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The functional logic of odor information processing in the Drosophila antennal lobe

Recent advances in molecular transduction of odorants in the Olfactory Sensory Neurons (OSNs) of the Drosophila Antenna have shown that the odorant object identity is multiplicatively coupled with the odorant concentration waveform. The resulting combinatorial neural code is a confounding representa...

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Autores principales: Lazar, Aurel A., Liu, Tingkai, Yeh, Chung-Heng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10156017/
https://www.ncbi.nlm.nih.gov/pubmed/37083547
http://dx.doi.org/10.1371/journal.pcbi.1011043
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author Lazar, Aurel A.
Liu, Tingkai
Yeh, Chung-Heng
author_facet Lazar, Aurel A.
Liu, Tingkai
Yeh, Chung-Heng
author_sort Lazar, Aurel A.
collection PubMed
description Recent advances in molecular transduction of odorants in the Olfactory Sensory Neurons (OSNs) of the Drosophila Antenna have shown that the odorant object identity is multiplicatively coupled with the odorant concentration waveform. The resulting combinatorial neural code is a confounding representation of odorant semantic information (identity) and syntactic information (concentration). To distill the functional logic of odor information processing in the Antennal Lobe (AL) a number of challenges need to be addressed including 1) how is the odorant semantic information decoupled from the syntactic information at the level of the AL, 2) how are these two information streams processed by the diverse AL Local Neurons (LNs) and 3) what is the end-to-end functional logic of the AL? By analyzing single-channel physiology recordings at the output of the AL, we found that the Projection Neuron responses can be decomposed into a concentration-invariant component, and two transient components boosting the positive/negative concentration contrast that indicate onset/offset timing information of the odorant object. We hypothesized that the concentration-invariant component, in the multi-channel context, is the recovered odorant identity vector presented between onset/offset timing events. We developed a model of LN pathways in the Antennal Lobe termed the differential Divisive Normalization Processors (DNPs), which robustly extract the semantics (the identity of the odorant object) and the ON/OFF semantic timing events indicating the presence/absence of an odorant object. For real-time processing with spiking PN models, we showed that the phase-space of the biological spike generator of the PN offers an intuit perspective for the representation of recovered odorant semantics and examined the dynamics induced by the odorant semantic timing events. Finally, we provided theoretical and computational evidence for the functional logic of the AL as a robust ON-OFF odorant object identity recovery processor across odorant identities, concentration amplitudes and waveform profiles.
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spelling pubmed-101560172023-05-04 The functional logic of odor information processing in the Drosophila antennal lobe Lazar, Aurel A. Liu, Tingkai Yeh, Chung-Heng PLoS Comput Biol Research Article Recent advances in molecular transduction of odorants in the Olfactory Sensory Neurons (OSNs) of the Drosophila Antenna have shown that the odorant object identity is multiplicatively coupled with the odorant concentration waveform. The resulting combinatorial neural code is a confounding representation of odorant semantic information (identity) and syntactic information (concentration). To distill the functional logic of odor information processing in the Antennal Lobe (AL) a number of challenges need to be addressed including 1) how is the odorant semantic information decoupled from the syntactic information at the level of the AL, 2) how are these two information streams processed by the diverse AL Local Neurons (LNs) and 3) what is the end-to-end functional logic of the AL? By analyzing single-channel physiology recordings at the output of the AL, we found that the Projection Neuron responses can be decomposed into a concentration-invariant component, and two transient components boosting the positive/negative concentration contrast that indicate onset/offset timing information of the odorant object. We hypothesized that the concentration-invariant component, in the multi-channel context, is the recovered odorant identity vector presented between onset/offset timing events. We developed a model of LN pathways in the Antennal Lobe termed the differential Divisive Normalization Processors (DNPs), which robustly extract the semantics (the identity of the odorant object) and the ON/OFF semantic timing events indicating the presence/absence of an odorant object. For real-time processing with spiking PN models, we showed that the phase-space of the biological spike generator of the PN offers an intuit perspective for the representation of recovered odorant semantics and examined the dynamics induced by the odorant semantic timing events. Finally, we provided theoretical and computational evidence for the functional logic of the AL as a robust ON-OFF odorant object identity recovery processor across odorant identities, concentration amplitudes and waveform profiles. Public Library of Science 2023-04-21 /pmc/articles/PMC10156017/ /pubmed/37083547 http://dx.doi.org/10.1371/journal.pcbi.1011043 Text en © 2023 Lazar et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Lazar, Aurel A.
Liu, Tingkai
Yeh, Chung-Heng
The functional logic of odor information processing in the Drosophila antennal lobe
title The functional logic of odor information processing in the Drosophila antennal lobe
title_full The functional logic of odor information processing in the Drosophila antennal lobe
title_fullStr The functional logic of odor information processing in the Drosophila antennal lobe
title_full_unstemmed The functional logic of odor information processing in the Drosophila antennal lobe
title_short The functional logic of odor information processing in the Drosophila antennal lobe
title_sort functional logic of odor information processing in the drosophila antennal lobe
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10156017/
https://www.ncbi.nlm.nih.gov/pubmed/37083547
http://dx.doi.org/10.1371/journal.pcbi.1011043
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