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Parallel encoding of CO₂ in attractive and aversive glomeruli by selective lateral signaling between olfactory afferents

Zocchi, Dhruv and Ye, Emily S. and Hauser, Virginie and O’Connell, Thomas F. and Hong, Elizabeth J. (2022) Parallel encoding of CO₂ in attractive and aversive glomeruli by selective lateral signaling between olfactory afferents. Current Biology, 32 (19). 4225-4239.e7. ISSN 0960-9822. PMCID PMC9561050. doi:10.1016/j.cub.2022.08.025.

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We describe a novel form of selective crosstalk between specific classes of primary olfactory receptor neurons (ORNs) in the Drosophila antennal lobe. Neurotransmitter release from ORNs is driven by two distinct sources of excitation: direct activity derived from the odorant receptor and stimulus-selective lateral signals originating from stereotypic subsets of other ORNs. Consequently, the level of presynaptic neurotransmitter release from an ORN can be significantly dissociated from its firing rate. Stimulus-selective lateral signaling results in the distributed representation of CO₂—a behaviorally important environmental cue that directly excites a single ORN class—in multiple olfactory glomeruli, each with distinct response dynamics. CO₂-sensitive glomeruli coupled to behavioral attraction respond preferentially to fast changes in CO₂ concentration, whereas those coupled to behavioral aversion more closely follow absolute levels of CO₂. Behavioral responses to CO₂ also depend on the temporal structure of the stimulus: flies walk upwind to fluctuating, but not sustained, pulses of CO₂. Stimulus-selective lateral signaling generalizes to additional odors and glomeruli, revealing a subnetwork of lateral interactions between ORNs that reshapes the spatial and temporal structure of odor representations in a stimulus-specific manner.

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URLURL TypeDescription InCaltech News
Hauser, Virginie0000-0003-3888-5230
Hong, Elizabeth J.0000-0003-3866-418X
Additional Information:We are grateful to B.D. Pfeiffer and D.J. Anderson for gifts of unpublished fly stocks. We thank T. Lee and R.J. Wyman for sharing fly stocks, and we thank G. Rubin and L.M. Stevens for sharing plasmids. We thank A. Dea for the generation of the LexAop-DTI flies and M. Lobb-Rabe for the generation of Or42a-LexA flies. We thank A. Matheson and K. Nagel for design files and advice on establishing the miniature wind tunnel walking assay. We thank F. van Breugel for help with implementing the Multi tracker package for tracking flies. We thank M. Meister, P.W. Sternberg, members of the Hong lab, and anonymous reviewers for their careful readings of the manuscript and their many insightful comments that improved this study. We especially acknowledge F. van Breugel and M.H. Dickinson for stimulating conversations and for sharing unpublished results that partially motivated this study. This work was funded by grants to E.J.H. from the NSF/CIHR/DFG/FRQ/UKRI-MRC Next Generation Networks for Neuroscience Program (NeuroNex Award #2014217), the National Institutes of Health (1U01MH109147), and the Shurl and Kay Curci Foundation. E.J.H. is a Chen Scholar of the Tianqiao and Chrissy Chen Institute for Neuroscience and a Clare Boothe Luce Professor of the Henry Luce Foundation. Author contributions. Conceptualization, D.Z. and E.J.H.; methodology, D.Z., T.F.O., and E.J.H.; validation, D.Z., E.S.Y., and V.H.; formal analysis, D.Z., E.S.Y., and E.J.H.; investigation, D.Z., E.S.Y., and V.H.; writing – original draft, D.Z. and E.J.H.; writing – review & editing, D.Z. and E.J.H.; visualization, D.Z. and E.J.H.; supervision, E.J.H.; funding acquisition, E.J.H. The authors declare no competing interests.
Group:Tianqiao and Chrissy Chen Institute for Neuroscience
Funding AgencyGrant Number
Shurl and Kay Curci FoundationUNSPECIFIED
Tianqiao and Chrissy Chen Institute for NeuroscienceUNSPECIFIED
Henry Luce FoundationUNSPECIFIED
Issue or Number:19
PubMed Central ID:PMC9561050
Record Number:CaltechAUTHORS:20220909-225792000
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:116792
Deposited By: Olivia Warschaw
Deposited On:15 Nov 2022 23:12
Last Modified:28 Feb 2023 22:47

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