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Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb

Respiration plays an essential role in odor processing. Even in the absence of odors, oscillating excitatory and inhibitory activity in the olfactory bulb synchronizes with respiration, commonly resulting in a burst of action potentials in mammalian mitral/tufted cells (MTCs) during the transition f...

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Autores principales: Short, Shaina M., Morse, Thomas M., McTavish, Thomas S., Shepherd, Gordon M., Verhagen, Justus V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5179112/
https://www.ncbi.nlm.nih.gov/pubmed/28005923
http://dx.doi.org/10.1371/journal.pone.0168356
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author Short, Shaina M.
Morse, Thomas M.
McTavish, Thomas S.
Shepherd, Gordon M.
Verhagen, Justus V.
author_facet Short, Shaina M.
Morse, Thomas M.
McTavish, Thomas S.
Shepherd, Gordon M.
Verhagen, Justus V.
author_sort Short, Shaina M.
collection PubMed
description Respiration plays an essential role in odor processing. Even in the absence of odors, oscillating excitatory and inhibitory activity in the olfactory bulb synchronizes with respiration, commonly resulting in a burst of action potentials in mammalian mitral/tufted cells (MTCs) during the transition from inhalation to exhalation. This excitation is followed by inhibition that quiets MTC activity in both the glomerular and granule cell layers. Odor processing is hypothesized to be modulated by and may even rely on respiration-mediated activity, yet exactly how respiration influences sensory processing by MTCs is still not well understood. By using optogenetics to stimulate discrete sensory inputs in vivo, it was possible to temporally vary the stimulus to occur at unique phases of each respiration. Single unit recordings obtained from the mitral cell layer were used to map spatiotemporal patterns of glomerular evoked responses that were unique to stimulations occurring during periods of inhalation or exhalation. Sensory evoked activity in MTCs was gated to periods outside phasic respiratory mediated firing, causing net shifts in MTC activity across the cycle. In contrast, odor evoked inhibitory responses appear to be permitted throughout the respiratory cycle. Computational models were used to further explore mechanisms of inhibition that can be activated by respiratory activity and influence MTC responses. In silico results indicate that both periglomerular and granule cell inhibition can be activated by respiration to internally gate sensory responses in the olfactory bulb. Both the respiration rate and strength of lateral connectivity influenced inhibitory mechanisms that gate sensory evoked responses.
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spelling pubmed-51791122017-01-04 Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb Short, Shaina M. Morse, Thomas M. McTavish, Thomas S. Shepherd, Gordon M. Verhagen, Justus V. PLoS One Research Article Respiration plays an essential role in odor processing. Even in the absence of odors, oscillating excitatory and inhibitory activity in the olfactory bulb synchronizes with respiration, commonly resulting in a burst of action potentials in mammalian mitral/tufted cells (MTCs) during the transition from inhalation to exhalation. This excitation is followed by inhibition that quiets MTC activity in both the glomerular and granule cell layers. Odor processing is hypothesized to be modulated by and may even rely on respiration-mediated activity, yet exactly how respiration influences sensory processing by MTCs is still not well understood. By using optogenetics to stimulate discrete sensory inputs in vivo, it was possible to temporally vary the stimulus to occur at unique phases of each respiration. Single unit recordings obtained from the mitral cell layer were used to map spatiotemporal patterns of glomerular evoked responses that were unique to stimulations occurring during periods of inhalation or exhalation. Sensory evoked activity in MTCs was gated to periods outside phasic respiratory mediated firing, causing net shifts in MTC activity across the cycle. In contrast, odor evoked inhibitory responses appear to be permitted throughout the respiratory cycle. Computational models were used to further explore mechanisms of inhibition that can be activated by respiratory activity and influence MTC responses. In silico results indicate that both periglomerular and granule cell inhibition can be activated by respiration to internally gate sensory responses in the olfactory bulb. Both the respiration rate and strength of lateral connectivity influenced inhibitory mechanisms that gate sensory evoked responses. Public Library of Science 2016-12-22 /pmc/articles/PMC5179112/ /pubmed/28005923 http://dx.doi.org/10.1371/journal.pone.0168356 Text en © 2016 Short et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://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
Short, Shaina M.
Morse, Thomas M.
McTavish, Thomas S.
Shepherd, Gordon M.
Verhagen, Justus V.
Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title_full Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title_fullStr Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title_full_unstemmed Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title_short Respiration Gates Sensory Input Responses in the Mitral Cell Layer of the Olfactory Bulb
title_sort respiration gates sensory input responses in the mitral cell layer of the olfactory bulb
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5179112/
https://www.ncbi.nlm.nih.gov/pubmed/28005923
http://dx.doi.org/10.1371/journal.pone.0168356
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