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Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models

The majority of olfaction studies focus on orthonasal stimulation where odors enter via the front nasal cavity, while retronasal olfaction, where odors enter the rear of the nasal cavity during feeding, is understudied. The coding of retronasal odors via coordinated spiking of neurons in the olfacto...

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Autores principales: Craft, Michelle F., Barreiro, Andrea K., Gautam, Shree Hari, Shew, Woodrow L., Ly, Cheng
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8483419/
https://www.ncbi.nlm.nih.gov/pubmed/34543261
http://dx.doi.org/10.1371/journal.pcbi.1009169
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author Craft, Michelle F.
Barreiro, Andrea K.
Gautam, Shree Hari
Shew, Woodrow L.
Ly, Cheng
author_facet Craft, Michelle F.
Barreiro, Andrea K.
Gautam, Shree Hari
Shew, Woodrow L.
Ly, Cheng
author_sort Craft, Michelle F.
collection PubMed
description The majority of olfaction studies focus on orthonasal stimulation where odors enter via the front nasal cavity, while retronasal olfaction, where odors enter the rear of the nasal cavity during feeding, is understudied. The coding of retronasal odors via coordinated spiking of neurons in the olfactory bulb (OB) is largely unknown despite evidence that higher level processing is different than orthonasal. To this end, we use multi-electrode array in vivo recordings of rat OB mitral cells (MC) in response to a food odor with both modes of stimulation, and find significant differences in evoked firing rates and spike count covariances (i.e., noise correlations). Differences in spiking activity often have implications for sensory coding, thus we develop a single-compartment biophysical OB model that is able to reproduce key properties of important OB cell types. Prior experiments in olfactory receptor neurons (ORN) showed retro stimulation yields slower and spatially smaller ORN inputs than with ortho, yet whether this is consequential for OB activity remains unknown. Indeed with these specifications for ORN inputs, our OB model captures the salient trends in our OB data. We also analyze how first and second order ORN input statistics dynamically transfer to MC spiking statistics with a phenomenological linear-nonlinear filter model, and find that retro inputs result in larger linear filters than ortho inputs. Finally, our models show that the temporal profile of ORN is crucial for capturing our data and is thus a distinguishing feature between ortho and retro stimulation, even at the OB. Using data-driven modeling, we detail how ORN inputs result in differences in OB dynamics and MC spiking statistics. These differences may ultimately shape how ortho and retro odors are coded.
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spelling pubmed-84834192021-10-01 Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models Craft, Michelle F. Barreiro, Andrea K. Gautam, Shree Hari Shew, Woodrow L. Ly, Cheng PLoS Comput Biol Research Article The majority of olfaction studies focus on orthonasal stimulation where odors enter via the front nasal cavity, while retronasal olfaction, where odors enter the rear of the nasal cavity during feeding, is understudied. The coding of retronasal odors via coordinated spiking of neurons in the olfactory bulb (OB) is largely unknown despite evidence that higher level processing is different than orthonasal. To this end, we use multi-electrode array in vivo recordings of rat OB mitral cells (MC) in response to a food odor with both modes of stimulation, and find significant differences in evoked firing rates and spike count covariances (i.e., noise correlations). Differences in spiking activity often have implications for sensory coding, thus we develop a single-compartment biophysical OB model that is able to reproduce key properties of important OB cell types. Prior experiments in olfactory receptor neurons (ORN) showed retro stimulation yields slower and spatially smaller ORN inputs than with ortho, yet whether this is consequential for OB activity remains unknown. Indeed with these specifications for ORN inputs, our OB model captures the salient trends in our OB data. We also analyze how first and second order ORN input statistics dynamically transfer to MC spiking statistics with a phenomenological linear-nonlinear filter model, and find that retro inputs result in larger linear filters than ortho inputs. Finally, our models show that the temporal profile of ORN is crucial for capturing our data and is thus a distinguishing feature between ortho and retro stimulation, even at the OB. Using data-driven modeling, we detail how ORN inputs result in differences in OB dynamics and MC spiking statistics. These differences may ultimately shape how ortho and retro odors are coded. Public Library of Science 2021-09-20 /pmc/articles/PMC8483419/ /pubmed/34543261 http://dx.doi.org/10.1371/journal.pcbi.1009169 Text en © 2021 Craft 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
Craft, Michelle F.
Barreiro, Andrea K.
Gautam, Shree Hari
Shew, Woodrow L.
Ly, Cheng
Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title_full Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title_fullStr Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title_full_unstemmed Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title_short Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
title_sort differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8483419/
https://www.ncbi.nlm.nih.gov/pubmed/34543261
http://dx.doi.org/10.1371/journal.pcbi.1009169
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