Plasticity is widely studied across different sensory systems and behavioral paradigms, but the underlying mechanisms are varied and incompletely understood. Previous work in the fruit fly Drosophila melanogaster reported changes in odor preference and walking behavior after chronic odor exposure during early adulthood. Here, we investigated the hypothesis that changes in behavior reflect changes in how odors are encoded in the first two layers of the fly olfactory circuit. We chronically exposed flies to naturalistic odor stimuli that selectively and robustly activate a single olfactory receptor neuron (ORN) class. We then performed targeted intracellular recordings from genetically identified second-order olfactory projection neurons (PNs) that either receive direct input from the activated ORN class, or receive indirect activity (via local lateral circuitry), during chronic odor exposure. In addition, we used existing reagents to create a novel optical method to characterize ORN-PN synaptic strength. We find that the fly antennal lobe is resistant to plasticity, with a few exceptions. Of the odors we tested, we find that rearing in trans-2-hexenal, a leaf aldehyde that selectively activates ab4a ORNs, weakly enhanced odor responses in some PNs. The effects of rearing on PNs were not explained by ORN odor responses or changes in ORN-PN synaptic strength. We find evidence that lateral excitation may increase across glomeruli following rearing, suggesting that some odors may alter PN responses globally. We discuss possible reasons for differences between our observations and prior work on olfactory plasticity in this circuit, which has been conducted primarily in the context of exposures to much higher, non-naturalistic concentrations of odor. Our results point to the stability of insect sensory circuits in the face of large perturbations in the sensory environment.
\r\n\r\n\u2028\u2028During our optical stimulation experiments, we find that driving Chrimson expression may abolish odor responses in some ORNs. We include sample data highlighting this observation in a population of pb1a olfactory neurons. Lastly, we include antennal local field potential recordings in response to a variety of odor concentrations to help guide future experiments seeking isointense odor panels.
", "doi": "10.7907/e39b-w024", "publication_date": "2020", "thesis_type": "phd", "thesis_year": "2020" }, { "id": "thesis:13695", "collection": "thesis", "collection_id": "13695", "cite_using_url": "https://resolver.caltech.edu/CaltechTHESIS:05032020-101047008", "primary_object_url": { "basename": "Processing at Primary Chemosensory Neurons.pdf", "content": "final", "filesize": 3226385, "license": "other", "mime_type": "application/pdf", "url": "/13695/1/Processing at Primary Chemosensory Neurons.pdf", "version": "v4.0.0" }, "type": "thesis", "title": "Processing at Primary Chemosensory Neurons", "author": [ { "family_name": "Zocchi", "given_name": "Dhruv Sergio", "clpid": "Zocchi-Dhruv-Sergio" } ], "thesis_advisor": [ { "family_name": "Hong", "given_name": "Elizabeth J.", "clpid": "Hong-Elizabeth-J" }, { "family_name": "Oka", "given_name": "Yuki", "orcid": "0000-0003-2686-0677", "clpid": "Oka-Yuki" } ], "thesis_committee": [ { "family_name": "Meister", "given_name": "Markus", "orcid": "0000-0003-2136-6506", "clpid": "Meister-M" }, { "family_name": "Sternberg", "given_name": "Paul W.", "orcid": "0000-0002-7699-0173", "clpid": "Sternberg-P-W" }, { "family_name": "Dickinson", "given_name": "Michael H.", "orcid": "0000-0002-8587-9936", "clpid": "Dickinson-M-H" }, { "family_name": "Hong", "given_name": "Elizabeth J.", "clpid": "Hong-Elizabeth-J" }, { "family_name": "Oka", "given_name": "Yuki", "orcid": "0000-0003-2686-0677", "clpid": "Oka-Yuki" } ], "local_group": [ { "literal": "div_bbe" } ], "abstract": "Chemosensory perception involves the detection of chemical compounds. In animals, there are 2 chemical senses: taste, and olfaction. The two are related in that they utilize ligand-gated receptors, expressed in primary sensory neurons, to detect chemical stimuli from the surrounding environment. However, the processing of these inputs is quite different in the two systems, leading to divergent roles for olfaction and taste in sensory perception. This dissertation highlights some of these differences, by looking at processing of ethologically relevant stimuli at the very peripheral receptor neurons. The work is divided into 2 parts: water sensing by the mammalian taste system, and CO\u2082 sensing by the Drosophila olfactory system.
\r\n\r\nIn Chapter 1, I talk about water sensing in the mammalian taste system. Initiation of drinking behavior relies on peripheral water detection. It is likely that this detection is mediated, at least in part, by the taste system. Here, I have shown that acid-sensing taste receptor cells (TRCs) that were previously suggested as the sensors for sour taste, also respond to water. This response is mediated by a bicarbonate-dependent molecular mechanism, likely involving the Carbonic Anhydrase enzyme family. Furthermore, optogenetic stimulation of the acid-sensing TRCs in thirsty animals induces robust licking responses towards the light source, even in the absence of water. Conversely, thirsty animals lacking functional acid-sensing TRCs show compromised discrimination between water and non-aqueous fluids. Taken together, this work reveals the cellular mechanism of water detection by the mammalian taste system.
\r\n\r\nIn chapter 2, I talk about CO\u2082 sensing in the fruit fly. The Drosophila olfactory system responds to most odors with the activation of a large subset of its olfactory receptors (ORs). This broad activation is a consequence of the ORs having affinity to multiple chemical compounds. In contrast, a small number of odors, like CO\u2082, elicit responses in only single ORs. These ORs are, in contrast to most ORs, very narrowly tuned, generally responding only to that one odor. It has been assumed up until now that the specificity of these unique ORs is inherited by the olfactory receptor neurons (ORNs) they are expressed in, and even in the projection neurons (PNs), that the ORNs synapse onto. I show here that CO\u2082, though it activates only a single OR, the GR63a/GR21a hetero-dimer complex, actually activates multiple ORN axon terminals. This activation is due to lateral excitatory connections between axon terminals of the GR63a/GR21a expressing ORNs, and at least 4 other ORN types. Focusing on one of these ORNs, Ab1B, I show the lateral connections bypass the ORN cell bodies, only driving responses at the axon terminals. Consequently, Ab1B ORN axon terminals receive 2 sources of excitatory input, a feed-forward excitation from its endogenous OR, and a lateral excitation from GR63a/GR21a. This effectively divides the ORN into 2 compartments, distinct in their odor tuning. Finally, I show that lateral excitation is a general feature of the ORN circuit by silencing the feed-forward input of another ORN class, Ab1A. The Ab1A cell body is completely silent, but the axon terminals retain odor responses from lateral excitatory inputs. Thus, there is a lateral flow of odor information between multiple ORNs of the Drosophila olfactory system.
", "doi": "10.7907/yshd-3195", "publication_date": "2020", "thesis_type": "phd", "thesis_year": "2020" } ]