on the question of how flies remain near the food. To determine whether flies use external stimuli, we individually eliminated visual, olfactory, and pheromonal cues. In all cases, flies still exhibited a centralized search behavior, suggesting that none of these cues are absolutely required for navigation back to the food. To simultaneously eliminate visual and olfactory cues associated with the position of the food, we constructed an apparatus in which the food could be rapidly translated from the center of the arena. Flies continued to search around the original location, even after the food was moved to a new position. A random search model based on measured locomotor statistics could not reproduce the centered nature of the animal’s trajectory. We conclude that this behavior is best explained by a form of path integration in which the flies use idiothetic cues to search near the location of the food. We argue that the use of path integration to perform a centered local search is not a specialization of Drosophila but rather represents an ancient behavioral mode that is homologous to the more elaborate foraging strategies of central place foragers such as ants.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/76499, title ="A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila", author = "Schnell, Bettina and Ros, Ivo G.", journal = "Current Biology", volume = "27", number = "8", pages = "1200-1205", month = "April", year = "2017", doi = "10.1016/j.cub.2017.03.004", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170411-082920130", note = "© 2017 Elsevier Ltd. \n\nReceived 26 August 2016, Revised 19 January 2017, Accepted 2 March 2017, Available online 6 April 2017Published: April 6, 2017. \n\nWe would like to thank Ainul Huda and Peter Weir for the image of the R56G08-Gal4 line; Shigehiro Namiki for information about Gal4 lines labeling descending neurons; and Gaby Maimon, Theodore Lindsay, and Peter Weir for comments on the manuscript. This work was supported by the Raymond and Beverly Sackler Foundation (B.S.), the Paul G. Allen Family Foundation (M.H.D.), and the National Institute of Neurological Disorders and Stroke of the NIH under award U01NS090514 (M.H.D). The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH. \n\nAuthor Contributions: Conceptualization, B.S. and M.H.D.; Methodology, B.S. and I.G.R.; Investigation, B.S. and I.G.R.; Formal Analysis, B.S. and I.G.R.; Writing – Original Draft, B.S. and M.H.D.; Writing – Review & Editing, B.S., I.G.R., and M.H.D.; Funding Acquisition, B.S. and M.H.D.; Supervision, M.H.D. \n\nAccession Numbers: Data reported in this manuscript have been deposited at the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.n7v41.", revision_no = "34", abstract = "To navigate through the world, animals must stabilize their path against disturbances and change direction to avoid obstacles and to search for resources [1 ; 2]. Locomotion is thus guided by sensory cues but also depends on intrinsic processes, such as motivation and physiological state. Flies, for example, turn with the direction of large-field rotatory motion, an optomotor reflex that is thought to help them fly straight [3; 4 ; 5]. Occasionally, however, they execute fast turns, called body saccades, either spontaneously or in response to patterns of visual motion such as expansion [6; 7 ; 8]. These turns can be measured in tethered flying Drosophila [ 3; 4 ; 9], which facilitates the study of underlying neural mechanisms. Whereas there is evidence for an efference copy input to visual interneurons during saccades [10], the circuits that control spontaneous and visually elicited saccades are not well known. Using two-photon calcium imaging and electrophysiological recordings in tethered flying Drosophila, we have identified a descending neuron whose activity is correlated with both spontaneous and visually elicited turns during tethered flight. The cell’s activity in open- and closed-loop experiments suggests that it does not underlie slower compensatory responses to horizontal motion but rather controls rapid changes in flight path. The activity of this neuron can explain some of the behavioral variability observed in response to visual motion and appears sufficient for eliciting turns when artificially activated. This work provides an entry point into studying the circuits underlying the control of rapid steering maneuvers in the fly brain.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/77602, title ="Celestial Navigation in Drosophila", author = "Giraldo, Y. M. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "57", number = "S1", pages = "E273", month = "March", year = "2017", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170519-124714969", note = "© 2017 Oxford University Press.", revision_no = "9", abstract = "Insects exhibit impressive navigational abilities, from long distance migrations of monarch butterflies to path integration of desert ants in the genus Cataglyphis. Celestial cues — including polarized light and solar position — provide valuable information to navigating insects, and the brain regions that process this information appear largely conserved. Although not generally considered migratory, mark-recapture experiments indicate that Drosophila can cover 10 km of open desert in perhaps as little as a few hours without stopping\nto refuel. This impressive feat required flies to adopt a fairly straight path, likely accomplished by visually-guided navigation using celestial cues. Like many insects Drosophila possess the ability to navigate using the polarization pattern of skylight but sun-compass navigation in this genus has not been examined. Using a flight simulator with machine-vision wing tracking, we found that tethered D. melanogaster can use the position of a simulated sun to fly straight, and individuals vary in their heading preference. This preferred heading is maintained over short intervals, but fidelity decays as the time between flights is increased. By training flies with a stimulus restricted to one half of the arena, we could bias subsequent headings towards the side of the training stimulus. These findings suggest that flight and/or visual experience can influence heading, although the neural basis remains unknown. Drosophila sun compass navigation has the potential for future behavioral, ecological and neurobiological studies that could shed light on the deep evolutionary roots of visually-guided locomotion.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/77567, title ="Drosophila haltere steering muscles are active during voluntary maneuvers and are directionally tuned", author = "Dickerson, B. H. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "57", number = "S1", pages = "E245", month = "March", year = "2017", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170518-103008787", note = "© 2017 Oxford University Press.\n", revision_no = "15", abstract = "As flies navigate their environment in search of food or mates, they execute sharp turns known as saccades that occur faster than the blink of a human eye. These maneuvers are initiated by changes in visual motion detected by the eyes, whereas their termination is under the control of small, dumbbell-shaped structures called halteres. The halteres are located behind the forewings and evolved from the hindwings. These structures oscillate during flight and function as biological gyroscopes; they detect unexpected body rotations during flight and trigger wing reflex maneuvers. Like the wings, the halteres possess a small set of muscles that control the structure’s motion from their base and receive input from the visual system. However, while the critical role of the halteres in stabilizing flight is long known as flies crash catastrophically without them, the role of the haltere and its steering muscles during flight maneuvers remains unclear. Using fluorescence imaging of the genetically encoded calcium sensor GCaMP6f, we observed haltere steering muscle activity in the fruit fly, Drosophila melanogaster, during a broad array of visual stimuli. We found that these muscles are particularly responsive during voluntary escape maneuvers and are tuned to rotations about the body’s cardinal axes. These results suggest that the visual system is able to activate individual muscles to control haltere motion, and thus mechanosensory input. With this work, we are beginning to understand how hard-wired reflexes may be modified by the nervous system to produce voluntary behaviors.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/77603, title ="Optimal search with unreliable and dangerous cues", author = "van Breugel, F. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "57", number = "S1", pages = "E435", month = "March", year = "2017", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170519-125008803", note = "© 2017 Oxford University Press.", revision_no = "11", abstract = "Carbon dioxide is a broad signal of molecular decay, and it is almost universally attractive among insects in search of hosts, wildfires, flowers, decaying matter, communal nests, predators, and fruit. CO_2 is also, however, toxic at naturally occurring high concentrations. It is not clear how insects balance the information provided by this\nbroad and dangerous signal with the information provided by odors that are more unique to their respective niches. This particular challenge is an example of a common dilemma that all animals face. To address this question, we studied how fruit flies balance the value of information provided by CO_2 and ethanol, both important odors produced during fermentation, their primary food source. We found\nthat flies exhibit similar attractive responses towards CO_2 as they do towards ethanol, however, they invest twice as much time in searching near sources of ethanol. To understand what these differences in search times might mean in terms of their ecology, we simulated different virtual ecosystems and found that their strategy is\noptimized for scenarios where CO_2 and ethanol correspond to 30% and 70% chances of finding food, respectively. Our simulations extend beyond this particular case study by providing a plausible explanation for why experimental observations so often do not agree with predictions of optimal foraging theory and the marginal value theorem. Curiously, our result that flies find CO_2 attractive runs contrary to the majority of the scientific literature, which has suggested that flies find CO_2 aversive. In our experiments, we did find that flies occasionally do find CO_2 aversive, but only during times of low activity. This could be an adaptation to reduce the chances of falling prey to parasites or lethal concentrations of CO_2.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/74247, title ="Flies compensate for unilateral wing damage through modular adjustments of wing and body kinematics", author = "Muijres, Florian T. and Iwasaki, Nicole A.", journal = "Interface Focus", volume = "7", number = "1", pages = "Art. No. 20160103", month = "February", year = "2017", doi = "10.1098/rsfs.2016.0103", issn = "2042-8898", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170213-124118184", note = "© 2016 The Author(s). Published by the Royal Society. \n\nOne contribution of 19 to a theme issue ‘Coevolving advances in animal flight and aerial robotics’. \n\nThis work was supported by grants (to F.T.M.) from the Netherlands Organization for Scientific Research, NWO-VENI-863-14-007 (to M.H.D.), the Air Force Office of Scientific Research (FA9550-10-1-0368) and the Paul G. Allen Family Foundation. \n\nAuthors' contributions: M.H.D. and F.T.M. designed the experiment and wrote the paper; N.A.I. performed the fruit fly experiments; M.J.E. performed the robotic fly experiments; J.M.M. developed the quasi-steady aerodynamic model. F.T.M. performed the data analysis. \n\nWe declare we have no competing interests.", revision_no = "29", abstract = "Using high-speed videography, we investigated how fruit flies compensate for unilateral wing damage, in which loss of area on one wing compromises both weight support and roll torque equilibrium. Our results show that flies control for unilateral damage by rolling their body towards the damaged wing and by adjusting the kinematics of both the intact and damaged wings. To compensate for the reduction in vertical lift force due to damage, flies elevate wingbeat frequency. Because this rise in frequency increases the flapping velocity of both wings, it has the undesired consequence of further increasing roll torque. To compensate for this effect, flies increase the stroke amplitude and advance the timing of pronation and supination of the damaged wing, while making the opposite adjustments on the intact wing. The resulting increase in force on the damaged wing and decrease in force on the intact wing function to maintain zero net roll torque. However, the bilaterally asymmetrical pattern of wing motion generates a finite lateral force, which flies balance by maintaining a constant body roll angle. Based on these results and additional experiments using a dynamically scaled robotic fly, we propose a simple bioinspired control algorithm for asymmetric wing damage.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/73761, title ="The Function and Organization of the Motor System Controlling Flight Maneuvers in Flies", author = "Lindsay, Theodore and Sustar, Anne", journal = "Current Biology", volume = "27", number = "3", pages = "345-358", month = "February", year = "2017", doi = "10.1016/j.cub.2016.12.018", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20170126-154336284", note = "© 2016 Elsevier Ltd. \n\nReceived 18 October 2016, Revised 6 December 2016, Accepted 8 December 2016, Available online 26 January 2017, Published: January 26, 2017. \n\nWe would like to thank Peter Weir for suggesting several insightful analyses. This work was supported by a grant from the National Science Foundation (IOS 1452510). \n\nAuthor Contributions: Conceptualization, M.D. and T.L.; Methodology, T.L., M.D., and A.S.; Investigation, T.L. and A.S.; Writing – Original Draft, T.L. and M.D.; Writing – Review & Editing, T.L., M.D., and A.S.; Funding Acquisition, M.D.; Resources, M.D.; Supervision, M.D. \n\nAccession Numbers: The accession number for the data reported in this paper is Dryad: http://dx.doi.org/10.5061/dryad.23nm1.", revision_no = "24", abstract = "Animals face the daunting task of controlling their limbs using a small set of highly constrained actuators. This problem is particularly demanding for insects such as Drosophila, which must adjust wing motion for both quick voluntary maneuvers and slow compensatory reflexes using only a dozen pairs of muscles. To identify strategies by which animals execute precise actions using sparse motor networks, we imaged the activity of a complete ensemble of wing control muscles in intact, flying flies. Our experiments uncovered a remarkably efficient logic in which each of the four skeletal elements at the base of the wing are equipped with both large phasically active muscles capable of executing large changes and smaller tonically active muscles specialized for continuous fine-scaled adjustments. Based on the responses to a broad panel of visual motion stimuli, we have developed a model by which the motor array regulates aerodynamically functional features of wing motion.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/72183, title ="An Array of Descending Visual Interneurons Encoding Self-Motion in Drosophila", author = "Suver, Marie P. and Huda, Ainul", journal = "Journal of Neuroscience", volume = "36", number = "46", pages = "11768-11780", month = "November", year = "2016", doi = "10.1523/JNEUROSCI.2277-16.2016", issn = "0270-6474", url = "https://resolver.caltech.edu/CaltechAUTHORS:20161121-082027280", note = "© 2016 the authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). \n\nReceived July 13, 2016; revised Sept. 22, 2016; accepted Sept. 24, 2016.\n\nThis work was supported by the National Institute of Neurological Disorders and Stroke–National Institutes of Health (Grant U01NS090514 to M.H.D.) and the Paul G. Allen Family Foundation (M.H.D.). We thank Anne Sustar for assistance with fly stocks; Allan Wong for guidance with the photoactivatible GFP technique; Gwyneth Card and Shigehiro Namiki for useful discussions about the descending interneurons; and Katherine Nagel and Peter Weir for helpful comments on the manuscript. \n\nAuthor contributions: M.P.S. and M.H.D. designed research; M.P.S., A.H., and N.I. performed research; S.S. contributed unpublished reagents/analytic tools; M.P.S. analyzed data; M.P.S. and M.H.D. wrote the paper. \n\nThe authors declare no competing financial interests.", revision_no = "16", abstract = "The means by which brains transform sensory information into coherent motor actions is poorly understood. In flies, a relatively small set of descending interneurons are responsible for conveying sensory information and higher-order commands from the brain to motor circuits in the ventral nerve cord. Here, we describe three pairs of genetically identified descending interneurons that integrate information from wide-field visual interneurons and project directly to motor centers controlling flight behavior. We measured the physiological responses of these three cells during flight and found that they respond maximally to visual movement corresponding to rotation around three distinct body axes. After characterizing the tuning properties of an array of nine putative upstream visual interneurons, we show that simple linear combinations of their outputs can predict the responses of the three descending cells. Last, we developed a machine vision-tracking system that allows us to monitor multiple motor systems simultaneously and found that each visual descending interneuron class is correlated with a discrete set of motor programs.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/69806, title ="The aerodynamics and control of free flight manoeuvres in Drosophila", author = "Dickinson, Michael H. and Muijres, Florian T.", journal = "Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences", volume = "371", number = "1704", pages = "Art. No. 20150388", month = "September", year = "2016", doi = "10.1098/rstb.2015.0388", issn = "0962-8436", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160822-083650699", note = "© 2016 The Author(s). Published by the Royal Society. \n\nAccepted: 18 March 2016; Published 15 August 2016. \n\nAuthors’ contributions: Both authors wrote the paper. \n\nCompeting interests. The authors have no confliction interests.\n\nThis work was supported by grants from the Netherlands Organization for Scientific Research, NWO-VENI-863-14-007 (F.T.M.), and the National Science Foundation, IOS 1452510 (M.H.D.).\n\nWe wish to dedicate this paper to Charles David (1948–2012) and Steven Vogel (1940–2015), two pioneers of research on Drosophila aerodynamics and flight control. We thank the following individuals for helpful comments on this manuscript: Brad Dickerson, Thad Lindsay, Floris van Breugel, Sawyer Fuller, Johan Melis and Ivo Ros.", revision_no = "11", abstract = "A firm understanding of how fruit flies hover has emerged over the past two decades, and recent work has focused on the aerodynamic, biomechanical and neurobiological mechanisms that enable them to manoeuvre and resist perturbations. In this review, we describe how flies manipulate wing movement to control their body motion during active manoeuvres, and how these actions are regulated by sensory feedback. We also discuss how the application of control theory is providing new insight into the logic and structure of the circuitry that underlies flight stability.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/70719, title ="Generalized regressive motion: a visual cue to collision", author = "Chalupka, Krzysztof and Dickinson, Michael", journal = "Bioinspiration and Biomimetics", volume = "11", number = "4", pages = "Art. No. 046008", month = "August", year = "2016", doi = "10.1088/1748-3190/11/4/046008", issn = "1748-3182", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160930-145713133", note = "© 2016 IOP Publishing. Original content from this work may be used under the terms of the Creative Commons Attribution 3.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI. \n\nReceived 17 November 2015; Accepted 7 June 2016; Published 18 July 2016. \n\nWe thank the anonymous reviewers for excellent pointers to relevant literature. This work was supported by National Science Foundation grants 0914783 and 1216045, NASA Stennis grant NAS7.03001 and ONR MURI grant N00014-10-1-0933.", revision_no = "22", abstract = "Brains and sensory systems evolved to guide motion. Central to this task is controlling the approach to stationary obstacles and detecting moving organisms. Looming has been proposed as the main monocular visual cue for detecting the approach of other animals and avoiding collisions with stationary obstacles. Elegant neural mechanisms for looming detection have been found in the brain of insects and vertebrates. However, looming has not been analyzed in the context of collisions between two moving animals. We propose an alternative strategy, generalized regressive motion (GRM), which is consistent with recently observed behavior in fruit flies. Geometric analysis proves that GRM is a reliable cue to collision among conspecifics, whereas agent-based modeling suggests that GRM is a better cue than looming as a means to detect approach, prevent collisions and maintain mobility.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/67149, title ="Anatomical Reconstruction and Functional Imaging Reveal an Ordered Array of Skylight Polarization Detectors in Drosophila", author = "Weir, Peter T. and Henze, Miriam J.", journal = "Journal of Neuroscience", volume = "36", number = "19", pages = "5397-5404", month = "May", year = "2016", doi = "10.1523/JNEUROSCI.0310-16.2016", issn = "0270-6474", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160517-082346810", note = "© 2016 the authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). \n\nReceived January 27, 2016. Revision received April 4, 2016. Accepted April 6, 2016. \n\nThis work was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award U01NS090514 (M.H.D.), the National Science Foundation under Grant No. 1352707 (M.H.D.), the Paul G. Allen Family Foundation (M.H.D.), and the German National Merit Foundation (Studienstiftung des deutschen Volkes; M.J.H.). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. We thank S. Sommer and J. Smolka for advice on statistics, M. Wernet for providing prh1-eGFP transgenic flies, B. Schnell for valuable discussions, and two anonymous reviewers for constructive comments. \n\nThe authors declare no competing financial interests.", revision_no = "12", abstract = "Many insects exploit skylight polarization as a compass cue for orientation and navigation. In the fruit fly, Drosophila melanogaster, photoreceptors R7 and R8 in the dorsal rim area (DRA) of the compound eye are specialized to detect the electric vector (e-vector) of linearly polarized light. These photoreceptors are arranged in stacked pairs with identical fields of view and spectral sensitivities, but mutually orthogonal microvillar orientations. As in larger flies, we found that the microvillar orientation of the distal photoreceptor R7 changes in a fan-like fashion along the DRA. This anatomical arrangement suggests that the DRA constitutes a detector for skylight polarization, in which different e-vectors maximally excite different positions in the array. To test our hypothesis, we measured responses to polarized light of varying e-vector angles in the terminals of R7/8 cells using genetically encoded calcium indicators. Our data confirm a progression of preferred e-vector angles from anterior to posterior in the DRA, and a strict orthogonality between the e-vector preferences of paired R7/8 cells. We observed decreased activity in photoreceptors in response to flashes of light polarized orthogonally to their preferred e-vector angle, suggesting reciprocal inhibition between photoreceptors in the same medullar column, which may serve to increase polarization contrast. Together, our results indicate that the polarization-vision system relies on a spatial map of preferred e-vector angles at the earliest stage of sensory processing.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/66446, title ="Burst muscle performance predicts the speed, acceleration, and turning performance of hummingbirds", author = "Segre, P. S. and Dakin, R.", journal = "Integrative and Comparative Biology", volume = "56", number = "S1", pages = "E198", month = "March", year = "2016", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160425-104937171", note = "© 2016 Oxford University Press.", revision_no = "11", abstract = "Despite recent advances in our understanding of animal flight, the\nbiomechanical determinants of maneuverability in birds are poorly\nunderstood. It is thought that maneuverability is influenced by\nmorphological features such as body mass, wing size, and wing\nshape, as well as by physiological traits such as muscle capacity. This\nhypothesis has not been evaluated for any animal because large\nnumbers of measurements of free flight maneuvers from the same\nindividuals have been lacking. We recorded a large number of flight\nsequences for 20 Anna's hummingbirds (Calypte anna) in a flight\nchamber to determine if an individual's maneuvering performance is\n1) repeatable across trials, 2) associated with morphology, burst\nmuscle capacity, or both, and 3) influenced by the presence of a\ncompetitor. Using a multi-camera tracking system, we analyzed\nperformance metrics based on body position and orientation. Most\nmeasures were highly repeatable. Burst muscle capacity was\nassociated with most performance metrics, such that birds with\nhigher burst capacity flew with faster velocities, accelerations, and\nrotations, and performed more demanding complex turns. Wing\nmorphology predicted only a few performance metrics, such that\nbirds with higher wing aspect ratio had higher centripetal\nacceleration and performed more arcing turns. In the presence of a\ncompetitor, birds exhibited faster changes in pitch and altered the\ntypes of complex turns used, but surprisingly, they had lower\nhorizontal accelerations. Collectively, these results indicate that burst\nmuscle capacity is a key predictor of maneuverability, and that body\nangular velocity and arcing turns are associated with competition in\nflight.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/66452, title ="Functional imaging from the muscles of the fruit fly wing-hinge during tethered flight", author = "Lindsay, T. H. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "56", number = "S1", pages = "E128", month = "March", year = "2016", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160425-130913017", note = "© 2016 Oxford University Press.", revision_no = "11", abstract = "Animal movement emerges from a system of inner and\nouter-feedback loops by which sensory information directs and\nstabilizes motor output. Compared to our knowledge of coding\nwithin sensory systems, our understanding of how motor codes\nproduce locomotion remains poorly understood. The agile aerial\nbehaviors of flies present a prime example of this problem: using\nsubtle changes in wing kinematics, flies respond to visual input and\nexecute hairpin turns in milliseconds. Although flies are equipped\nwith relatively few muscles with which to regulate wing motion, they\nnevertheless execute very precise maneuvers. As in other flies, in the\nfruit fly, Drosophila melanogaster, the 15 tiny control muscles of\neach wing are anatomically grouped according to the skeletal\nelements within the wing hinge on which they insert: the first, third,\nand fourth axillary sclerites and the basalare. Prior studies have\nrecorded the activation of a small subset of these muscles during\nflight behaviors using fine metal electrodes however, the activity of\nthe entire population has not been observed due the small size of\nmost muscles and their complex overlapping pattern of insertion. To\novercome these limitations, we expressed a genetically-encoded\ncalcium indicator (GCaMP6f) in the steering muscles of Drosophila,\nand imaged their activity through the intact thorax of tethered, flying\nflies. During flight, activity was distributed broadly across the entire\npopulation of steering muscles. By presenting the flies with a set of\nlarge field visual motion, we have begun to map the tuning of\nindividual muscles and muscle groups to the control of body\ntranslation and rotation during flight.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/66453, title ="Influence of female orientation and pigmentation on male positioning during courtship", author = "Agrawal, S. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "56", number = "S1", pages = "E3", month = "March", year = "2016", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160425-131150570", note = "© 2016 Oxford University Press.", revision_no = "10", abstract = "Despite its emergence as a premier model for visual processing, little\nis known about object recognition in Drosophila. One possible\nexplanation for this deficit is that Drosophila do not display\nbehaviors typically associated with exemplary feats of object\nrecognition, like the flower shape memory exhibited by bees. In\naddition, Drosophila eyes provide poor spatial resolution.\nNevertheless, visual object recognition may be important during\ncourtship. Because courtship occurs at a very close distance, flies\ncould distinguish fine-scale pigmentation patterns. At a greater\ndistance, a chasing male would have access to cues such as shape,\nsize, and patterns of motion. To understand how courting male flies\nuse vision, we developed a behavioral apparatus, dubbed \"Flyatar,\"\nconsisting of a remotely actuated fly dummy. We can modify the\ndummy's appearance, pattern of motion, and pheromone coating.\nMales will robustly court the dummy, enabling us to delineate the\nrelative contributions of visual and other sensory cues to male\ncourtship behavior. We are using Flyatar to examine how a male uses\nvision and chemosensation to position its body during chases. To\nhave a chance at successful copulation, a male must position itself\nappropriately around the female. Male flies preferentially bias their\nchasing towards the female's abdomen, irrespective of her body\norientation and direction of movement. This preference is maintained\ntowards females that have been genetically altered to not produce\npheromones, suggesting that males can distinguish different parts of\nthe female body using vision alone. In addition, males demonstrate a\npreference for chasing objects painted specific shades, and are not\nstrongly attracted towards very dark or very light objects. These\nresults suggest that, though simple, visual object recognition\nnevertheless plays an important role in courtship behavior.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/66444, title ="Mysterious diving flies of Mono Lake", author = "van Breugel, F. and Dickinson, M.", journal = "Integrative and Comparative Biology", volume = "56", number = "S1", pages = "E227", month = "March", year = "2016", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160425-104056580", note = "© 2016 Oxford University Press.", revision_no = "11", abstract = "In late summer, the shores of Mono Lake, California, are bustling\nwith small flies, Ephydra hydropyrus, which dive under water inside\nsmall air bubbles to feed. After returning to the surface, the flies pop\nout of the highly alkaline water and fly away completely dry. Despite\nMark Twain's charismatic description of them in 1872 , we still do\nnot understand how these tiny flies are able to perform this\nremarkable feat. We have begun to probe the underlying biophysics\nof this phenomenon using a combination of highspeed video, micro\nforce measurements, and simple surface chemistry manipulations.\nLike many insects, Ephydra are covered in waxy coatings and small\nwater repellent hairs. This adaptation allows insects such as the water\nstrider to glide across the surface of ponds by floating on cushions of\nair trapped by microscopic hairs on their legs. In order to crawl\nunderwater, however, Ephydra must overcome these strong surface\ntension forces that are 10-20 times their body weight. Specially\nadapted claws on their tarsi allow them to crawl through the air-water\ninterface on the surface of Mono Lake's tufa formations. Once\nsatiated and ready to return to the air, they must come free of the\nwater without wetting their wings, which would attach them\nhelplessly to the water surface where they would quickly succumb to\npredation. Here, the high surface tension forces help them escape the\nwater by gently catapulting the flies free of the surface so they can\nsafely take flight. Making a safe exit, however, requires that they\nbreak their bubble right side up, which they accomplish through\nactively controlling their ascent with their legs. In addition to\nunderstanding the most critical adaptation of this key species,\ndetermining the physics underlying their behavior may find\napplications in waterproofing materials and amphibious technologies.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/66445, title ="Sensory integration by descending interneurons in the flying fruit fly", author = "Suver, M. P. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "56", number = "S1", pages = "E216", month = "March", year = "2016", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20160425-104558133", note = "© 2016 Oxford University Press.", revision_no = "12", abstract = "A flying fly relies on many senses, including vision, olfaction, and\nmechanosensation, to navigate through the world and locate an\nattractive food source. How are these sensory signals integrated in\nthe central brain and relayed to the motor system to guide behavior?\nIntegration of multiple sensory signals can be performed by\ndescending interneurons, which relay this information to motor\nsystems via circuits in the thoracic ganglion. We have identified a\ngroup of three descending interneurons in the fruit fly that integrate\ninformation from discrete sets of visual interneurons. Each exhibits a\ndistinct preference for optic flow corresponding to self-motion. We\nmeasured the tuning properties of the presynaptic visual interneurons,\nand found that a simple linear model based on these inputs can\nexplain much of the response of the descending interneurons.\nProjection patterns of the three descending interneurons in the\nthoracic ganglion suggest that they deliver self-motion information to\ncircuits that control movement of the head, wings, and abdomen. We\nmonitored the output of these motor systems during tethered flight\nand found evidence that suggests that these three neurons are\ninvolved in distinct motor programs. This circuit may play a crucial\nrole in sensory-motor tranformations used to guide stable flight, and\nprovides insight into strategies employed by other flying insects.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/62329, title ="Burst muscle performance predicts the speed, acceleration, and turning performance of Anna's hummingbirds", author = "Segre, Paolo S. and Dakin, Roslyn", journal = "eLife", volume = "4", pages = "Art. No. 11159", month = "November", year = "2015", doi = "10.7554/eLife.11159", issn = "2050-084X", url = "https://resolver.caltech.edu/CaltechAUTHORS:20151123-105843576", note = "© 2015, Segre et al. This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited. \n\nReceived: 27 August 2015; Accepted: 13 November 2015; Published: 19 November 2015. \n\nAdam Behroozian and Tyson Read assisted with data collection. Tungesh Kapil, Janet Li, Sachiko Ouchi, Jordan Roth, Sorosh Safa, Humraaz Samra, Nandhini Sankhyan, Tom Tsou, Sherry Young, Bo Zhang assisted with behavioral scoring. \n\nThis research was supported by grants from the U.S. National Science Foundation to D.L.A. (IOS 0923849) and to M.H.D. (IOS 0923802), and by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (402667) to D.L.A, and a Postdoctoral Fellowship to R.D. \n\nEthics: Animal experimentation: All procedures were conducted under approval of the Institutional Animal Care and Use Committee at the University of California, Riverside and the Animal Care Committee at the University of British Columbia.\n\nReviewing editor: Russ Fernald, Reviewing editor, Stanford University, United States \n\nThe funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. \n\nAuthor contributions: \nPSS, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article\nRD, Conception and design, Analysis and interpretation of data, Drafting or revising the article. VBZ, Conception and design, Drafting or revising the article. MHD, Conception and design, Drafting or revising the article. ADS, Conception and design, Drafting or revising the article, Contributed unpublished essential data or reagents. \nDLA, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article.", revision_no = "14", abstract = "Despite recent advances in the study of animal flight, the biomechanical determinants of maneuverability are poorly understood. It is thought that maneuverability may be influenced by intrinsic body mass and wing morphology, and by physiological muscle capacity, but this hypothesis has not yet been evaluated because it requires tracking a large number of free flight maneuvers from known individuals. We used an automated tracking system to record flight sequences from 20 Anna's hummingbirds flying solo and in competition in a large chamber. We found that burst muscle capacity predicted most performance metrics. Hummingbirds with higher burst capacity flew with faster velocities, accelerations, and rotations, and they used more demanding complex turns. In contrast, body mass did not predict variation in maneuvering performance, and wing morphology predicted only the use of arcing turns and high centripetal accelerations. Collectively, our results indicate that burst muscle capacity is a key predictor of maneuverability.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/60058, title ="Functional divisions for visual processing in the central brain of flying Drosophila", author = "Weir, Peter T. and Dickinson, Michael H.", journal = "Proceedings of the National Academy of Sciences", volume = "112", number = "40", pages = "E5523-E5532", month = "October", year = "2015", doi = "10.1073/pnas.1514415112", issn = "0027-8424", url = "https://resolver.caltech.edu/CaltechAUTHORS:20150903-142543425", note = "© 2015 National Academy of Sciences.\n\nEdited by Sten Grillner, Karolinska Institute, Stockholm, Sweden, and approved August 3, 2015 (received for review July 23, 2015). Published ahead of print August 31, 2015. \n\nWe thank Rachel Wilson, Philip Holmes, and Bettina Schnell for valuable feedback. Research reported in this publication was supported by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award U01NS090514. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. \n\nAuthor contributions: P.T.W. and M.H.D. designed research; P.T.W. performed research; P.T.W. contributed new reagents/analytic tools; P.T.W. analyzed data; and P.T.W. and M.H.D. wrote the paper. \n\nThe authors declare no conflict of interest. \n\nThis article is a PNAS Direct Submission. \n\nThis article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1514415112/-/DCSupplemental.", revision_no = "37", abstract = "Although anatomy is often the first step in assigning functions to neural structures, it is not always clear whether architecturally distinct regions of the brain correspond to operational units. Whereas neuroarchitecture remains relatively static, functional connectivity may change almost instantaneously according to behavioral context. We imaged panneuronal responses to visual stimuli in a highly conserved central brain region in the fruit fly, Drosophila, during flight. In one substructure, the fan-shaped body, automated analysis revealed three layers that were unresponsive in quiescent flies but became responsive to visual stimuli when the animal was flying. The responses of these regions to a broad suite of visual stimuli suggest that they are involved in the regulation of flight heading. To identify the cell types that underlie these responses, we imaged activity in sets of genetically defined neurons with arborizations in the targeted layers. The responses of this collection during flight also segregated into three sets, confirming the existence of three layers, and they collectively accounted for the panneuronal activity. Our results provide an atlas of flight-gated visual responses in a central brain circuit.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/58906, title ="Mosquitoes Use Vision to Associate Odor Plumes with Thermal Targets", author = "van Breugel, Floris and Riffell, Jeff", journal = "Current Biology", volume = "25", number = "16", pages = "2123-2129", month = "August", year = "2015", doi = "10.1016/j.cub.2015.06.046 ", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20150716-090310399", note = "© 2015 Elsevier Ltd. \n\nReceived: May 20, 2015; Revised: June 17, 2015; Accepted: June 19, 2015; Published: July 16, 2015. \n\nWe thank A. Straw for help with the three-dimensional tracking software, C. Vinauger and B. Nguyen for help with raising the mosquitos, and members of the M.H.D. lab for experimental and manuscript feedback. This work was funded by NIH grant NIH1RO1DCO13693-01. \n\nAuthor Contributions: F.v.B. carried out all the experiments and analyzed the data. All authors contributed to the experimental design, and interpretation of the data. F.v.B and M.H.D. together produced the figures and wrote the manuscript, with help from J.R. and A.F.", revision_no = "36", abstract = "All moving animals, including flies [1, 2 and 3], sharks [4], and humans [5], experience a dynamic sensory landscape that is a function of both their trajectory through space and the distribution of stimuli in the environment. This is particularly apparent for mosquitoes, which use a combination of olfactory, visual, and thermal cues to locate hosts [6, 7, 8, 9 and 10]. Mosquitoes are thought to detect suitable hosts by the presence of a sparse CO2 plume, which they track by surging upwind and casting crosswind [11]. Upon approach, local cues such as heat and skin volatiles help them identify a landing site [12, 13, 14 and 15]. Recent evidence suggests that thermal attraction is gated by the presence of CO2 [6], although this conclusion was based experiments in which the actual flight trajectories of the animals were unknown and visual cues were not studied. Using a three-dimensional tracking system, we show that rather than gating heat sensing, the detection of CO2 actually activates a strong attraction to visual features. This visual reflex guides the mosquitoes to potential hosts where they are close enough to detect thermal cues. By experimentally decoupling the olfactory, visual, and thermal cues, we show that the motor reactions to these stimuli are independently controlled. Given that humans become visible to mosquitoes at a distance of 5–15 m [16], visual cues play a critical intermediate role in host localization by coupling long-range plume tracking to behaviors that require short-range cues. Rather than direct neural coupling, the separate sensory-motor reflexes are linked as a result of the interaction between the animal’s reactions and the spatial structure of the stimuli in the environment.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/58842, title ="Antennal Mechanosensory Neurons Mediate Wing Motor Reflexes in Flying Drosophila", author = "Mamiya, Akira and Dickinson, Michael H.", journal = "Journal of Neuroscience", volume = "35", number = "20", pages = "7977-7991", month = "May", year = "2015", doi = "10.1523/JNEUROSCI.0034-15.2015", issn = "0270-6474", url = "https://resolver.caltech.edu/CaltechAUTHORS:20150710-100236744", note = "© 2015 the authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). \n\nReceived Jan. 5, 2015; revised April 8, 2015; accepted April 13, 2015.\n\nThis work was supported by the Paul G. Allen Family Foundation to M.H.D. We thank Allan Wong for flies (JO1,\nJO-AB, JO-CE, and F GAL4 drivers, and JO-CE;eyeflp flies); Anne Sustar and Ainul Huda for technical assistance; and\nBettina Schnell, Marie P. Suver, and Peter T. Weir for helpful discussions and comments.\n\nAuthor contributions: A.M. and M.H.D. designed research; A.M. performed research; A.M. analyzed data; A.M.\nand M.H.D. wrote the paper.", revision_no = "12", abstract = "Although many behavioral studies have shown the importance of antennal mechanosensation in various aspects of insect flight control, the identities of the mechanosensory neurons responsible for these functions are still unknown. One candidate is the Johnston's organ (JO) neurons that are located in the second antennal segment and detect phasic and tonic rotations of the third antennal segment relative to the second segment. To investigate how different classes of JO neurons respond to different types of antennal movement during flight, we combined 2-photon calcium imaging with a machine vision system to simultaneously record JO neuron activity and the antennal movement from tethered flying fruit flies (Drosophila melanogaster). We found that most classes of JO neurons respond strongly to antennal oscillation at the wing beat frequency, but not to the tonic deflections of the antennae. To study how flies use input from the JO neurons during flight, we genetically ablated specific classes of JO neurons and examined their effect on the wing motion. Tethered flies flying in the dark require JO neurons to generate slow antiphasic oscillation of the left and right wing stroke amplitudes. However, JO neurons are not necessary for this antiphasic oscillation when visual feedback is available, indicating that there are multiple pathways for generating antiphasic movement of the wings. Collectively, our results are consistent with a model in which flying flies use JO neurons to detect increases in the wing-induced airflow and that JO neurons are involved in a response that decreases contralateral wing stoke amplitude.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/55907, title ="Motor Control: How Dragonflies Catch Their Prey", author = "Dickinson, Michael H.", journal = "Current Biology", volume = "25", number = "6", pages = "R232-R234", month = "March", year = "2015", doi = "10.1016/j.cub.2015.01.046", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20150319-065559382", note = "© 2015 Elsevier B.V.", revision_no = "9", abstract = "Detailed measurements of head and body motion have revealed previously unknown complexity in the predatory behavior of dragonflies. The new evidence suggests that the brains of these agile predators compute internal models of their own actions and those of their prey.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/54873, title ="Body saccades of Drosophila 1 consist of stereotyped banked turns", author = "Muijres, Florian T. and Elzinga, Michael J.", journal = "Journal of Experimental Biology", volume = "218", number = "6", pages = "864-875", month = "March", year = "2015", doi = "10.1242/\u200bjeb.114280 ", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20150217-123946070", note = "© 2015. Published by The Company of Biologists Ltd.\n\nReceived September 22, 2014; Accepted January 12, 2015; First posted online \nFebruary 5, 2015.\n\nThe authors wish to thank Johan Melis, Steve Safarik, and Darren Howell for help with this project.\n\nCompeting interests:\nThe authors declare no competing financial interests.\n\nAuthor contributions:\nF.T.M and M.H.D planned experiments and wrote the paper. F.T.M. and N.A.I. collected data in flight arena, ran the automated machine vision tracking software, and identified sequences with saccadic turns. M.J.E. collected data using the robotic fly. F.T.M. analyzed the data, with the help of M.J.E. and M.H.D.\n\nFunding:\nThis research was supported by grants (to M.H.D) from the Air Force Office of Scientific Research (FA9550-10-1-0368), the Paul G. Allen Family Foundation, and the U.S. Army Research Laboratory (DAAD 19-03-D-0004) and (to F.T.M.) the Swedish Research Council (Vetenskapsrådet).", revision_no = "15", abstract = "The flight pattern of many fly species consists of straight flight segments interspersed with rapid turns called body saccades, a strategy that is thought to minimize motion blur. We analyzed the body saccades of fruit flies (Drosophila hydei), using high-speed 3D videography to track body and wing kinematics and a dynamically-scaled robot to study the production of aerodynamic forces and moments. Although the size, degree and speed of the saccades vary, the dynamics of the maneuver are remarkably stereotypic. In executing a body saccade, flies perform a quick roll and counter-roll, combined with a slower unidirectional rotation around their yaw axis. Flies regulate the size of the turn by adjusting the magnitude of torque that they produce about these control axes, while maintaining the orientation of the rotational axes in the body frame constant. In this way, body saccades are different from escape responses in the same species, in which the roll and pitch component of banking is varied to adjust turn angle. Our analysis of the wing kinematics and aerodynamics showed that flies control aerodynamic torques during the saccade primarily by adjusting the timing and amount of span-wise wing rotation.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90930, title ="Hovering Flight in the Honeybee Apis mellifera: Kinematic Mechanisms for Varying Aerodynamic Forces", author = "Vance, Jason T. and Altshuler, Douglas L.", journal = "Physiological and Biochemical Zoology", volume = "87", number = "6", pages = "870-881", month = "November", year = "2014", doi = "10.1086/678955", issn = "1522-2152", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181115-151957763", note = "© 2014 University of Chicago Press. \n\nAccepted 8/31/2014; Electronically Published 11/10/2014. \n\nWe thank David Shelton for the loan of equipment during filming and Nicholas Kostreski and J. Sean Humbert (University of Maryland, Department of Aerospace Engineering) for constructing the three-dimensional honey bee model and simulation videos used for the analysis of digitizing error. Funding was provided by a Nevada NASA Space Grant Fellowship (to J.T.V.), National Institutes of Health Fellowship F32 NS46221 (to D.L.A.), Office of Naval Research grant N00014-03-1-0604 (to M.H.D.), Packard Foundation grant 2001-17741A (to M.H.D.), and National Science Foundation grants IBN-0217229 (to M.H.D.) and IOS-0725030 (to S.P.R).", revision_no = "10", abstract = "During hovering flight, animals can increase the wing velocity and therefore the net aerodynamic force per stroke by increasing wingbeat frequency, wing stroke amplitude, or both. The magnitude and orientation of aerodynamic forces are also influenced by the geometric angle of attack, timing of wing rotation, wing contact, and pattern of deviation from the primary stroke plane. Most of the kinematic data available for flying animals are average values for wing stroke amplitude and wingbeat frequency because these features are relatively easy to measure, but it is frequently suggested that the more subtle and difficult-to-measure features of wing kinematics can explain variation in force production for different flight behaviors. Here, we test this hypothesis with multicamera high-speed recording and digitization of wing kinematics of honeybees (Apis mellifera) hovering and ascending in air and hovering in a hypodense gas (heliox: 21% O_2, 79% He). Bees employed low stroke amplitudes (86.7° ± 7.9°) and high wingbeat frequencies (226.8 ± 12.8 Hz) when hovering in air. When ascending in air or hovering in heliox, bees increased stroke amplitude by 30%–45%, which yielded a much higher wing tip velocity relative to that during simple hovering in air. Across the three flight conditions, there were no statistical differences in the amplitude of wing stroke deviation, minimum and stroke-averaged geometric angle of attack, maximum wing rotation velocity, or even wingbeat frequency. We employed a quasi-steady aerodynamic model to estimate the effects of wing tip velocity and geometric angle of attack on lift and drag. Lift forces were sensitive to variation in wing tip velocity, whereas drag was sensitive to both variation in wing tip velocity and angle of attack. Bees utilized kinematic patterns that did not maximize lift production but rather maintained lift-to-drag ratio. Thus, our data indicate that, at least for honeybees, the overall time course of wing angles is generally preserved and modulation of wing tip velocity is sufficient to perform a diverse set of vertical flight behaviors.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90968, title ="Automated monitoring and quantitative analysis of feeding behaviour in Drosophila", author = "Itskov, Pavel M. and Moreira, José-Maria", journal = "Nature Communications", volume = "5", pages = "Art. No. 4560", month = "August", year = "2014", doi = "10.1038/ncomms5560", issn = "2041-1723", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-112934152", note = "© 2014 The Author(s). This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-sa/4.0/ \n\nReceived 3 Jun 2014 | Accepted 30 Jun 2014 | Published 4 Aug 2014. \n\nWe thank Thomas R. Clandinin, Jürgen Knoblich, Kristin Scott and and Bruno Lemaitre for sharing fly stocks. We thank Célia Baltazar, Ana Paula Elias and Ana Sofia Valente for technical assistance in running experiments, Matthieu Pasquet and Ricardo Ribeiro for assistance in hardware and acquisition software development and the Instituto Gulbenkian de Ciência for providing us access to experimental setups. Thomas R. Clandinin, Rui Costa, Samuel Walker and all the members of the Behavior and Metabolism Laboratory for helpful discussions and comments on the manuscript. This project was supported by a Human Frontiers Program Project Grant RGP0022/2012 to M.H.D. and C.R., an Allen Distinguished Investigator award to M.H.D. and the BIAL Foundation grant #167/10 and the Portuguese Foundation for Science and Technology (FCT) grant PTDC/BIA-BCM/118684/2010 to CR. P.M.I. is supported by the postdoctoral fellowship SFRH/BPD/79325/2011 from the Foundation for Science and Technology, E.V. by the fellowship 193-2012 from the BIAL Foundation and G.L. by the PhD Studentship SFRH/BD/51714/2011 from the Foundation for Science and Technology. The Champalimaud Neuroscience Programme is supported by the Champalimaud Foundation. \n\nAuthor Contributions: P.M.I. and C.R. conceived and developed the project; P.M.I., J.-M.M., G.L., S.S., M.H.D. and C.R. developed hardware and software: P.M.I. and J.-M.M. performed experiments: P.M.I., E.V. and C.R. performed data analysis and interpretation: P.M.I., M.H.D. and C.R. wrote the manuscript. \n\nThe authors declare no competing financial interests.", revision_no = "14", abstract = "Food ingestion is one of the defining behaviours of all animals, but its quantification and analysis remain challenging. This is especially the case for feeding behaviour in small, genetically tractable animals such as Drosophila melanogaster. Here, we present a method based on capacitive measurements, which allows the detailed, automated and high-throughput quantification of feeding behaviour. Using this method, we were able to measure the volume ingested in single sips of an individual, and monitor the absorption of food with high temporal resolution. We demonstrate that flies ingest food by rhythmically extending their proboscis with a frequency that is not modulated by the internal state of the animal. Instead, hunger and satiety homeostatically modulate the microstructure of feeding. These results highlight similarities of food intake regulation between insects, rodents, and humans, pointing to a common strategy in how the nervous systems of different animals control food intake.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/52219, title ="Reverse Engineering Animal Vision with Virtual Reality and Genetics", author = "Stowers, John R. and Fuhrmann, Anton", journal = "Computer", volume = "47", number = "7", pages = "38-45", month = "July", year = "2014", doi = "10.1109/MC.2014.190", issn = "0018-9162", url = "https://resolver.caltech.edu/CaltechAUTHORS:20141201-104938191", note = "© 2014 IEEE.\n\nThis work was funded by ERC (Starting Grant 281884), WWTF (CS2011-029), and AFOSR (FA9550-10-1-0085), with IMP core funding to Andrew D. Straw, an FWF (P24355) grant to Axel Schmid, and AFOSR (FA9550-06-1-0079) and NSF (0923802) grants to Michael H. Dickinson. The fly brain images were made by Karin Panser with help from the IMP-IMBA bio-optics department, and the IMP-IMBA workshop helped with construction of the VR arenas. All flies were obtained through the Bloomington Drosophila Stock Center. G. Rubin and A. Nern generated the GMR81G07-GAL4 line (BDSC 40122), and B. Hassan and H. Bellen generated the ato-Gal4-14a-GAL4 line (BDSC 6840). The IMP workshop helped build the VR arenas. Emil Persson provided the panoramic image texture used in many of the images.", revision_no = "13", abstract = "Neuroscientists are using virtual reality systems, combined with other advances such as new molecular genetic tools and brain-recording technologies, to reveal how neuronal circuits process and act on visual information. The Web extra at http://youtu.be/e_BxdbNidyQ is an overview video showing the FlyVR system in operation, including four example experiments.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/46549, title ="Monocular distance estimation from optic flow during active landing maneuvers", author = "van Breugel, Floris and Morgansen, Kristi", journal = "Bioinspiration and Biomimetics", volume = "9", number = "2", pages = "Art. No. 025002", month = "June", year = "2014", doi = "10.1088/1748-3182/9/2/025002", issn = "1748-3182", url = "https://resolver.caltech.edu/CaltechAUTHORS:20140627-092344566", note = "© 2014 Institute of Physics. \n\nContent from this work may be used under the terms of\nthe Creative Commons Attribution 3.0 licence. Any further\ndistribution of this work must maintain attribution to the author(s) and the\ntitle of the work, journal citation and DOI.\n\nReceived 21 July 2013, revised 1 October 2013. Accepted for publication 4 October 2013.\nPublished 22 May 2014. \n\nThe authors wish to thank Dr Michael Elzinga for help with constructing the linear rail mechanism used in our robotic implementation, and Nathan Powell for providing MATLAB code to run the square root implementation of the unscented Kalman filter. Funding was provided by the Hertz Foundation Graduate Research Fellowship (awarded to FvB), NSF Graduate Research Fellowship (awarded to FvB), Air Force Office of Scientific Research (FA9550-10-1-0368), and the Paul G. Allen Family Foundation Distinguished Investigator Award (awarded to MHD). The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication. The authors declare that no competing interests exist. ", revision_no = "21", abstract = "Vision is arguably the most widely used sensor for position and velocity estimation in animals, and it is increasingly used in robotic systems as well. Many animals use stereopsis and object recognition in order to make a true estimate of distance. For a tiny insect such as a fruit fly or honeybee, however, these methods fall short. Instead, an insect must rely on calculations of optic flow, which can provide a measure of the ratio of velocity to distance, but not either parameter independently. Nevertheless, flies and other insects are adept at landing on a variety of substrates, a behavior that inherently requires some form of distance estimation in order to trigger distance-appropriate motor actions such as deceleration or leg extension. Previous studies have shown that these behaviors are indeed under visual control, raising the question: how does an insect estimate distance solely using optic flow? In this paper we use a nonlinear control theoretic approach to propose a solution for this problem. Our algorithm takes advantage of visually controlled landing trajectories that have been observed in flies and honeybees. Finally, we implement our algorithm, which we term dynamic peering, using a camera mounted to a linear stage to demonstrate its real-world feasibility.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/46565, title ="Strategies for the stabilization of longitudinal forward flapping flight revealed using a dynamically-scaled robotic fly", author = "Elzinga, Michael J. and van Breugel, Floris", journal = "Bioinspiration and Biomimetics", volume = "9", number = "2", pages = "Art. No. 025001", month = "June", year = "2014", doi = "10.1088/1748-3182/9/2/025001 ", issn = "1748-3182", url = "https://resolver.caltech.edu/CaltechAUTHORS:20140630-091405439", note = "© 2014 IOP Publishing Ltd.\n\nReceived 31 October 2013, revised 14 January 2014;\nAccepted for publication 22 January 2014;\nPublished 22 May 2014.\n\nResearch was supported by the US Army Research Laboratory\nMicro Autonomous Systems and Technology (MAST)\nCollaborative Technology Alliance (DAAD 19-03-D-0004).", revision_no = "16", abstract = "The ability to regulate forward speed is an essential requirement for flying animals. Here, we use a dynamically-scaled robot to study how flapping insects adjust their wing kinematics to regulate and stabilize forward flight. The results suggest that the steady-state lift and thrust requirements at different speeds may be accomplished with quite subtle changes in hovering kinematics, and that these adjustments act primarily by altering the pitch moment. This finding is consistent with prior hypotheses regarding the relationship between body pitch and flight speed in fruit flies. Adjusting the mean stroke position of the wings is a likely mechanism for trimming the pitch moment at all speeds, whereas changes in the mean angle of attack may be required at higher speeds. To ensure stability, the flapping system requires additional pitch damping that increases in magnitude with flight speed. A compensatory reflex driven by fast feedback of pitch rate from the halteres could provide such damping, and would automatically exhibit gain scheduling with flight speed if pitch torque was regulated via changes in stroke deviation. Such a control scheme would provide an elegant solution for stabilization across a wide range of forward flight speeds.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/43984, title ="Octopaminergic modulation of the visual flight speed regulator of Drosophila", author = "van Breugel, Floris and Suver, Marie P.", journal = "Journal of Experimental Biology", volume = "217", number = "10", pages = "1737-1744", month = "May", year = "2014", doi = "10.1242/\u200bjeb.098665", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20140225-130816052", note = "© 2013 Published by The Company of Biologists Ltd. \n\nReceived October 18, 2013. Accepted January 29, 2014. First posted online February 13, 2014. \n\nThe authors thank Anne Sustar and Ainul Huda for helping to create the necessary\ngenetic constructs, and running experiments, as well as Dr Bettina Schnell and Dr\nEatai Roth for providing valuable feedback on the manuscript.\n\nFunding:\nFunding for this research was provided by The Hertz Foundation Graduate\nResearch Fellowship (F.v.B.); the National Science Foundation Graduate\nResearch Fellowship (F.v.B.); the Air Force Office of Scientific Research FA9550-\n10-1-0368 (M.H.D.); and the Paul G. Allen Family Foundation Distinguished\nInvestigator Award (M.H.D.).\n\nAuthor contributions:\nThe initial idea for these experiments came from work by M.P.S., who also\nprovided the fly lines and performed confocal imaging. All authors worked together\nto design the experiments. F.v.B. performed the experiments, analysis, modelling\nand wrote the first draft of the paper. All authors contributed to the interpretation of\nresults and revision of the manuscript.\n\nCompeting interests:\nThe authors declare no competing financial interests.", revision_no = "24", abstract = "Recent evidence suggests that flies' sensitivity to large-field optic flow is increased by the release of octopamine during flight. This increase in gain presumably enhances visually mediated behaviors such as the active regulation of forward speed, a process that involves the comparison of a vision-based estimate of velocity with an internal set point. To determine where in the neural circuit this comparison is made, we selectively silenced the octopamine neurons in the fruit fly Drosophila, and examined the effect on vision-based velocity regulation in free-flying flies. We found that flies with inactivated octopamine neurons accelerated more slowly in response to visual motion than control flies, but maintained nearly the same baseline flight speed. Our results are parsimonious with a circuit architecture in which the internal control signal is injected into the visual motion pathway upstream of the interneuron network that estimates groundspeed.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90966, title ="Cellular mechanisms for integral feedback in visually guided behavior", author = "Schnell, Bettina and Weir, Peter T.", journal = "Proceedings of the National Academy of Sciences of the United States of America", volume = "111", number = "15", pages = "5700-5705", month = "April", year = "2014", doi = "10.1073/pnas.1400698111", issn = "0027-8424", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-112838609", note = "© 2014 National Academy of Sciences. Freely available online through the PNAS open access option. \n\nEdited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved March 7, 2014 (received for review January 14, 2014) \n\nWe thank Anne Sustar for the confocal image of the R27B03-Gal4 line. This work was supported by the Raymond and Beverly Sackler Foundation (B.S.), the Paul G. Allen Family Foundation (M.H.D.), and Air Force Office of Scientific Research Grant FA9550-10-1-0368 (M.H.D). \n\nAuthor contributions: B.S., P.T.W., A.L.F., and M.H.D. designed research; B.S., P.T.W., and E.R. performed research; B.S., P.T.W., and E.R. analyzed data; and B.S., P.T.W., A.L.F., and M.H.D. wrote the paper. \n\nThe authors declare no conflict of interest. \n\nThis article is a PNAS Direct Submission. \n\nThis article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1400698111/-/DCSupplemental.", revision_no = "11", abstract = "Sensory feedback is a ubiquitous feature of guidance systems in both animals and engineered vehicles. For example, a common strategy for moving along a straight path is to turn such that the measured rate of rotation is zero. This task can be accomplished by using a feedback signal that is proportional to the instantaneous value of the measured sensory signal. In such a system, the addition of an integral term depending on past values of the sensory input is needed to eliminate steady-state error [proportional-integral (PI) control]. However, the means by which nervous systems implement such a computation are poorly understood. Here, we show that the optomotor responses of flying Drosophila follow a time course consistent with temporal integration of horizontal motion input. To investigate the cellular basis of this effect, we performed whole-cell patch-clamp recordings from the set of identified visual interneurons [horizontal system (HS) cells] thought to control this reflex during tethered flight. At high stimulus speeds, HS cells exhibit steady-state responses during flight that are absent during quiescence, a state-dependent difference in physiology that is explained by changes in their presynaptic inputs. However, even during flight, the membrane potential of the large-field interneurons exhibits no evidence for integration that could explain the behavioral responses. However, using a genetically encoded indicator, we found that calcium accumulates in the terminals of the interneurons along a time course consistent with the behavior and propose that this accumulation provides a mechanism for temporal integration of sensory feedback consistent with PI control.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90967, title ="Flies Evade Looming Targets by Executing Rapid Visually Directed Banked Turns", author = "Muijres, Florian T. and Elzinga, Michael J.", journal = "Science", volume = "344", number = "6180", pages = "172-177", month = "April", year = "2014", doi = "10.1126/science.1248955", issn = "0036-8075", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-112933979", note = "© 2014 American Association for the Advancement of Science. \n\n25 November 2013; accepted 11 March 2014. \n\nThis work was supported by grants from the Air Force Office of Scientific Research (FA9550-10-1-0368) to M.H.D., the Paul G. Allen Family Foundation to M.H.D., Army Research Laboratory (DAAD 19-03-D-0004) to M.H.D., Swedish Research Council to F.T.M., and the Royal Physiographical Society in Lund to F.T.M. We thank S. Safarik, X. Zabala, and J. Liu for their technical support, and B. van Oudheusden for co-supervising J.M.M. The data reported in this paper are tabulated in the supplementary materials: The body and wing kinematics data for all reported flight sequences, as well as forces and torques from the robotic fly experiments, are stored in Database S1, and the Fourier series coefficients required to reconstruct the here analyzed wingbeat kinematics (using eq. S1) are available in table S1.", revision_no = "48", abstract = "Avoiding predators is an essential behavior in which animals must quickly transform sensory cues into evasive actions. Sensory reflexes are particularly fast in flying insects such as flies, but the means by which they evade aerial predators is not known. Using high-speed videography and automated tracking of flies in combination with aerodynamic measurements on flapping robots, we show that flying flies react to looming stimuli with directed banked turns. The maneuver consists of a rapid body rotation followed immediately by an active counter-rotation and is enacted by remarkably subtle changes in wing motion. These evasive maneuvers of flies are substantially faster than steering maneuvers measured previously and indicate the existence of sensory-motor circuitry that can reorient the fly’s flight path within a few wingbeats.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/45467, title ="Flying Drosophila stabilize their vision-based velocity controller by sensing wind with their antennae", author = "Fuller, Sawyer Buckminster and Straw, Andrew D.", journal = "Proceedings of the National Academy of Sciences of the United States of America", volume = "111", number = "13", pages = "E1182-E1191", month = "April", year = "2014", doi = "10.1073/pnas.1323529111 ", issn = "0027-8424", url = "https://resolver.caltech.edu/CaltechAUTHORS:20140502-103349067", note = "© 2014 National Academy of Sciences.\nEdited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved February 20, 2014 (received for review December 18, 2013). Published online before print March 17, 2014.\n\nThe authors thank Matthias Wittlinger for help\nconstructing the apparatus and Michael Elzinga, Robert Engle, K. Rhett\nNichols, and Katharina Reinecke for helpful comments regarding the\nmanuscript. Also, thanks to Patrice Engle, in memoriam, for the laughter.\nThis work was supported by the Institute for Collaborative Biotechnologies\nthrough Grant DAAD19-03-D-0004 from the US Army Research Office and by\na National Science Foundation Graduate Fellowship (to S.B.F.).\n\nAuthor contributions: S.B.F., A.D.S., R.M.M., and M.H.D. designed research; S.B.F. and\nM.Y.P. performed research; S.B.F. and A.D.S. contributed new reagents/analytic tools;\nS.B.F. analyzed data; and S.B.F. and M.H.D. wrote the paper.\nThe authors declare no conflict of interest.", revision_no = "15", abstract = "Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (~100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly’s velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (~20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies’ multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/43479, title ="Plume-Tracking Behavior of Flying Drosophila Emerges from a Set of Distinct Sensory-Motor Reflexes", author = "van Breugel, Floris and Dickinson, Michael H.", journal = "Current Biology", volume = "24", number = "3", pages = "274-286", month = "February", year = "2014", doi = "10.1016/j.cub.2013.12.023", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20140123-081449248", note = "© 2014 Elsevier Ltd.\n\nReceived: October 28, 2013; Revised: November 25, 2013; Accepted: December 11, 2013; Published: January 16, 2014.\n\nThe authors wish to thank Jeff Riffell for many helpful comments and advice on this work. Andrew Straw provided help with use of the fly-tracking system. This work was supported by grants from the National Science Foundation (0623527), the Air Force Office of Scientific Research (FA9550-10-1-0368), and the Paul G. Allen Family Foundation (to M.H.D.) and graduate training fellowships from The Hertz Foundation and The National Science Foundation (to F.v.B.).", revision_no = "22", abstract = "Background:\n\nFor a fruit fly, locating fermenting fruit where it can feed, find mates, and lay eggs is an essential and difficult task requiring the integration of olfactory and visual cues. Here, we develop an approach to correlate flies’ free-flight behavior with their olfactory experience under different wind and visual conditions, yielding new insight into plume tracking based on over 70 hr of data.\n\nResults:\n\nTo localize an odor source, flies exhibit three iterative, independent, reflex-driven behaviors, which remain constant through repeated encounters of the same stimulus: (1) 190 ± 75 ms after encountering a plume, flies increase their flight speed and turn upwind, using visual cues to determine wind direction. Due to this substantial response delay, flies pass through the plume shortly after entering it. (2) 450 ± 165 ms after losing the plume, flies initiate a series of vertical and horizontal casts, using visual cues to maintain a crosswind heading. (3) After sensing an attractive odor, flies exhibit an enhanced attraction to small visual features, which increases their probability of finding the plume’s source.\n\nConclusions:\n\nDue to plume structure and sensory-motor delays, a fly’s olfactory experience during foraging flights consists of short bursts of odor stimulation. As a consequence, delays in the onset of crosswind casting and the increased attraction to visual features are necessary behavioral components for efficiently locating an odor source. Our results provide a quantitative behavioral background for elucidating the neural basis of plume tracking using genetic and physiological approaches.\n", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90987, title ="Fly with a little flap from your friends", author = "Muijres, Florian T. and Dickinson, Michael H.", journal = "Nature", volume = "505", number = "7483", pages = "295-296", month = "January", year = "2014", doi = "10.1038/505295a", issn = "0028-0836", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-144741989", note = "© 2014 Nature Publishing Group.", revision_no = "11", abstract = "In-air measurements of northern bald ibises flying in a V formation show that the birds conform to predictions for saving energy by regulating their relative body position and synchronizing their flapping motion.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90975, title ="Central complex neurons exhibit behaviorally gated responses to visual motion in Drosophila", author = "Weir, Peter T. and Schnell, Bettina", journal = "Journal of Neurophysiology", volume = "111", number = "1", pages = "62-71", month = "January", year = "2014", doi = "10.1152/jn.00593.2013", issn = "0022-3077", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-113011724", note = "© 2014 the American Physiological Society. \n\nReceived 20 August 2013. Accepted 3 October 2013. Published online 1 January 2014. \n\nWe thank Akira Mamiya and two anonymous reviewers for helpful comments. \n\nThis work was supported by the Raymond and Beverly Sackler Foundation (B. Schnell), the Paul G. Allen Family Foundation (M. H. Dickinson), the Air Force Office of Scientific Research Grant FA9550-10-1-0368 (M. H. Dickinson). \n\nAuthor Contributions: P.T.W. and M.H.D. conception and design of research; P.T.W. and B.S. performed experiments; P.T.W. analyzed data; P.T.W., B.S., and M.H.D. interpreted results of experiments; P.T.W. prepared figures; P.T.W. drafted manuscript; P.T.W., B.S., and M.H.D. edited and revised manuscript; P.T.W., B.S., and M.H.D. approved final version of manuscript. \n\nNo conflicts of interest, financial or otherwise, are declared by the authors.", revision_no = "10", abstract = "Sensory systems provide abundant information about the environment surrounding an animal, but only a small fraction of that information is relevant for any given task. One example of this requirement for context-dependent filtering of a sensory stream is the role that optic flow plays in guiding locomotion. Flying animals, which do not have access to a direct measure of ground speed, rely on optic flow to regulate their forward velocity. This observation suggests that progressive optic flow, the pattern of front-to-back motion on the retina created by forward motion, should be especially salient to an animal while it is in flight, but less important while it is standing still. We recorded the activity of cells in the central complex of Drosophila melanogaster during quiescence and tethered flight using both calcium imaging and whole cell patch-clamp techniques. We observed a genetically identified set of neurons in the fan-shaped body that are unresponsive to visual motion while the animal is quiescent. During flight their baseline activity increases, and they respond to front-to-back motion with changes relative to this baseline. The results provide an example of how nervous systems selectively respond to complex sensory stimuli depending on the current behavioral state of the animal.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90976, title ="Death Valley, Drosophila, and the Devonian Toolkit", author = "Dickinson, Michael H.", journal = "Annual Review of Entomology", volume = "59", pages = "51-72", month = "January", year = "2014", doi = "10.1146/annurev-ento-011613-162041", issn = "0066-4170", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-113011826", note = "© 2014 Annual Reviews. \n\nI wish to thank all the members of my laboratory who provided valuable feedback on this essay. This includes Peter Weir, Eatai Roth, Floris van Breugel, Sweta Agrawal, and Tim Warren. John Tuthill and Gwyneth Card also provided useful advice, as did my wife, Usha Lee McFarling. While working on this manuscript I was supported in part by the Paul G. Allen Family Foundation and the Air Force Office of Scientific Research. \n\nThe author is not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.", revision_no = "9", abstract = "Most experiments on the flight behavior of Drosophila melanogaster have been performed within confined laboratory chambers, yet the natural history of these animals involves dispersal that takes place on a much larger spatial scale. Thirty years ago, a group of population geneticists performed a series of mark-and-recapture experiments on Drosophila flies, which demonstrated that even cosmopolitan species are capable of covering 10 km of open desert, probably in just a few hours and without the possibility of feeding along the way. In this review I revisit these fascinating and informative experiments and attempt to explain how—from takeoff to landing—the flies might have made these journeys based on our current knowledge of flight behavior. This exercise provides insight into how animals generate long behavioral sequences using sensory-motor modules that may have an ancient evolutionary origin.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/38249, title ="Foraging for food: multimodel sensory fusion in freely flying fruit flies", author = "van Breugel, F. and Dickinson, M.", journal = "Integrative and Comparative Biology", volume = "53", number = "S1", pages = "E217", month = "April", year = "2013", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20130503-073231763", note = "© 2013 The Society for Integrative and Comparative Biology.", revision_no = "23", abstract = "The ability to find food by tracking wind−borne odor plumes to their source is one of the most critical yet difficult tasks an insect performs. In a natural environment, turbulent air breaks apart the odor distribution in a plume, resulting in packets of high concentration interspersed with clean air. The visual sense, however,\nprovides continuous information about where objects are, but very little about what they are. Thus, it would seem prudent for an animal to integrate the two sensory cues to maximize their ability to localize food sources. In this study we focus on the fruit fly, and how they are able to track a time varying plume of an attractive odor to its physical source, and whether or not they decide to land on it. To answer these questions we built an experimental rig capable of delivering predictable pulses of odor into a windtunnel with minimal turbulence. We used a mini PID to characterize the odor pulses and build an accurate model, allowing us to predict the time varying odor landscape in the wind tunnel. To study how the flies integrate this\nolfactory cue with their visual sense we added a vertical black post near the plume. Using a 9−camera tracking system we were able to track the flies in 3D as they flew through the wind tunnel with different olfactory and visual scenarios. Preliminary results suggest that flies that recently passed through an odor plume are 3 times more likely to land on a nearby object (N=699), compared to flies\nwho have not experienced any odor, yet flew within the same general area (N=879). Furthermore, the effect of the odor stimulus appears to persist − flies that have experienced odor, but less recently, are 7 times more likely to land than in the control case (N=679, 686, resp.). In summary, our unique experimental paradigm has allowed us to begin probing the roles of olfaction, vision, and memory, in food\nfinding behavior in freely flying fruit flies.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/38251, title ="Stroke features involved in the stabilization of longitudinal forward flight in flies", author = "Elzinga, M. J. and Dickinson, M. H.", journal = "Integrative and Comparative Biology", volume = "53", number = "S1", pages = "E63", month = "April", year = "2013", issn = "1540-7063", url = "https://resolver.caltech.edu/CaltechAUTHORS:20130503-081421118", note = "© 2013 The Society for Integrative and Comparative Biology. ", revision_no = "10", abstract = "The ability to regulate forward speed is an essential capability for flying animals. Here, we use a dynamically scaled robot to gain insight into how flapping insects adjust stroke features to regulate and stabilize level forward flight. The results suggest that few changes to hovering kinematics are actually required to meet lift and\nthrust requirements, and the primary driver of equilibrium velocity is the aerodynamic pitch moment. This finding is consistent with prior hypotheses and observations regarding the relationship between body pitch and flight speed in fruit flies. We considered three different deformations of hovering wing kinematics, which were inspired by previous experimental studies and that result in the generation of a\npitch moment: a shift in the mean stroke position, upstroke to downstroke differences in wing rotation angle, and upstroke to downstroke differences in stroke deviation. The results suggest that a shift in the mean stroke position is a likely candidate for trimming the pitch moment at all speeds, whereas shifts in the wing rotation angle are required only at high speeds. The results also show that the\ndynamics may be stabilized with the addition of a pitch damper, but the magnitude of required damping increases with flight speed. We posit that differences in stroke deviation between the upstroke and downstroke play a critical role in this stabilization. Fast mechanosensory feedback of the pitch rate enables active damping\nwhich becomes inherently gain scheduled with flight speed when pitch torque is generated by differences in deviation. This provides an elegant solution for flight stabilization across a wide range of flight speeds.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90932, title ="Visual motion speed determines a behavioral switch from forward flight to expansion avoidance in Drosophila", author = "Reiser, Michael B. and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "216", number = "4", pages = "719-732", month = "February", year = "2013", doi = "10.1242/jeb.074732", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181115-153344279", note = "© 2013 Published by The Company of Biologists Ltd. \n\nReceived 4 May 2012; Accepted 26 October 2012. \n\nWe thank Dr Mark Frye and members of the Dickinson lab for constructive feedback throughout the development of this project. \n\nThis work was supported by the Institute for Collaborative Biotechnologies through grant DAAD 19-03-D-0004 from the US Army Research Office, by the National Science Foundation (NSF) through award 0623527 to M.H.D. and by the Center for Neuromorphic Systems Engineering (CNSE) Engineering Research Center at Caltech through NSF award EEC-9402726.", revision_no = "9", abstract = "As an animal translates through the world, its eyes will experience a radiating pattern of optic flow in which there is a focus of expansion directly in front and a focus of contraction behind. For flying fruit flies, recent experiments indicate that flies actively steer away from patterns of expansion. Whereas such a reflex makes sense for avoiding obstacles, it presents a paradox of sorts because an insect could not navigate stably through a visual scene unless it tolerated flight towards a focus of expansion during episodes of forward translation. One possible solution to this paradox is that a fly’s behavior might change such that it steers away from strong expansion, but actively steers towards weak expansion. In this study, we use a tethered flight arena to investigate the influence of stimulus strength on the magnitude and direction of turning responses to visual expansion in flies. These experiments indicate that the expansion-avoidance behavior is speed dependent. At slower speeds of expansion, flies exhibit an attraction to the focus of expansion, whereas the behavior transforms to expansion avoidance at higher speeds. Open-loop experiments indicate that this inversion of the expansion-avoidance response depends on whether or not the head is fixed to the thorax. The inversion of the expansion-avoidance response with stimulus strength has a clear manifestation under closed-loop conditions. Flies will actively orient towards a focus of expansion at low temporal frequency but steer away from it at high temporal frequency. The change in the response with temporal frequency does not require motion stimuli directly in front or behind the fly. Animals in which the stimulus was presented within 120 deg sectors on each side consistently steered towards expansion at low temporal frequency and steered towards contraction at high temporal frequency. A simple model based on an array of Hassenstein–Reichardt type elementary movement detectors suggests that the inversion of the expansion-avoidance reflex can explain the spatial distribution of straight flight segments and collision-avoidance saccades when flies fly freely within an open circular arena.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/62390, title ="Discriminating External and Internal Causes for Heading Changes in Freely Flying Drosophila", author = "Censi, Andrea and Straw, Andrew D.", journal = "PLOS Computational Biology", volume = "9", number = "2", pages = "Art. No. e1002891", month = "February", year = "2013", doi = "10.1371/journal.pcbi.1002891", issn = "1553-7358", url = "https://resolver.caltech.edu/CaltechAUTHORS:20151124-141949989", note = "© 2013 Censi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. \n\nReceived: August 2, 2012; Accepted: December 4, 2012; Published: February 28, 2013. \n\nThis study was funded by AFOSR (FA9550-06-1-0079 and FA9550-10-1-0086), ARO (DAAD 19-03-D-0004), and NSF (NSF-0931746), DARPA (MSEE). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. \n\nWe thank Kit Longden for insightful comments on a preliminary version of this work. \n\nAuthor Contributions: Conceived and designed the experiments: ADS MHD. Performed the experiments: ADS RWS. Analyzed the data: AC ADS. Wrote the paper: AC ADS RMM MHD. \n\nThe authors declare that no competing interests exist.", revision_no = "20", abstract = "As animals move through the world in search of resources, they change course in reaction to both external sensory cues and internally-generated programs. Elucidating the functional logic of complex search algorithms is challenging because the observable actions of the animal cannot be unambiguously assigned to externally- or internally-triggered events. We present a technique that addresses this challenge by assessing quantitatively the contribution of external stimuli and internal processes. We apply this technique to the analysis of rapid turns (“saccades”) of freely flying Drosophila melanogaster. We show that a single scalar feature computed from the visual stimulus experienced by the animal is sufficient to explain a majority (93%) of the turning decisions. We automatically estimate this scalar value from the observable trajectory, without any assumption regarding the sensory processing. A posteriori, we show that the estimated feature field is consistent with previous results measured in other experimental conditions. The remaining turning decisions, not explained by this feature of the visual input, may be attributed to a combination of deterministic processes based on unobservable internal states and purely stochastic behavior. We cannot distinguish these contributions using external observations alone, but we are able to provide a quantitative bound of their relative importance with respect to stimulus-triggered decisions. Our results suggest that comparatively few saccades in free-flying conditions are a result of an intrinsic spontaneous process, contrary to previous suggestions. We discuss how this technique could be generalized for use in other systems and employed as a tool for classifying effects into sensory, decision, and motor categories when used to analyze data from genetic behavioral screens.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/36776, title ="Octopamine Neurons Mediate Flight-Induced Modulation of Visual Processing in Drosophila", author = "Suver, Marie P. and Mamiya, Akira", journal = "Current Biology", volume = "22", number = "24", pages = "2294-2302", month = "December", year = "2012", doi = "10.1016/j.cub.2012.10.034", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20130205-104129299", note = "© 2012 Elsevier Ltd.\n\nReceived: September 28, 2012; Revised: October 15, 2012; Accepted: October 16, 2012; Published: November 8, 2012.\n\nWe would like to thank Anne Sustar for the confocal image of the Tdc2-Gal4 line and for helpful comments and aid in setting up fly lines for the paper. We would also like to thank Gaby Maimon for helpful discussion. This work was\nsupported by grants from the National Science Foundation (0623527), the Air Force Office of Scientific Research (FA9550-10-1-0368), and the Paul G. Allen Family Foundation (all to M.H.D.).", revision_no = "14", abstract = "Background: Activity-dependent modulation of sensory systems has been documented in many organisms and is likely to be essential for appropriate processing of information during different behavioral states. However, the mechanisms underlying these phenomena remain poorly characterized.\nResults: We investigated the role of octopamine neurons in the flight-dependent modulation observed in visual interneurons in Drosophila. The vertical system (VS) cells exhibit a boost in their response to visual motion during flight compared to quiescence. Pharmacological application of octopamine evokes responses in quiescent flies that mimic those observed during flight, and octopamine cells that project to the optic lobes increase in activity during flight. Using genetic tools to manipulate the activity of octopamine neurons, we find that they are both necessary and sufficient for the flight-induced visual boost.\nConclusions: This study provides the first evidence that endogenous release of octopamine is involved in state-dependent modulation of visual interneurons in flies.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90973, title ="Editorial policy on computational, simulation and/or robotic papers", author = "Biewener, Andrew A. and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "215", number = "23", pages = "4051-4051", month = "December", year = "2012", doi = "10.1242/jeb.081794", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-113011529", note = "© 2012 Company of Biologists.", revision_no = "8", abstract = "[no abstract]", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/90972, title ="Social structures depend on innate determinants and chemosensory processing in Drosophila", author = "Schneider, Jonathan and Dickinson, Michael H.", journal = "Proceedings of the National Academy of Sciences of the United States of America", volume = "109", number = "Suppl. 2", pages = "17174-17179", month = "October", year = "2012", doi = "10.1073/pnas.1121252109", issn = "0027-8424", url = "https://resolver.caltech.edu/CaltechAUTHORS:20181116-113011346", note = "© 2012 National Academy of Sciences. \n\nEdited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved May 14, 2012 (received for review February 9, 2012) \n\nWe thank Jean-Christoph Billeter, Jayed Atallah, Rebecca Rooke, Altaf Ramji, Carl Bergstrom, Phillip Kim, Laurent Keller, Bruce Schneider, Andrew Straw, and Kristin Branson for their suggestions and discussion. This study was funded by grants from the Canada Research Chair, the Canadian Institutes of Health Research, and the National Sciences and Engineering Research Council of Canada (to J.D.L.) and by National Science Foundation Grant 0623527 (to M.H.D.). \n\nAuthor contributions: J.S. and J.D.L. designed research; J.S. and J.D.L. performed research; J.S. and M.H.D. contributed new reagents/analytic tools; J.S. analyzed data; and J.S., M.H.D., and J.D.L. wrote the paper. \n\nThe authors declare no conflict of interest. \n\nThis article is a PNAS Direct Submission. \n\nThis paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Biological Embedding of Early Social Adversity: From Fruit Flies to Kindergartners,” held December 9–10, 2011, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and audio files of most presentations are available on the NAS Web site at www.nasonline.org/biological-embedding. \n\nThis article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1121252109/-/DCSupplemental.", revision_no = "21", abstract = "Flies display transient social interactions in groups. However, whether fly–fly interactions are stochastic or structured remains unknown. We hypothesized that groups of flies exhibit patterns of social dynamics that would manifest as nonrandom social interaction networks. To test this, we applied a machine vision system to track the position and orientation of flies in an arena and designed a classifier to detect interactions between pairs of flies. We show that the vinegar fly, Drosophila melanogaster, forms nonrandom social interaction networks, distinct from virtual network controls (constructed from the intersections of individual locomotor trajectories). In addition, the formation of interaction networks depends on chemosensory cues. Gustatory mutants form networks that cannot be distinguished from their virtual network controls. Olfactory mutants form networks that are greatly disrupted compared with control flies. Different wild-type strains form social interaction networks with quantitatively different properties, suggesting that the genes that influence this network phenotype vary across and within wild-type populations. We have established a paradigm for studying social behaviors at a group level in Drosophila and expect that a genetic dissection of this phenomenon will identify conserved molecular mechanisms of social organization in other species.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/33549, title ="A Simple Strategy for Detecting Moving Objects during Locomotion Revealed by Animal-Robot Interactions", author = "Zabala, Francisco and Polidoro, Peter", journal = "Current Biology", volume = "22", number = "14", pages = "1344-1350", month = "July", year = "2012", doi = "10.1016/j.cub.2012.05.024", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20120827-095639871", note = "© 2012 Elsevier Ltd. \n\nReceived: April 10, 2012; Revised: May 2, 2012; Accepted: May 11, 2012; Published online: June 21, 2012. \n\nWe wish to thank Andrew Straw for his help with the design of experiments and the development of the software used to create the \"fly’s eye view\" in Movie S2. Peter Weir and Joel Levine provided helpful comments on the manuscript. Funding for this research was provided by US National Institutes of Health grant R01 DA022777 (M.H.D. and P.P.), US National Science Foundation grant 0623527 (M.H.D.), ONR MURI grant 1015-G-NA-127 (P.P.), and the Paul G. Allen Family Foundation (M.H.D.).", revision_no = "25", abstract = "An important role of visual systems is to detect nearby predators, prey, and potential mates, which may be distinguished in part by their motion. When an animal is at rest, an object moving in any direction may easily be detected by motion-sensitive visual circuits. During locomotion, however, this strategy is compromised because the observer must detect a moving object within the pattern of optic flow created by its own motion through the stationary background. However, objects that move creating back-to-front (regressive) motion may be unambiguously distinguished from stationary objects because forward locomotion creates only front-to-back (progressive) optic flow. Thus, moving animals should exhibit an enhanced sensitivity to regressively moving objects. We explicitly tested this hypothesis by constructing a simple fly-sized robot that was programmed to interact with a real fly. Our measurements indicate that whereas walking female flies freeze in response to a regressively moving object, they ignore a progressively moving one. Regressive motion salience also explains observations of behaviors exhibited by pairs of walking flies. Because the assumptions underlying the regressive motion salience hypothesis are general, we suspect that the behavior we have observed in Drosophila may be widespread among eyed, motile organisms.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/32267, title ="The influence of sensory delay on the yaw dynamics of a flapping insect", author = "Elzinga, Michael J. and Dickson, William B.", journal = "Journal of the Royal Society Interface", volume = "9", number = "72", pages = "1685-1696", month = "July", year = "2012", doi = "10.1098/rsif.2011.0699", issn = "1742-5689", url = "https://resolver.caltech.edu/CaltechAUTHORS:20120705-111213410", note = "© 2011 The Royal Society.\n\nReceived 11 October 2011; Accepted 30 November 2011. Published online before print December 21, 2011. \n\nWe would like to thank Noah Cowan, Floris van Breugel and Francisco Zabala for valuable discussions during the preparation of this manuscript. Research was supported by The U.S. Army Research Laboratory Micro Autonomous Systems and Technology (MAST) Collaborative Technology Alliance. The work was carried out at California Institute of Technology.", revision_no = "15", abstract = "In closed-loop systems, sensor feedback delays may have disastrous implications for performance and stability. Flies have evolved multiple specializations to reduce this latency, but the fastest feedback during flight involves a delay that is still significant on the timescale of body dynamics. We explored the effect of sensor delay on flight stability and performance for yaw turns using a dynamically scaled robotic model of the fruitfly, Drosophila. The robot was equipped with a real-time feedback system that performed active turns in response to measured torque about the functional yaw axis. We performed system response experiments for a proportional controller in yaw velocity for a range of feedback delays, similar in dimensionless timescale to those experienced by a fly. The results show a fundamental trade-off between sensor delay and permissible feedback gain, and suggest that fast mechanosensory feedback in flies, and most probably in other insects, provide a source of active damping which compliments that contributed by passive effects. Presented in the context of these findings, a control architecture whereby a haltere-mediated inner-loop proportional controller provides damping for slower visually mediated feedback is consistent with tethered-flight measurements, free-flight observations and engineering design principles. ", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/31820, title ="The visual control of landing and obstacle avoidance in the fruit fly Drosophila melanogaster", author = "van Breugel, Floris and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "215", number = "11", pages = "1783-1798", month = "June", year = "2012", doi = "10.1242/jeb.066498", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20120605-123458002", note = "© 2012 The Company of Biologists Ltd. \n\nAccepted 8 February 2012. \n\nThe authors gratefully acknowledge Dr Andrew Straw, who wrote the 3D tracking software used for our experiments, Sawyer Fuller for building the wind tunnel apparatus, and Will Dickson and Peter Polidoro for their help in building the automated follow focus system used for the high speed video recordings. \n\nThis research was supported by grants from the Air Force Office of Scientific Research (AFOSR) [grant no. 66-1257 to M.H.D.], a Hertz Fellowship and a National Science Foundation (NSF) Graduate Research Fellowship.", revision_no = "39", abstract = "Landing behavior is one of the most critical, yet least studied, aspects of insect flight. In order to land safely, an insect must recognize a visual feature, navigate towards it, decelerate, and extend its legs in preparation for touchdown. Although previous studies have focused on the visual stimuli that trigger these different components, the complete sequence has not been systematically studied in a free-flying animal. Using a real-time 3D tracking system in conjunction with high speed digital imaging, we were able to capture the landing sequences of fruit flies (Drosophila melanogaster) from the moment they first steered toward a visual target, to the point of touchdown. This analysis was made possible by a custom-built feedback system that actively maintained the fly in the focus of the high speed camera. The results suggest that landing is composed of three distinct behavioral modules. First, a fly actively turns towards a stationary target via a directed body saccade. Next, it begins to decelerate at a point determined by both the size of the visual target and its rate of expansion on the retina. Finally, the fly extends its legs when the visual target reaches a threshold retinal size of approximately 60 deg. Our data also let us compare landing sequences with flight trajectories that, although initially directed toward a visual target, did not result in landing. In these ‘fly-by’ trajectories, flies steer toward the target but then exhibit a targeted aversive saccade when the target subtends a retinal size of approximately 33 deg. Collectively, the results provide insight into the organization of sensorimotor modules that underlie the landing and search behaviors of insects.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/29258, title ="Flying Drosophila Orient to Sky Polarization", author = "Weir, Peter T. and Dickinson, Michael H.", journal = "Current Biology", volume = "22", number = "1", pages = "21-27", month = "January", year = "2012", doi = "10.1016/j.cub.2011.11.026 ", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20120213-112818749", note = "© 2012 Elsevier Ltd. \n\nReceived: October 21, 2011; Revised: November 10, 2011; Accepted: November 10, 2011; Published online: December 15, 2011. \n\nWe thank Marie P. Suver for contributing to a set of preliminary experiments and useful conversations throughout the project. This work was supported by a National Science Foundation FIBR award 0623527 (M.H.D.) and a National Institutes of Health training grant 5-T32-MH019138 (P.T.W.).", revision_no = "25", abstract = "Insects maintain a constant bearing across a wide range of spatial scales. Monarch butterflies and locusts traverse continents [[1] and [2]], and foraging bees and ants travel hundreds of meters to return to their nests [[1], [3] and [4]], whereas many other insects fly straight for only a few centimeters before changing direction. Despite this variation in spatial scale, the brain region thought to underlie long-distance navigation is remarkably conserved [[5] and [6]], suggesting that the use of a celestial compass is a general and perhaps ancient capability of insects. Laboratory studies of Drosophila have identified a local search mode in which short, straight segments are interspersed with rapid turns [[7] and [8]]. However, this flight mode is inconsistent with measured gene flow between geographically separated populations [[9], [10] and [11]], and individual Drosophila can travel 10 km across desert terrain in a single night [[9], [12] and [13]]—a feat that would be impossible without prolonged periods of straight flight. To directly examine orientation behavior under outdoor conditions, we built a portable flight arena in which a fly viewed the natural sky through a liquid crystal device that could experimentally rotate the polarization angle. Our findings indicate that Drosophila actively orient using the sky's natural polarization pattern.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/25309, title ="Prior Mating Experience Modulates the Dispersal of Drosophila in Males More Than in Females \n", author = "Simon, Jasper C. and Dickson, William B.", journal = "Behavior Genetics", volume = "41", number = "5", pages = "754-767", month = "September", year = "2011", doi = "10.1007/s10519-011-9470-5", issn = "0001-8244", url = "https://resolver.caltech.edu/CaltechAUTHORS:20110912-150533522", note = "© 2011 The Author(s). This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. \n\nReceived: 19 September 2010; Accepted: 20 April 2011; Published online: 27 May 2011. \n\nWe thank R. Bailey for help in developing the circuit boards that run our technology; J. Birch for early drafts of the machine drawings used in the design of our hardware; M. Vondrus for help with machining various parts used in the construction of our experimental chambers; M. Sokolowski for fly strains; the late S. Benzer and members of his laboratory for much criticism; and finally, members of the Dickinson laboratory for experimental guidance\nand helpful discussions. This work was supported by NIH grant 5R01DA22777-3, NSF Engineering Research Center Grant EEC9407 226, and HHMI (J.C.S.).", revision_no = "15", abstract = "Cues from both an animal’s internal physiological state and its local environment may influence its decision to disperse. However, identifying and quantifying the causative factors underlying the initiation of dispersal is difficult in uncontrolled natural settings. In this study, we automatically monitored the movement of fruit flies and examined the influence of food availability, sex, and reproductive status on their dispersal between laboratory environments. In general, flies with mating experience behave as if they are hungrier than virgin flies, leaving at a greater rate when food is unavailable and staying longer when it is available. Males dispersed at a higher rate and were more active than females when food was unavailable, but tended to stay longer in environments containing food than did females. We found no significant relationship between weight and activity, suggesting the behavioral differences between males and females are caused by an intrinsic factor relating to the sex of a fly and not simply its body size. Finally, we observed a significant difference between the dispersal of the natural isolate used throughout this study and the widely-used laboratory strain, Canton-S, and show that the difference cannot be explained by allelic differences in the foraging gene. \n", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/23747, title ="Active and Passive Antennal Movements during Visually Guided Steering in Flying Drosophila", author = "Mamiya, Akira and Straw, Andrew D.", journal = "Journal of Neuroscience", volume = "31", number = "18", pages = "6900-6914", month = "May", year = "2011", doi = "10.1523/JNEUROSCI.0498-11.2011", issn = "0270-6474", url = "https://resolver.caltech.edu/CaltechAUTHORS:20110520-101227285", note = "© 2011 The Authors. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). \n\nReceived Jan. 28, 2011; revised March 10, 2011; accepted March 17, 2011. \n\nThis work was supported by National Science Foundation Frontiers in Integrative Biological Research Award 0623527 (M.H.D.). We thank Martin Peek for technical assistance and Gaby Maimon for helpful discussion and comments.\n\nAuthor contributions: A.M., A.D.S., and M.H.D. designed research; A.M. performed research; A.D.S. and E.T. contributed unpublished reagents/analytic tools; A.M. analyzed data; A.M. and M.H.D. wrote the paper.", revision_no = "23", abstract = "Insects use feedback from a variety of sensory modalities, including mechanoreceptors on their antennae, to stabilize the direction and speed of flight. Like all arthropod appendages, antennae not only supply sensory information but may also be actively positioned by control muscles. However, how flying insects move their antennae during active turns and how such movements might influence steering responses are currently unknown. Here we examined the antennal movements of flying Drosophila during visually induced turns in a tethered flight arena. In response to both rotational and translational patterns of visual motion, Drosophila actively moved their antennae in a direction opposite to that of the visual motion. We also observed two types of passive antennal movements: small tonic deflections of the antenna and rapid oscillations at wing beat frequency. These passive movements are likely the result of wing-induced airflow and increased in magnitude when the angular distance between the wing and the antenna decreased. In response to rotational visual motion, increases in passive antennal movements appear to trigger a reflex that reduces the stroke amplitude of the contralateral wing, thereby enhancing the visually induced turn. Although the active antennal movements significantly increased antennal oscillation by bringing the arista closer to the wings, it did not significantly affect the turning response in our head-fixed, tethered flies. These results are consistent with the hypothesis that flying Drosophila use mechanosensory feedback to detect changes in the wing induced airflow during visually induced turns and that this feedback plays a role in regulating the magnitude of steering responses.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/22657, title ="Multi-camera real-time three-dimensional tracking of multiple flying animals", author = "Straw, Andrew D. and Branson, Kristin", journal = "Journal of the Royal Society Interface", volume = "8", number = "56", pages = "395-409", month = "March", year = "2011", doi = "10.1098/rsif.2010.0230 ", issn = "1742-5689", url = "https://resolver.caltech.edu/CaltechAUTHORS:20110304-085606048", note = "© 2010 The Royal Society. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. \n\nReceived 19 April 2010. Accepted 21 June 2010. Published online 14 July 2010. \n\nThe data for figure 4 were gathered in collaboration with Douglas Altshuler. Sawyer Fuller helped with the EKF formulation, provided helpful feedback on the manuscript and, together with Gaby Maimon, Rosalyn Sayaman, Martin Peek and Aza Raskin, helped with physical construction of arenas and bug reports on the software. Pete Trautmann provided insight on data association, and Pietro Perona provided helpful suggestions on the manuscript. This work was supported by grants from the Packard Foundation, AFOSR (FA9550-06-1-0079), ARO (DAAD 19-03-D-0004), NIH (R01 DA022777) and NSF (0923802) to M.H.D. and AFOSR (FA9550-10-1-0086) to A.D.S.", revision_no = "23", abstract = "Automated tracking of animal movement allows analyses that would not otherwise be possible by providing great quantities of data. The additional capability of tracking in real time—with minimal latency—opens up the experimental possibility of manipulating sensory feedback, thus allowing detailed explorations of the neural basis for control of behaviour. Here, we describe a system capable of tracking the three-dimensional position and body orientation of animals such as flies and birds. The system operates with less than 40 ms latency and can track multiple animals simultaneously. To achieve these results, a multi-target tracking algorithm was developed based on the extended Kalman filter and the nearest neighbour standard filter data association algorithm. In one implementation, an 11-camera system is capable of tracking three flies simultaneously at 60 frames per second using a gigabit network of nine standard Intel Pentium 4 and Core 2 Duo computers. This manuscript presents the rationale and details of the algorithms employed and shows three implementations of the system. An experiment was performed using the tracking system to measure the effect of visual contrast on the flight speed of Drosophila melanogaster. At low contrasts, speed is more variable and faster on average than at high contrasts. Thus, the system is already a\nuseful tool to study the neurobiology and behaviour of freely flying animals. If combined with other techniques, such as ‘virtual reality’-type computer graphics or genetic manipulation, the tracking system would offer a powerful new way to investigate the biology of flying animals.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/20716, title ="Olfactory modulation of flight in Drosophila is sensitive, selective and rapid\n", author = "Bhandawat, Vikas and Maimon, Gaby", journal = "Journal of Experimental Biology", volume = "213", number = "21", pages = "3625-3635", month = "November", year = "2010", doi = "10.1242/jeb.040402 ", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20101108-113145488", note = "© 2010 Published by The Company of Biologists Ltd.\n\nAccepted 14 July 2010. First published online October 15, 2010. \n\nWe thank K. I. Nagel for help in data acquisition, assistance in writing the image analysis software, and helpful conversations. We are grateful to members of the Wilson lab for feedback on the manuscript. This work was funded by a grant from the NIH (R01DC008174), a McKnight Scholar Award, a Sloan Foundation Research Fellowship, and a Beckman Young Investigator Award (to R.I.W.), together with a grant from the NSF (FIBR 0623527, to M.H.D.). V.B. was partially supported by Charles A. King Trust Postdoctoral Fellowship. G.M. was supported by a Caltech Della Martin Fellowship. R.I.W. is an HHMI Early Career Scientist. \n\nV.B. and R.I.W. designed the experiments. V.B. collected the data. Pilot experiments were performed by V.B. with assistance from G.M. in the laboratory of M.H.D. Both G.M. and M.H.D. provided technical support and intellectual contributions. V.B. and R.I.W. wrote the manuscript. \n\nDeposited in PMC for releaseafter 12 months.", revision_no = "22", abstract = "Freely flying Drosophila melanogaster respond to odors by increasing their flight speed and turning upwind. Both these flight behaviors can be recapitulated in a tethered fly, which permits the odor stimulus to be precisely controlled. In this study, we investigated the relationship between these behaviors and odor-evoked activity in primary sensory neurons. First, we verified that these behaviors are abolished by mutations that silence olfactory receptor neurons (ORNs). We also found that antennal mechanosensors in Johnston's organ are required to guide upwind turns. Flight responses to an odor depend on the identity of the ORNs that are active, meaning that these behaviors involve odor discrimination and not just odor detection. Flight modulation can begin rapidly (within about 85 ms) after the onset of olfactory transduction. Moreover, just a handful of spikes in a single ORN type is sufficient to trigger these behaviors. Finally, we found that the upwind turn is triggered independently from the increase in wingbeat frequency, implying that ORN signals diverge to activate two independent and parallel motor commands. Together, our results show that odor-evoked flight modulations are rapid and sensitive responses to specific patterns of sensory neuron activity. This makes these behaviors a useful paradigm for studying the relationship between sensory neuron activity and behavioral decision-making in a simple and genetically tractable organism.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/20398, title ="Visual Control of Altitude in Flying Drosophila", author = "Straw, Andrew D. and Lee, Serin", journal = "Current Biology", volume = "20", number = "17", pages = "1550-1556", month = "September", year = "2010", doi = "10.1016/j.cub.2010.07.025", issn = "0960-9822", url = "https://resolver.caltech.edu/CaltechAUTHORS:20101012-100951687", note = "© 2010 Elsevier Ltd.\n\nReceived 18 May 2010; revised 11 June 2010; accepted 7 July 2010. Published online: August 19, 2010. Available online 19 August 2010.\n\nWe thank Sawyer Fuller for assistance in the construction of the projection\nand mirror system and Figure 1A, as well as Gaby Maimon for providing\nvaluable comments on the manuscript. This work was supported by grants\nfrom the Air Force Office of Scientific Research (AFOSR, FA9550-06-1-0079)\nand Army Research Office (DAAD 19-03-D-0004) to M.H.D., as well as\nAFOSR (FA9550-10-1-0085) to A.D.S.\n", revision_no = "32", abstract = "Unlike creatures that walk, flying animals need to control their horizontal motion as well as their height above the ground. Research on insects, the first animals to evolve flight, has revealed several visual reflexes that are used to govern horizontal course. For example, insects orient toward prominent vertical features in their environment [1], [2], [3], [4] and [5] and generate compensatory reactions to both rotations [6] and [7] and translations [1], [8], [9], [10] and [11] of the visual world. Insects also avoid impending collisions by veering away from visual expansion [9], [12], [13] and [14]. In contrast to this extensive understanding of the visual reflexes that regulate horizontal course, the sensory-motor mechanisms that animals use to control altitude are poorly understood. Using a 3D virtual reality environment, we found that Drosophila utilize three reflexes—edge tracking, wide-field stabilization, and expansion avoidance—to control altitude. By implementing a dynamic visual clamp, we found that flies do not regulate altitude by maintaining a fixed value of optic flow beneath them, as suggested by a recent model [15]. The results identify a means by which insects determine their absolute height above the ground and uncover a remarkable correspondence between the sensory-motor algorithms used to regulate motion in the horizontal and vertical domains.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/19702, title ="A linear systems analysis of the yaw dynamics of a dynamically scaled insect model", author = "Dickson, William B. and Polidoro, Peter", journal = "Journal of Experimental Biology", volume = "213", number = "17", pages = "3047-3061", month = "September", year = "2010", doi = "10.1242/jeb.042978 ", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100830-100025776", note = "© 2010 Published by The Company of Biologists Ltd. \n\nAccepted 23 April 2010. First published online August 13, 2010. \n\nWe thank Sawyer B. Fuller and Martin Y. Peek for technical advice and assistance. Research was supported by the Army Research Office (ARO) DAAD 19-003-D-0004, the National Science Foundation (NSF) FIBR 0623527, and The U.S. Army Research Laboratory Micro Autonomous Systems and Technology (MAST) Collaborative Technology Alliance.", revision_no = "12", abstract = "Recent studies suggest that fruit flies use subtle changes to their wing motion to actively generate forces during aerial maneuvers. In addition, it has been estimated that the passive rotational damping caused by the flapping wings of an insect is around two orders of magnitude greater than that for the body alone. At present, however, the relationships between the active regulation of wing kinematics, passive damping produced by the flapping wings and the overall trajectory of the animal are still poorly understood. In this study, we use a dynamically scaled robotic model equipped with a torque feedback mechanism to study the dynamics of yaw turns in the fruit fly Drosophila melanogaster. Four plausible mechanisms for the active generation of yaw torque are examined. The mechanisms deform the wing kinematics of hovering in order to introduce asymmetry that results in the active production of yaw torque by the flapping wings. The results demonstrate that the stroke-averaged yaw torque is well approximated by a model that is linear with respect to both the yaw velocity and the magnitude of the kinematic deformations. Dynamic measurements, in which the yaw torque produced by the flapping wings was used in real-time to determine the rotation of the robot, suggest that a first-order linear model with stroke-average coefficients accurately captures the yaw dynamics of the system. Finally, an analysis of the stroke-average dynamics suggests that both damping and inertia will be important factors during rapid body saccades of a fruit fly. \n", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/23690, title ="Detection of molecular gas in a distant submillimetre galaxy at z= 4.76 with Australia Telescope Compact Array", author = "Coppin, K. E. K. and Chapman, S. C.", journal = "Monthly Notices of the Royal Astronomical Society", volume = "407", number = "1", pages = "L103-L107", month = "September", year = "2010", doi = "10.1111/j.1745-3933.2010.00914.x", issn = "0035-8711", url = "https://resolver.caltech.edu/CaltechAUTHORS:20110517-102157085", note = "© 2010 The Authors. Journal compilation © 2010 Royal Astronomical Society. \n\nAccepted 2010 July 5. Received 2010 June 17; in original form 2010 April 22. Article first published online: 12 Aug. 2010. \n\nWe thank an anonymous referee for suggestions which improved the Letter. KEKC acknowledges support from a Science and Technology Facilities Council (STFC) fellowship. We thank John Helly, Carlton Baugh and Cedric Lacey for help with extracting information from the Millenium and GALFORM data bases. IS and JLW acknowledge support from STFC, and AMS acknowledges support from a Lockyer fellowship. JSD acknowledges the support of the Royal Society via a Wolfson Research merit Award. TRG acknowledges support from IDA. The DARK Cosmology Centre is funded by DNRF. The ATCA is part of the Australia Telescope which is funded by the Commonwealth of Australia for operation as a National Facility managed by CSIRO. We thank Stefano Zibetti and Nelson Padilla for the HAWK-I imaging which was obtained during ESO programme ID 082.A-0890.", revision_no = "26", abstract = "We have detected the CO(2–1) transition from the submillimetre galaxy (SMG) LESS J033229.4−275619 at z= 4.755 using the new Compact Array Broadband Backend system on the Australian Telescope Compact Array. These data have identified a massive gas reservoir available for star formation for the first time in an SMG at z~ 5. We use the luminosity and velocity width (full width at half-maximum, FWHM, of ≃160 km s^(−1)) of the CO(2–1) line emission to constrain the gas and dynamical mass of M_(gas)≃ 1.6 × 10^(10) M_⊙ and Mdyn(<2 kpc) ≃ 5 × 10^(10) (0.25/sin^(2)i) M_⊙, respectively, similar to that observed for SMGs at lower redshifts of z~ 2–4, although we note that our observed CO FWHM is a factor of ~3 narrower than typically seen in SMGs. Together with the stellar mass we estimate a total baryonic mass of M_(bary)≃ 1 × 10^(11) M_⊙, consistent with the dynamical mass for this young galaxy within the uncertainties. Dynamical and baryonic mass limits of high-redshift galaxies are useful tests of galaxy formation models: using the known z~ 4–5 SMGs as examples of massive baryonic systems, we find that their space density is consistent with that predicted by current galaxy formation models. In addition, these observations have helped to confirm that z~ 4–5 SMGs possess the baryonic masses and gas consumption time-scales necessary to be the progenitors of the luminous old red galaxies seen at z~ 3. Our results provide a preview of the science that ALMA will enable on the formation and evolution of the earliest massive galaxies in the Universe.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/19057, title ="Neuromuscular control of wingbeat kinematics in Anna's hummingbirds (Calypte anna)", author = "Altshuler, Douglas L. and Welch, Kenneth C., Jr.", journal = "Journal of Experimental Biology", volume = "213", number = "14", pages = "2507-2514", month = "July", year = "2010", doi = "10.1242/jeb.043497", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100714-154823395", note = "© 2010 Published by The Company of Biologists Ltd. \n\nAccepted 11 April 2010. First published online June 25, 2010. \n\nWe thank Scott Currie and Bob Josephson for comments on the manuscript and Qing Liu for assistance with digitization. Funding for this research was provided by a University of California Regents Faculty Fellowship, a National Institutes of Health National Research Service Award (5F32NS046221), and a National Science Foundation Award (IOS 0923849) to D.L.A., and by a National Science Foundation Award (IOS 0217229) to M.H.D. Deposited in PMC for release after 12 months.", revision_no = "13", abstract = "Hummingbirds can maintain the highest wingbeat frequencies of any flying vertebrate – a feat accomplished by the large pectoral muscles that power the wing strokes. An unusual feature of these muscles is that they are activated by one or a few spikes per cycle as revealed by electromyogram recordings (EMGs). The relatively simple nature of this activation pattern provides an opportunity to understand how motor units are recruited to modulate limb kinematics. Hummingbirds made to fly in low-density air responded by moderately increasing wingbeat frequency and substantially increasing the wing stroke amplitude as compared with flight in normal air. There was little change in the number of spikes per EMG burst in the pectoralis major muscle between flight in normal and low-density heliox (mean=1.4 spikes cycle^(–1)). However the spike amplitude, which we take to be an indication of the number of active motor units, increased in concert with the wing stroke amplitude, 1.7 times the value in air. We also challenged the hummingbirds using transient load lifting to elicit maximum burst performance. During maximum load lifting, both wing stroke amplitude and wingbeat frequency increased substantially above those values during hovering flight. The number of spikes per EMG burst increased to a mean of 3.3 per cycle, and the maximum spike amplitude increased to approximately 1.6 times those values during flight in heliox. These results suggest that hummingbirds recruit additional motor units (spatial recruitment) to regulate wing stroke amplitude but that temporal recruitment is also required to maintain maximum stroke amplitude at the highest wingbeat frequencies.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/19035, title ="Object preference by walking fruit flies, Drosophila melanogaster, is mediated by vision and graviperception", author = "Robie, Alice A. and Straw, Andrew D.", journal = "Journal of Experimental Biology", volume = "213", number = "14", pages = "2494-2506", month = "July", year = "2010", doi = "10.1242/jeb.041749 ", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100713-141548440", note = "© 2010 Published by The Company of Biologists Ltd.\n\n\nAccepted 7 April 2010.\n\nThe authors thank Kristin Branson for her discussions of behavioral analysis, as\nwell as Martin Peek and Neil Halelamien for their help developing the first version\nof the arena and tracking software. This work was supported by grants from the\nNational Institutes of Health (R01DA022777-04; A.R.), and the National Science\nFoundation (0623527) to M.H.D. Deposited in PMC for release after 12 months.", revision_no = "30", abstract = "Walking fruit flies, Drosophila melanogaster, use visual information to orient towards salient objects in their environment,\npresumably as a search strategy for finding food, shelter or other resources. Less is known, however, about the role of vision or\nother sensory modalities such as mechanoreception in the evaluation of objects once they have been reached. To study the role\nof vision and mechanoreception in exploration behavior, we developed a large arena in which we could track individual fruit flies\nas they walked through either simple or more topologically complex landscapes. When exploring a simple, flat environment\nlacking three-dimensional objects, flies used visual cues from the distant background to stabilize their walking trajectories. When\nexploring an arena containing an array of cones, differing in geometry, flies actively oriented towards, climbed onto, and explored\nthe objects, spending most of their time on the tallest, steepest object. A fly’s behavioral response to the geometry of an object\ndepended upon the intrinsic properties of each object and not a relative assessment to other nearby objects. Furthermore, the\npreference was not due to a greater attraction towards tall, steep objects, but rather a change in locomotor behavior once a fly\nreached and explored the surface. Specifically, flies are much more likely to stop walking for long periods when they are perched\non tall, steep objects. Both the vision system and the antennal chordotonal organs (Johnston’s organs) provide sufficient\ninformation about the geometry of an object to elicit the observed change in locomotor behavior. Only when both these sensory\nsystems were impaired did flies not show the behavioral preference for the tall, steep objects.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/18423, title ="Drosophila fly straight by fixating objects in the face of expanding optic flow", author = "Reiser, Michael B. and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "213", number = "10", pages = "1771-1781", month = "May", year = "2010", doi = "10.1242/jeb.035147 ", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100525-105422563", note = "© 2010 The Company of Biologists Ltd. \n\nAccepted 30 January 2010. \n\nWe thank Dr Mark Frye for constructive discussion during the early stages of this project. This work was supported by the Institute for Collaborative Biotechnologies through grant DAAD 19-03-D-0004 from the US Army Research Office, by NSF award 0623527 to M.H.D. and the CNSE Engineering Research Center at Caltech though NSF award EEC-9402726. We are grateful to the Howard Hughes Medical Institute for supporting M.B.R. as a Janelia Fellow. Deposited in PMC for release after 6 months.", revision_no = "27", abstract = "Flies, like all animals that depend on vision to navigate through the world, must integrate the optic flow created by self-motion with the images generated by prominent features in their environment. Although much is known about the responses of Drosophila melanogaster to rotating flow fields, their reactions to the more complex patterns of motion that occur as they translate through the world are not well understood. In the present study we explore the interactions between two visual reflexes in Drosophila: object fixation and expansion avoidance. As a fly flies forward, it encounters an expanding visual flow field. However, recent results have demonstrated that Drosophila strongly turn away from patterns of expansion. Given the strength of this reflex, it is difficult to explain how flies make forward progress through a visual landscape. This paradox is partially resolved by the finding reported here that when undergoing flight directed towards a conspicuous object, Drosophila will tolerate a level of expansion that would otherwise induce avoidance. This navigation strategy allows flies to fly straight when orienting towards prominent visual features. \n", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/17754, title ="Active flight increases the gain of visual motion processing in Drosophila", author = "Maimon, Gaby and Straw, Andrew D.", journal = "Nature Neuroscience", volume = "13", number = "3", pages = "393-399", month = "March", year = "2010", doi = "10.1038/nn.2492 ", issn = "1097-6256", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100316-105718344", note = "© 2010 Nature Publishing Group.\nReceived 08 September 2009. Accepted 28 December 2009. Published online 14 February 2010.\nWe thank J. Assad, V. Bhandawat, G. Card, C. Chiu, M. Do, T. Herrington, W. Korff, G. Laurent, M. Murthy, P. Polidoro, G. Turner and R. Wilson for helpful discussion, comments and aid in developing the preparation. We are grateful to L. Luo for the Gal4-3a fly line. This work was supported by a National Science Foundation Frontiers in Integrative Biological Research 0623527 award (M.H.D.) and a Caltech Della Martin fellowship (G.M.).\nAuthor Contributions: \nG.M., A.D.S. and M.H.D. designed the experiments. G.M. and M.H.D. wrote the paper. G.M. developed the preparation, conducted the experiments and analyzed the data. A.D.S. designed the software and hardware system for tracking wing beat amplitudes in real time. ", revision_no = "17", abstract = "We developed a technique for performing whole-cell patch-clamp recordings from genetically identified neurons in behaving Drosophila. We focused on the properties of visual interneurons during tethered flight, but this technique generalizes to different cell types and behaviors. We found that the peak-to-peak responses of a class of visual motion–processing interneurons, the vertical-system visual neurons (VS cells), doubled when flies were flying compared with when they were at rest. Thus, the gain of the VS cells is not fixed, but is instead behaviorally flexible and changes with locomotor state. Using voltage clamp, we found that the passive membrane resistance of VS cells was reduced during flight, suggesting that the elevated gain was a result of increased synaptic drive from upstream motion-sensitive inputs. The ability to perform patch-clamp recordings in behaving Drosophila promises to help unify the understanding of behavior at the gene, cell and circuit levels.\n\n", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/17591, title ="A New Chamber for Studying the Behavior of Drosophila", author = "Simon, Jasper C. and Dickinson, Michael H.", journal = "PLoS ONE", volume = "5", number = "1", pages = "e8793", month = "January", year = "2010", doi = "10.1371/journal.pone.0008793", issn = "1932-6203", url = "https://resolver.caltech.edu/CaltechAUTHORS:20100225-094228460", note = "© 2010 Simon, Dickinson. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.\n\nReceived: November 6, 2009; accepted: December 2, 2009; published: January 27, 2010.\nEditor: Kenji Hashimoto, Chiba University Center for Forensic Mental Health, Japan.\nFunding for this research was provided by United States National Institutes of Health grant 320 R01 DA022777 (to MHD). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.\n\nWe thank Kristin Branson, Andrew Straw, and Heiko Dankert for council\nregarding the use of their software. Pietro Perona and Peter Polidoro\ncontributed to the design of early chambers. We thank Mike Vondrus and\nPeter Polidoro for help machining early prototypes of the new chamber.\nDavid Anderson and members of his laboratory, Liming Wang and Kiichi\nWatanabe, provided space, advice, and the CS strain for the courtship and\naggression trials. We thank Kristin Branson for help producing the\nsupplementary movies.\nAuthor contributions: Conceived and designed the experiments: JCS. Performed the experiments:\nJCS. Analyzed the data: JCS. Wrote the paper: JCS MD.\nConceived and developed the technology: JCS.", revision_no = "62", abstract = "Methods available for quickly and objectively quantifying the behavioral phenotypes of the fruit fly, Drosophila melanogaster, lag behind in sophistication the tools developed for manipulating their genotypes. We have developed a simple, easy-to-replicate, general-purpose experimental chamber for studying the ground-based behaviors of fruit flies. The major innovative feature of our design is that it restricts flies to a shallow volume of space, forcing all behavioral interactions to take place within a monolayer of individuals. The design lessens the frequency that flies occlude or obscure each other, limits the variability in their appearance, and promotes a greater number of flies to move throughout the center of the chamber, thereby increasing the frequency of their interactions. The new chamber design improves the quality of data collected by digital video and was conceived and designed to complement automated machine vision methodologies for studying behavior. Novel and improved methodologies for better quantifying the complex behavioral phenotypes of Drosophila will facilitate studies related to human disease and fundamental questions of behavioral neuroscience.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/15393, title ="Flight Dynamics and Control of Evasive Maneuvers: The Fruit Fly's Takeoff", author = "Zabala, Francisco A. and Card, Gwyneth M.", journal = "IEEE Transactions on Biomedical Engineering", volume = "56", number = "9, par", pages = "2295-2298", month = "September", year = "2009", doi = "10.1109/TBME.2009.2027606", issn = "0018-9294", url = "https://resolver.caltech.edu/CaltechAUTHORS:20090828-100125867", note = "© Copyright 2009 IEEE. \n\nManuscript received February 10, 2009; revised June 04, 2009. First published July 28, 2009; current version published August 14, 2009. \n\n", revision_no = "13", abstract = "We have approached the problem of reverse-engineering the flight control mechanism of the fruit fly by studying the dynamics of the responses to a visual stimulus during takeoff. Building upon a prior framework [G. Card and M. Dickinson, J. Exp. Biol., vol. 211, pp. 341–353, 2008], we seek to understand the strategies employed by the animal to stabilize attitude and orientation during these evasive, highly dynamical maneuvers. As a first step, we consider the dynamics from a gray-box perspective: examining lumped forces produced by the insect's legs and wings. The reconstruction of the flight initiation dynamics, based on the unconstrained motion formulation for a rigid body, allows us to assess the fly's responses to a variety of initial conditions induced by its jump. Such assessment permits refinement by using a visual tracking algorithm to extract the kinematic envelope of the wings [E. I. Fontaine, F. Zabala, M. Dickinson, and J. Burdick, “Wing and body motion during flight initiation in Drosophila revealed by automated visual tracking,” submitted for publication] in order to estimate lift and drag forces [F. Zabala, M. Dickinson, and R. Murray, “Control and stability of insect flight during highly dynamical maneuvers,” submitted for publication], and recording actual leg-joint kinematics and using them to estimate jump forces [F. Zabala, “A bio-inspired model for directionality control of flight initiation,” to be published.]. In this paper, we present the details of our approach in a comprehensive manner, including the salient results.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/15113, title ="Biofluiddynamic scaling of flapping, spinning and translating fins and wings", author = "Lentink, David and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "212", number = "16", pages = "2691-2704", month = "August", year = "2009", doi = "10.1242/jeb.022251", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20090817-144817248", note = "© The Company of Biologists Ltd 2009. \n\nAccepted 5 February 2009. First published online July 31, 2009. \n\nWe gratefully acknowledge Will Dickson, Koert Lindenburg and John Dabiri for proof reading preliminary versions of the manuscript. We thank Thomas Daniel for proof reading the final manuscript. We thank Johan van Leeuwen and GertJan van Heijst for hearty support, encouragement and proof reading of the various versions of the manuscript. This research is supported by NWO-ALW grant 817.02.012 to D.L. and by NSF grant IBN-0217229 to M.H.D.", revision_no = "11", abstract = "Organisms that swim or fly with fins or wings physically interact with the surrounding water and air. The interactions are governed by the morphology and kinematics of the locomotory system that form boundary conditions to the Navier–Stokes (NS) equations. These equations represent Newton's law of motion for the fluid surrounding the organism. Several dimensionless numbers, such as the Reynolds number and Strouhal number, measure the influence of morphology and kinematics on the fluid dynamics of swimming and flight. There exists, however, no coherent theoretical framework that shows how such dimensionless numbers of organisms are linked to the NS equation. Here we present an integrated approach to scale the biological fluid dynamics of a wing that flaps, spins or translates. Both the morphology and kinematics of the locomotory system are coupled to the NS equation through which we find dimensionless numbers that represent rotational accelerations in the flow due to wing kinematics and morphology. The three corresponding dimensionless numbers are (1) the angular acceleration number, (2) the centripetal acceleration number, and (3) the Rossby number, which measures Coriolis acceleration. These dimensionless numbers consist of length scale ratios, which facilitate their geometric interpretation. This approach gives fundamental insight into the physical mechanisms that explain the differences in performance among flapping, spinning and translating wings. Although we derived this new framework for the special case of a model fly wing, the method is general enough to make it applicable to other organisms that fly or swim using wings or fins.", } @article {CaltechAUTHORS_https://authors.library.caltech.edu/id/eprint/15114, title ="Rotational accelerations stabilize leading edge vortices on revolving fly wings", author = "Lentink, David and Dickinson, Michael H.", journal = "Journal of Experimental Biology", volume = "212", number = "16", pages = "2705-2719", month = "August", year = "2009", doi = "10.1242/jeb.022269", issn = "0022-0949", url = "https://resolver.caltech.edu/CaltechAUTHORS:20090817-144817394", note = "© The Company of Biologists Ltd 2009. \n\nAccepted 19 April 2009. First published online July 31, 2009. \n\nSupplementary material available online at http://jeb.biologists.org/cgi/content/full/212/16/2705/DC1 \n\nWe gratefully acknowledge Will Dickson for help with the experimental setup, valuable suggestions and proof reading the manuscript, and Andrew Straw for helping with the video set-up. We also thank Douglas Althshuler for valuable comments and lending his waterproof force sensor. And we thank Ulrike Müller, Jim Usherwood, Mees Muller, John Dabiri and GertJan van Heijst for valuable comments. We acknowledge Koert Lindenburg for proof reading the manuscript and mathematical derivations. We thank Johan van Leeuwen for hearty support, encouragement and proof reading of the various versions of the manuscript. Finally D.L. wishes to thank Peter Bakker, Hester Bijl and Bas van Oudheusden for helping him obtain travel bursaries for this research. This research is supported by travel bursaries of the Netherlands Organization for Scientific Research, the Journal of Experimental Biology and the J. M. Burgerscentrum for fluid dynamic research and NWO-ALW grant 817.02.012 to D.L. and a Grant from the National Science Foundation (IBN-0217229) and Packard Foundation (2001-17741A) to M.H.D.", revision_no = "20", abstract = "The aerodynamic performance of hovering insects is largely explained by the presence of a stably attached leading edge vortex (LEV) on top of their wings. Although LEVs have been visualized on real, physically modeled, and simulated insects, the physical mechanisms responsible for their stability are poorly understood. To gain fundamental insight into LEV stability on flapping fly wings we expressed the Navier–Stokes equations in a rotating frame of reference attached to the wing's surface. Using these equations we show that LEV dynamics on flapping wings are governed by three terms: angular, centripetal and Coriolis acceleration. Our analysis for hovering conditions shows that angular acceleration is proportional to the inverse of dimensionless stroke amplitude, whereas Coriolis and centripetal acceleration are proportional to the inverse of the Rossby number. Using a dynamically scaled robot model of a flapping fruit fly wing to systematically vary these dimensionless numbers, we determined which of the three accelerations mediate LEV stability. Our force measurements and flow visualizations indicate that the LEV is stabilized by the `quasi-steady' centripetal and Coriolis accelerations that are present at low Rossby number and result from the propeller-like sweep of the wing. In contrast, the unsteady angular acceleration that results from the back and forth motion of a flapping wing does not appear to play a role in the stable attachment of the LEV. Angular acceleration is, however, critical for LEV integrity as we found it can mediate LEV spiral bursting, a high Reynolds number effect. Our analysis and experiments further suggest that the mechanism responsible for LEV stability is not dependent on Reynolds number, at least over the range most relevant for insect flight (100