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Processing at Primary Chemosensory Neurons

Citation

Zocchi, Dhruv Sergio (2020) Processing at Primary Chemosensory Neurons. Dissertation (Ph.D.), California Institute of Technology. doi:10.7907/yshd-3195. https://resolver.caltech.edu/CaltechTHESIS:05032020-101047008

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 CO₂ sensing by the Drosophila olfactory system.

In 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.

In chapter 2, I talk about CO₂ 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 CO₂, 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 CO₂, 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.

Item Type:Thesis (Dissertation (Ph.D.))
Subject Keywords:Neurobiology, sensory neurobiology
Degree Grantor:California Institute of Technology
Division:Biology and Biological Engineering
Major Option:Neurobiology
Thesis Availability:Public (worldwide access)
Research Advisor(s):
  • Hong, Elizabeth J. (advisor)
  • Oka, Yuki (advisor)
Thesis Committee:
  • Meister, Markus (chair)
  • Sternberg, Paul W. (co-chair)
  • Dickinson, Michael H.
  • Hong, Elizabeth J.
  • Oka, Yuki
Defense Date:28 January 2020
Non-Caltech Author Email:dhruvzocchi (AT) gmail.com
Record Number:CaltechTHESIS:05032020-101047008
Persistent URL:https://resolver.caltech.edu/CaltechTHESIS:05032020-101047008
DOI:10.7907/yshd-3195
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/nn.4575DOIArticle adapted for Chapter 1.
Default Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:13695
Collection:CaltechTHESIS
Deposited By: Dhruv Zocchi
Deposited On:06 May 2020 22:30
Last Modified:04 Nov 2021 21:28

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