The flight system of the fly is remarkable. A fly can execute an escape maneuver in milliseconds, compensate for wing damage when half of the wing is missing, fly in turbulent conditions, and migrate over large distances. While there are many factors that contribute to the robustness and versatility of insect flight, it is the mechanical encoding of wing motion in the wing hinge that allows flies to rapidly and accurately change wing motion over a large dynamic range. The wing hinge consists of several hardened skeletal elements, named sclerites, and a set of twelve steering muscles are attached to some of these components within the exoskeleton. Due to the anatomical complexity and minute size of the sclerites, the way in which the steering muscles alter the mechanical encoding of wing motion in the hinge is poorly understood.
Using genetically encoded calcium indicators and high-speed videography, is is possible to simultaneously image steering muscle activity and wing motion. In order to extract wing pose from the high-speed video frames, an automated tracking algorithm was developed, that used a neural network and model fitting to accurately reconstruct the wing kinematics. The synchronous recordings of wing motion and steering muscle activity were used to train a convolutional neural network that learned to accurately predict the wing kinematics from muscle activity patterns. After training, the convolutional neural network was used to perform virtual experiments, revealing how the steering muscles regulate wing motion. Correlation analysis revealed that the 12 steering muscles have highly correlated activity. The correlation of muscle activity can be approximated well by a 12D-plane, in which all activity has to reside.
To study the function of the sclerites, a bottleneck was introduced in the convolutional neural network. The bottleneck consists of five neurons, or latent parameters, four parameters corresponding to the state of the different sclerites, on which the steering muscles act, and one parameter representing the wingbeat frequency. This so called latent network predicts both the changes in wing motion and muscle activity patterns as a function of sclerite state. The predicted wing motion as a function of sclerite state matches with previous anatomy and electrophysiology studies for the basalare, first axillary and third axillary sclerites. The fourth axillary sclerite has not been studied before, but shows an antagonistic relationship between the hg1,2 and hg3,4 muscles, resulting in a strong decrease and increase, respectively, of stroke amplitude, deviation and wing pitch angles.
By replaying the wing kinematics of the virtual experiments on a dynamically scaled robotic fly, a model of the aerodynamic and inertial control forces as a function of steering muscle activity was constructed. This control force model was subsequently integrated in a state-space system of fly flight, which in turn was integrated in a model predictive control simulation that was used to simulate free flight maneuvers. The body motion, steering muscle activity, and wing kinematics of the model predictive control simulations were strikingly similar to the recorded maneuvers of free-flying flies.
The integrative, multi-disciplinary approach that was used to reveal the mechanical logic of the wing hinge, and the control problem that a fly needs to solve to stay airborne, are both unprecedented in prior literature. The methodologies and models of this study will be a valuable resource in future research on how the fly’s nervous system controls the complex behavior that is flight.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/yyjd-a554, author = {Palmer, Emily Hope}, title = {Locomotory Control Algorithms and Their Neuronal Implementation in Drosophila melanogaster}, school = {California Institute of Technology}, year = {2023}, doi = {10.7907/yyjd-a554}, url = {https://resolver.caltech.edu/CaltechTHESIS:05192023-015643241}, abstract = {Scientists and engineers alike have long looked to animals in their pursuit of understanding the natural world and how best to interact with it. While researchers have looked across diverse classes, insects have been extensively studied for their rich diversity of life histories and abilities to perform at spatial and temporal scales difficult for engineered systems. Within insects, the fruit fly, Drosophila melanogaster, is a particularly well-studied organism because of its experimental tractability and status as a genetic model organism, providing both detailed descriptions of a broad suite of behaviors and access to and control over specific sets of tissue. In this work, we make use of these tools to study two behaviors in Drosophila, local search, the behavior in which walking flies will search the area around a food site in search of other food sources nearby, and the optomotor response, wherein they will stabilize in response to visual motion during flight. In these studies, we will use modern techniques from both biology and engineering, to exhaustively characterize and describe the observed behaviors and attempt to untangle the underlying algorithms and their neuronal implementation.
First, we explore the algorithmic structure of local search in fruit flies. When flies encounter a piece of food, they will often perform walking searches nearby; as food tends to be patchy in natural settings, searches may allow flies to locate other food sites in the area. We induce local search using optogenetic stimulation of sugar-sensing neurons and constrain the flies to a dark, annular arena. These experimental details result in a simplified behavior, as the fly has access to a limited sensory environment, so that the search can be interpreted as an example of idiothetic path integration, and the search itself is one-dimensionalized and therefore more easily analyzed. Our experiments, in tandem with complementary modeling using a state transition diagram formalization of the behaviors, generate two principle findings. First, flies can integrate their location in two dimensions–after the optogenetic activation is disabled and the flies can no longer receive the food stimulus, they will continue to search over the former food site even after completing a full revolution of the annular arena. Second, when multiple food sites are present, they search over a center of the food sites, rather than over one distinct food site. These results both provide insights into the algorithmic structure of local search and an experimental and descriptive paradigm for further inquiries into the behavior.
Second, we investigate the role of a population of neurons, the DNg02s, in the optomotor response. In response to visual patterns of wide-field motion, such that the entire world is moving in the fly-centric reference frame, the animal will attempt to steer to cancel the visual motion, as the most parsimonious explanation of the motion is that the fly itself is moving in the global reference frame. We demonstrate that the DNg02 neurons are a required component in the neural circuitry underlying the optomotor response, but that they are insufficient to induce steering behaviors. We conclude with a set of models that fully recapitulate the collected dataset. With current techniques, distinguishing between the two possible models of the downstream connectivity from the DNg02s to the motor neurons associated with wing motor output is not possible. However, as new datasets become available, particularly complete connectomes of the Drosophila nervous system, the neuronal pathways from the DNg02s to the motor systems may be elucidated.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/part-mf19, author = {de Souza, Alysha Maria}, title = {Sparse Neural and Motor Networks Underlying Control in the Drosophila Flight System}, school = {California Institute of Technology}, year = {2022}, doi = {10.7907/part-mf19}, url = {https://resolver.caltech.edu/CaltechTHESIS:10312021-193119771}, abstract = {We often look to the natural world for inspiration in design and engineering. The fruit fly, Drosophila melanogaster, with approximately 100,000 neurons in its central nervous system (CNS) versus the roughly 100 billion neurons of the human brain, is relatively uncompromising in the richness of behaviors it is capable of performing given its comparatively sparse nervous system. It exhibits exceptional aerial agility, despite the steep aerodynamic constraints of miniaturization thanks to unique physiological and biomechanical thoracic adaptations. However, the mechanisms governing its sparse and precise flight control have remained largely inaccessible due to technological and geometric limitations, leaving many long-standing questions in the field of insect flight control unexplored. Recent advances in the field of molecular biology have created a vast toolkit for both optical imaging and genetic manipulation of cellular function. This revolution of genetic advances allows us to visualize changes in muscle activity in situ as fluorescent signals, to record from fluorescently targeted cells via electrophysiology or 2-photon imaging, and to optogenetically activate or silence the activity of targeted cells. This thesis utilizes recent technological and molecular advances to probe three key aspects of fly flight control: 1) the dynamic interactions of flight steering muscles to produce flight maneuvers, 2) the source of timing information for the structuring of the the motor phase code, an extremely temporally precise wingbeat-synchronous aspect neural firing, and 3) the mechanisms by which slow, graded descending visual process recruit the flight muscles.
In the contents of the ensuing chapters I propose mechanisms for flight control pertaining to the wing muscles as well as their inputs. First, I describe the activities of each of the flight steering muscles in response to visual motion to generate movement in yaw, pitch, and roll (Chapter II). I then characterize the flexible individual dynamics and combinatorial timing of the system, and propose specific mechanisms by which interneurons rather than muscle physiology govern these adaptable firing patterns according to sensory inputs(Chapter II). Sensory inputs within this thesis take two forms: thoracic mechanosensory and timing information as well as descending visual input. I characterize mechanosensory and timing adaptations of an evolutionarily evolved hind wing, as well as the impact of haltere feedback to flight control (Chapter III). Lastly, I propose a mechanism by which descending visual commands produce graded outputs of the muscles.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/WSE4-WG98, author = {van Breugel, Floris}, title = {Complex Behavior and Perception in Drosophila Emerges from Iterative Feedback-Regulated Reflexes}, school = {California Institute of Technology}, year = {2014}, doi = {10.7907/WSE4-WG98}, url = {https://resolver.caltech.edu/CaltechTHESIS:01032014-164946523}, abstract = {For a hungry fruit fly, locating and landing on a fermenting fruit where it can feed, find mates, and lay eggs, is an essential and difficult task requiring the integration of both olfactory and visual cues. Understanding how flies accomplish this will help provide a comprehensive ethological context for the expanding knowledge of their neural circuits involved in processing olfaction and vision, as well as inspire novel engineering solutions for control and estimation in computationally limited robotic applications. In this thesis, I use novel high throughput methods to develop a detailed overview of how flies track odor plumes, land, and regulate flight speed. Finally, I provide an example of how these insights can be applied to robotic applications to simplify complicated estimation problems. To localize an odor source, flies exhibit three iterative, reflex-driven behaviors. Upon encountering an attractive plume, flies increase their flight speed and turn upwind using visual cues. After losing the plume, flies begin zigzagging crosswind, again using visual cues to control their heading. After sensing an attractive odor, flies become more attracted to small visual features, which increases their chances of finding the plume source. Their changes in heading are largely controlled by open-loop maneuvers called saccades, which they direct towards and away from visual features. If a fly decides to land on an object, it begins to decelerate so as to maintain a stereotypical ratio of expansion to retinal size. Once they reach a stereotypical distance from the target, flies extend their legs in preparation for touchdown. Although it is unclear what cues they use to trigger this behavior, previous studies have indicated that it is likely under visual control. In Chapter 3, I use a nonlinear control theoretic analysis and robotic testbed to propose a novel and putative mechanism for how a fly might visually estimate distance by actively decelerating according to a visual control law. Throughout these behaviors, a common theme is the visual control of flight speed. Using genetic tools I show that the neuromodulator octopamine plays an important role in regulating flight speed, and propose a neural circuit for how this controller might be implemented in the flies brain. Two general biological and engineering principles are evident across my experiments: (1) complex behaviors, such as foraging, can emerge from the interactions of simple independent sensory-motor modules; (2) flies control their behavior in such a way that simplifies complex estimation problems.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/DJKK-TC21, author = {Suver, Marie Patricia}, title = {Octopamine Neurons Mediate Flight-Induced Modulation of Visual Processing in Drosophila melanogaster}, school = {California Institute of Technology}, year = {2014}, doi = {10.7907/DJKK-TC21}, url = {https://resolver.caltech.edu/CaltechTHESIS:08162013-150835965}, abstract = {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, and often their functional consequences, remain poorly characterized. I investigated the role of octopamine neurons in the flight-dependent modulation observed in visual interneurons in the fruit fly Drosophila melanogaster. 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 neurons that project to the optic lobes increase in activity during flight. Using genetic tools to manipulate the activity of octopamine neurons, I find that they are both necessary and sufficient for the flight-induced visual boost. This work provides the first evidence that endogenous release of octopamine is involved in state-dependent modulation of visual interneurons in flies. Further, I investigated the role of a single pair of octopamine neurons that project to the optic lobes, and found no evidence that chemical synaptic transmission via these neurons is necessary for the flight boost. However, I found some evidence that activation of these neurons may contribute to the flight boost. Wind stimuli alone are sufficient to generate transient increases in the VS cell response to motion vision, but result in no increase in baseline membrane potential. These results suggest that the flight boost originates not from a central command signal during flight, but from mechanosensory stimuli relayed via the octopamine system. Lastly, in an attempt to understand the functional consequences of the flight boost observed in visual interneurons, we measured the effect of inactivating octopamine neurons in freely flying flies. We found that flies whose octopamine neurons we silenced accelerate less than wild-type flies, consistent with the hypothesis that the flight boost we observe in VS cells is indicative of a gain control mechanism mediated by octopamine neurons. Together, this work serves as the basis for a mechanistic and functional understanding of octopaminergic modulation of vision in flying flies.}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/MSRS-JG88, author = {Elzinga, Michael John}, title = {Flight Dynamics in Drosophila Through a Dynamically-scaled Robotic Approach}, school = {California Institute of Technology}, year = {2013}, doi = {10.7907/MSRS-JG88}, url = {https://resolver.caltech.edu/CaltechTHESIS:06072013-110839676}, abstract = {Flies are particularly adept at balancing the competing demands of delay tolerance, performance, and robustness during flight, which invites thoughtful examination of their multimodal feedback architecture. This dissertation examines stabilization requirements for inner-loop feedback strategies in the flapping flight of Drosophila, the fruit fly, against the backdrop of sensorimotor transformations present in the animal. Flies have evolved multiple specializations to reduce sensorimotor latency, but sensory delay during flight is still significant on the timescale of body dynamics. I explored the effect of sensor delay on flight stability and performance for yaw turns using a dynamically-scaled robot equipped with a real-time feedback system that performed active turns in response to measured yaw torque. The results show a fundamental tradeoff between sensor delay and permissible feedback gain, and suggest that fast mechanosensory feedback provides a source of active damping that 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.
Additionally, I investigated how flies adjust stroke features to regulate and stabilize level forward flight. The results suggest that few changes to hovering kinematics are actually required to meet steady-state lift and thrust requirements at different flight speeds, 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. The results also show that the dynamics may be stabilized with additional pitch damping, but the magnitude of required damping increases with flight speed. I posit that differences in stroke deviation between the upstroke and downstroke might play a critical role in this stabilization. Fast mechanosensory feedback of the pitch rate could enable active damping, which would inherently exhibit gain scheduling with flight speed if pitch torque is regulated by adjusting stroke deviation. Such a control scheme would provide an elegant solution for flight stabilization across a wide range of flight speeds.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/3VXQ-TE73, author = {Weir, Peter Thomas}, title = {Polarization-Based Navigation in Drosophila}, school = {California Institute of Technology}, year = {2013}, doi = {10.7907/3VXQ-TE73}, url = {https://resolver.caltech.edu/CaltechTHESIS:07242012-154851161}, abstract = {
Insects maintain a constant bearing across a wide range of spatial scales. Monarch butterflies and locusts traverse continents (Williams, 1957; Wehner, 1984), and foraging bees and ants travel hundreds of meters to return to their nests (Dyer, 1996; Wehner, 1984, 2003), 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 (Loesel et al., 2002; Homberg, 2008), 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 (Mayer et al., 1988; Bender and Dickinson, 2006). However, this flight mode is inconsistent with measured gene flow between geographically separated populations (Jones et al., 1981; Slatkin, 1985; Turelli and Hoffmann, 1991), and individual Drosophila can travel 10 km in a single night (Yerington, 1961; Jones et al., 1981; Coyne et al., 1982, 1987) – a feat that would be impossible without prolonged periods of straight flight. One well-known cue relevant to orientation and navigation is the pattern of polarization of skylight. To study possible mechanisms of orientation to skylight polarization, we built an arena in which we could observe individual flight responses to rotating the angle of polarized light in the laboratory. We found that flies robustly steer in response to changes in the polarization angle of light. Individual flies also stabilize a particular polarization plane when they are given closed-loop control of such a stimulus. To directly examine orientation behavior under outdoor conditions, we built two portable flight arenas in which a fly viewed the natural sky through a clear aperture. In the first we examined the ability of flies to compensate for external rotations with or without the aid of skylight polarization. The second arena contained a liquid crystal device that could experimentally rotate the polarization angle of the skylight. In both outdoor arenas we tracked fly orientation using a digital video camera and custom computer vision system. Our findings indicate that Drosophila actively orient using the sky’s natural polarization pattern.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/Z3D0-GG27, author = {Fuller, Sawyer Buckminster}, title = {Steady as She Goes: Visual Autocorrelators and Antenna-Mediated Airspeed Feedback in the Control of Flight Dynamics in Fruit Flies and Robotics}, school = {California Institute of Technology}, year = {2011}, doi = {10.7907/Z3D0-GG27}, url = {https://resolver.caltech.edu/CaltechThesis:06082011-191034348}, abstract = {Achieving agile autonomous flight by an insect-sized micro aerial vehicle (MAV) will require improved technology that is radically smaller, lighter, and more power-efficient. One animal that has solved the problem is the fly, a virtuoso among insect flyers whose nervous system can perform sophisticated aerial maneuvers under severe computational constraints. This thesis is concerned with understanding and emulating the dynamics of the fly’s feedback control system. Because vision is noisy and information rich, processing time may a problem for a fast-moving MAV or fly. By tracking the fruit fly Drosophila melanogaster in free flight in gusts of wind, I found that they incorporate feedback from wind-sensing antennae in a fast feedback loop that dampens the forward-flight dynamics. The slower dynamics are easier to control for long-delay visual feedback, making the fly more robust to the limitations of its visual system. Using the fly as inspiration, I designed a minimal, visual autocorrelation based controller that used a small array of visual sensors to stabilize a fan-actuated hovercraft robot in a narrow corridor. Using a model for correlators developed for the robot, I showed that a uniform array of visual correlators was sufficient to explain the free-flight velocity regulation behavior of flies, rather than a different model. In addition to illustrating the benefits of concurrent scientific analysis and engineering synthesis, the results give new insight into how to control small biological and man-made flying vehicles using limited, noisy sensors.}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Murray, Richard M.}, } @phdthesis{10.7907/P7PH-5K38, author = {Simon, Jasper Chen}, title = {Behavioral Analysis of Exploration and Dispersal in Drosophila}, school = {California Institute of Technology}, year = {2010}, doi = {10.7907/P7PH-5K38}, url = {https://resolver.caltech.edu/CaltechTHESIS:11122009-111028665}, abstract = {A fundamentally important decision for all animals is whether to utilize a particular resource or to disperse elsewhere in search of potentially superior resources. Within this dissertation, I present results from laboratory experiments carried out using the experimental genetic workhorse, Drosophila melanogaster, to identify and quantify various causal factors contributing to an animal’s decision to disperse from food.
With the set of experiments described within the second chapter, I studied the influence of mating experience on the movement priorities of Drosophila. From these experiments, I suggest that prior mating experience is a significant and likely an important factor modulating the dispersal of Drosophila, and that the change in dispersal results from a change in the fly’s priorities rather than simply a change in the general levels of activity. In chapter three, using methods similar to those used to assess the modulatory effects of mating, I explored how the amount and accessibility of food affects the dispersal of hungry Drosophila. From these experiments, I suggest that the hunger state of flies can override the visual and olfactory cues from food, and I hypothesize that the observed increase in dispersal resulting from hunger is due to a qualitative change in locomotor behavior related to food search.
With a new machine-vision tracking strategy discussed within the fourth chapter, I studied the exploratory behaviors of individual flies within the environmental chambers discussed in Chapters 2 and 3. I introduced single flies that had recently consumed food into chambers and tracked their walking and monitored their flying movements as they became hungry. In collaboration, I have attempted to use learning algorithms based on the statistics of each fly’s behavior during short windows of time to predict the fly’s behavior during the rest of their experimental trial.
I conclude with chapter five by describing a new experimental chamber that I have developed to complement machine-vision methods for tracking individuals within large groups. The motivation behind developing the chamber was to study the changes of social interaction, e.g., courtship and aggressive posturing, of flies near food.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/GN01-P258, author = {Robie, Alice Anne Pennoyer}, title = {Multimodal Sensory Control of Exploration by Walking Drosophila melanogaster}, school = {California Institute of Technology}, year = {2010}, doi = {10.7907/GN01-P258}, url = {https://resolver.caltech.edu/CaltechTHESIS:05242010-123734162}, abstract = {Walking fruit flies, Drosophila melanogaster, use visual information to orient towards salient objects in their environment, presumably as a search strategy for finding food, shelter or other resources. Less is known about the role of vision or other sensory modalities in the evaluation of objects once they have been reached. In order to study these behaviors, I developed a large arena in which I could track individual fruit flies as they walk through either simple or more topologically complex landscapes. Flies use visual cues from the distant background to stabilize their walking trajectories. When exploring an arena containing objects, flies actively orient towards, climb onto, and explore the objects, spending most of their time on the tallest, steepest object. A fly’s behavioral response to an object’s geometry depends upon the intrinsic properties of each object and not an assessment relative to other nearby objects. Further, the preference is due to a change in locomotor behavior once a fly reaches and explores the object’s surface. Specifically, flies are much more likely to stop walking for long periods on tall, steep objects. Both the visual and the antennal mechanosensory systems provide sufficient information about an object’s geometry to elicit the observed change in locomotor behavior. Only when both these sensory systems are impaired do flies not show the behavioral preference for the tall, steep objects. Additionally, I examined the locomotor and social behaviors of large groups of flies. In order to do these studies, I assisted in the development of automated software for tracking and maintaining the individual identity of large groups of flies and for the quantification of individual flies’ locomotor and social behaviors. Behavioral differences between individuals are consistent over the time of the trials and are sufficient to predict a fly’s gender (male vs. female), genotype (wild type vs. fruitless), or sensory environment (with vs. without visual cues). During encounters, males approach other flies more closely than do females and are most often located behind the other fly. The software developed is publicly available and represents a new level of automated quantification in behavioral studies of flies.}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/PR7S-Y618, author = {Card, Gwyneth Megan}, title = {Neural Control and Biomechanics of Flight Initiation in Drosophila melanogaster}, school = {California Institute of Technology}, year = {2009}, doi = {10.7907/PR7S-Y618}, url = {https://resolver.caltech.edu/CaltechETD:etd-05282009-215548}, abstract = {In response to abrupt visual stimulation, the fruit fly, Drosophila melanogaster, quickly initiates flight. This rapid takeoff is believed to be a reflex coordinated by a pair of large descending interneurons (the “giant fibers”). However, it has been difficult to evoke escapes in wild-type flies, and thus flight initiation behavior in the unrestrained wild-type fly is poorly described. I have taken advantage of recent advances in high-speed videography to capture video sequences of Drosophila flight initiation at the temporal resolution of 6,000 frames per second. A three-dimensional kinematic analysis of takeoff sequences indicates that wing use during the jumping phase of flight initiation is essential for stabilizing flight. During voluntary takeoffs, flies raise their wings prior to leaving the ground, resulting in a stable, controlled takeoff. In contrast, during visually-elicited escapes flies pull their wings down close to their body during the takeoff jump, resulting in tumbling flights that are faster but less steady. The takeoff kinematics suggest that the power delivered by the legs is substantially greater during these escapes than during voluntary takeoffs. Thus, I show that the two types of Drosophila flight initiation result in different flight performances once the fly is airborne, and that these performances are distinguished by a trade-off between speed and stability. I also determined that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the simple architecture of the giant fiber pathway thought to mediate escape. I found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the looming stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies’ initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/HEVK-7T03, author = {Bender, John Andrew}, title = {Elements of Feed-Forward and Feedback Control in Drosophila Body Saccades}, school = {California Institute of Technology}, year = {2007}, doi = {10.7907/HEVK-7T03}, url = {https://resolver.caltech.edu/CaltechETD:etd-03042007-163003}, abstract = {I have developed a new experimental preparation of the fruit fly, Drosophila melanogaster. A fly is glued to a steel pin, which is held in the field between two magnets such that the fly is free to rotate about only one axis. Such “magnetically tethered” flies perform rapid yaw turns, similar to the behaviors termed “body saccades” in free flight. Saccades can be evoked by visual stimulation, in a manner suggesting that the underlying neural circuitry may be performing an angular threshold calculation. Once a saccade is initiated, however, visual feedback has very little effect on its dynamics, but rotational feedback from the haltere system plays an important role in structuring the time course of saccades. Vision is important, though, in maintaining a stable orientation in both intact flies and flies with asymmetrical wing alterations. The halteres are known to mediate responses to Coriolis forces correlated with the fly’s rotations in flight, but flies with modified halteres also exhibit distorted saccade dynamics when they are not free to rotate. This suggests that the halteres may be involved in saccade initiation, although the precise mechanisms are not clear. There is preliminary evidence suggesting that the haltere strokes may be actively modulated during flight.}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, } @phdthesis{10.7907/YYSN-7C82, author = {Reiser, Michael Bernard}, title = {Visually Mediated Control of Flight in Drosophila: Not Lost in Translation}, school = {California Institute of Technology}, year = {2007}, doi = {10.7907/YYSN-7C82}, url = {https://resolver.caltech.edu/CaltechETD:etd-01082007-033253}, abstract = {Flying insects exhibit stunning behavioral repertoires that are largely mediated by the visual control of flight. For this reason, presenting a controlled visual environment to tethered insects has been and continues to be a powerful tool for studying the sensory control of complex behaviors. The work presented in this dissertation concerns several robust behavioral responses exhibited by Drosophila that shed light on some of the challenges of visual navigation. To address questions of visual flight control in Drosophila, a modular display system has been designed and has proven to be a robust experimental instrument. The display system has enabled the wide variety of experimental paradigms presented in the thesis.
Much is known about the responses of tethered Drosophila to rotational stimuli. However, the processing of the more complex patterns of motion that occur during translatory flight is largely unknown. Recent experimental results have demonstrated that Drosophila turn away from visual patterns of expansion. However, the avoidance of expansion is so vigorous, that flies robustly orient towards the focus of contraction of a translating flow field. Much of the effort documented in this thesis has sought to explain this paradox.
The paradox has been largely resolved by several significant findings. When undergoing flight directed towards a prominent object, Drosophila will tolerate a level of expansion that would otherwise induce avoidance. The expansion-avoidance behavior is also critically dependent on the speed of image motion; in response to reduced speeds of expansion, Drosophila exhibit a centering response in which they steer towards the focus of expansion by balancing the image motion seen by both eyes. Taken together, these behaviors contribute to a model of Drosophila’s visual flight control as emerging from multiple behavioral modules that operate concurrently.
Simple computational models of Drosophila’s visual system are used to demonstrate that the experimental results arrived at by doing psychophysics on tethered animals actually yield sensible navigation strategies. This final component of the thesis documents an effort to close the feedback loop around the experimenter, by using computational models of Drosophila behavior to constrain the design of future experiments.
}, address = {1200 East California Boulevard, Pasadena, California 91125}, advisor = {Dickinson, Michael H.}, }