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Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb

Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result...

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Autores principales: Zavatone-Veth, Jacob A., Masset, Paul, Tong, William L., Zak, Joseph D., Murthy, Venkatesh N., Pehlevan, Cengiz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634677/
https://www.ncbi.nlm.nih.gov/pubmed/37961548
http://dx.doi.org/10.1101/2023.06.21.545947
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author Zavatone-Veth, Jacob A.
Masset, Paul
Tong, William L.
Zak, Joseph D.
Murthy, Venkatesh N.
Pehlevan, Cengiz
author_facet Zavatone-Veth, Jacob A.
Masset, Paul
Tong, William L.
Zak, Joseph D.
Murthy, Venkatesh N.
Pehlevan, Cengiz
author_sort Zavatone-Veth, Jacob A.
collection PubMed
description Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result, the olfactory system must solve a compressed sensing problem, relying on the fact that only a handful of the millions of possible odorants are present in a given scene. Inspired by this principle, past works have proposed normative compressed sensing models for olfactory decoding. However, these models have not captured the unique anatomy and physiology of the olfactory bulb, nor have they shown that sensing can be achieved within the 100-millisecond timescale of a single sniff. Here, we propose a rate-based Poisson compressed sensing circuit model for the olfactory bulb. This model maps onto the neuron classes of the olfactory bulb, and recapitulates salient features of their connectivity and physiology. For circuit sizes comparable to the human olfactory bulb, we show that this model can accurately detect tens of odors within the timescale of a single sniff. We also show that this model can perform Bayesian posterior sampling for accurate uncertainty estimation. Fast inference is possible only if the geometry of the neural code is chosen to match receptor properties, yielding a distributed neural code that is not axis-aligned to individual odor identities. Our results illustrate how normative modeling can help us map function onto specific neural circuits to generate new hypotheses.
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spelling pubmed-106346772023-11-13 Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb Zavatone-Veth, Jacob A. Masset, Paul Tong, William L. Zak, Joseph D. Murthy, Venkatesh N. Pehlevan, Cengiz bioRxiv Article Within a single sniff, the mammalian olfactory system can decode the identity and concentration of odorants wafted on turbulent plumes of air. Yet, it must do so given access only to the noisy, dimensionally-reduced representation of the odor world provided by olfactory receptor neurons. As a result, the olfactory system must solve a compressed sensing problem, relying on the fact that only a handful of the millions of possible odorants are present in a given scene. Inspired by this principle, past works have proposed normative compressed sensing models for olfactory decoding. However, these models have not captured the unique anatomy and physiology of the olfactory bulb, nor have they shown that sensing can be achieved within the 100-millisecond timescale of a single sniff. Here, we propose a rate-based Poisson compressed sensing circuit model for the olfactory bulb. This model maps onto the neuron classes of the olfactory bulb, and recapitulates salient features of their connectivity and physiology. For circuit sizes comparable to the human olfactory bulb, we show that this model can accurately detect tens of odors within the timescale of a single sniff. We also show that this model can perform Bayesian posterior sampling for accurate uncertainty estimation. Fast inference is possible only if the geometry of the neural code is chosen to match receptor properties, yielding a distributed neural code that is not axis-aligned to individual odor identities. Our results illustrate how normative modeling can help us map function onto specific neural circuits to generate new hypotheses. Cold Spring Harbor Laboratory 2023-10-28 /pmc/articles/PMC10634677/ /pubmed/37961548 http://dx.doi.org/10.1101/2023.06.21.545947 Text en https://creativecommons.org/licenses/by-nc/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/) , which allows reusers to distribute, remix, adapt, and build upon the material in any medium or format for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Zavatone-Veth, Jacob A.
Masset, Paul
Tong, William L.
Zak, Joseph D.
Murthy, Venkatesh N.
Pehlevan, Cengiz
Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title_full Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title_fullStr Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title_full_unstemmed Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title_short Neural Circuits for Fast Poisson Compressed Sensing in the Olfactory Bulb
title_sort neural circuits for fast poisson compressed sensing in the olfactory bulb
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634677/
https://www.ncbi.nlm.nih.gov/pubmed/37961548
http://dx.doi.org/10.1101/2023.06.21.545947
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