Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.

Neocortical neurons can increasingly be divided into well-defined classes, but their activity patterns during quantified behavior remain to be fully determined. Here, we obtained membrane potential recordings from various classes of excitatory and inhibitory neurons located across different cortical...

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Main Authors: Taro Kiritani, Aurélie Pala, Célia Gasselin, Sylvain Crochet, Carl C H Petersen
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0287174
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author Taro Kiritani
Aurélie Pala
Célia Gasselin
Sylvain Crochet
Carl C H Petersen
author_facet Taro Kiritani
Aurélie Pala
Célia Gasselin
Sylvain Crochet
Carl C H Petersen
author_sort Taro Kiritani
collection DOAJ
description Neocortical neurons can increasingly be divided into well-defined classes, but their activity patterns during quantified behavior remain to be fully determined. Here, we obtained membrane potential recordings from various classes of excitatory and inhibitory neurons located across different cortical depths in the primary whisker somatosensory barrel cortex of awake head-restrained mice during quiet wakefulness, free whisking and active touch. Excitatory neurons, especially those located superficially, were hyperpolarized with low action potential firing rates relative to inhibitory neurons. Parvalbumin-expressing inhibitory neurons on average fired at the highest rates, responding strongly and rapidly to whisker touch. Vasoactive intestinal peptide-expressing inhibitory neurons were excited during whisking, but responded to active touch only after a delay. Somatostatin-expressing inhibitory neurons had the smallest membrane potential fluctuations and exhibited hyperpolarising responses at whisking onset for superficial, but not deep, neurons. Interestingly, rapid repetitive whisker touch evoked excitatory responses in somatostatin-expressing inhibitory neurons, but not when the intercontact interval was long. Our analyses suggest that distinct genetically-defined classes of neurons at different subpial depths have differential activity patterns depending upon behavioral state providing a basis for constraining future computational models of neocortical function.
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spelling doaj.art-19dc5fbbe9064b41ba3f6187c5b8a1db2023-06-23T05:31:24ZengPublic Library of Science (PLoS)PLoS ONE1932-62032023-01-01186e028717410.1371/journal.pone.0287174Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.Taro KiritaniAurélie PalaCélia GasselinSylvain CrochetCarl C H PetersenNeocortical neurons can increasingly be divided into well-defined classes, but their activity patterns during quantified behavior remain to be fully determined. Here, we obtained membrane potential recordings from various classes of excitatory and inhibitory neurons located across different cortical depths in the primary whisker somatosensory barrel cortex of awake head-restrained mice during quiet wakefulness, free whisking and active touch. Excitatory neurons, especially those located superficially, were hyperpolarized with low action potential firing rates relative to inhibitory neurons. Parvalbumin-expressing inhibitory neurons on average fired at the highest rates, responding strongly and rapidly to whisker touch. Vasoactive intestinal peptide-expressing inhibitory neurons were excited during whisking, but responded to active touch only after a delay. Somatostatin-expressing inhibitory neurons had the smallest membrane potential fluctuations and exhibited hyperpolarising responses at whisking onset for superficial, but not deep, neurons. Interestingly, rapid repetitive whisker touch evoked excitatory responses in somatostatin-expressing inhibitory neurons, but not when the intercontact interval was long. Our analyses suggest that distinct genetically-defined classes of neurons at different subpial depths have differential activity patterns depending upon behavioral state providing a basis for constraining future computational models of neocortical function.https://doi.org/10.1371/journal.pone.0287174
spellingShingle Taro Kiritani
Aurélie Pala
Célia Gasselin
Sylvain Crochet
Carl C H Petersen
Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
PLoS ONE
title Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
title_full Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
title_fullStr Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
title_full_unstemmed Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
title_short Membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing.
title_sort membrane potential dynamics of excitatory and inhibitory neurons in mouse barrel cortex during active whisker sensing
url https://doi.org/10.1371/journal.pone.0287174
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