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Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior

New technologies make it possible to measure activity from many neurons simultaneously. One approach is to analyze simultaneously recorded neurons individually, then group together neurons which increase their activity during similar behaviors into an “ensemble.” However, this notion of an ensemble...

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Detalles Bibliográficos
Autores principales: Frost, Nicholas A., Haggart, Anna, Sohal, Vikaas S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8118626/
https://www.ncbi.nlm.nih.gov/pubmed/33939689
http://dx.doi.org/10.1371/journal.pbio.3001235
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author Frost, Nicholas A.
Haggart, Anna
Sohal, Vikaas S.
author_facet Frost, Nicholas A.
Haggart, Anna
Sohal, Vikaas S.
author_sort Frost, Nicholas A.
collection PubMed
description New technologies make it possible to measure activity from many neurons simultaneously. One approach is to analyze simultaneously recorded neurons individually, then group together neurons which increase their activity during similar behaviors into an “ensemble.” However, this notion of an ensemble ignores the ability of neurons to act collectively and encode and transmit information in ways that are not reflected by their individual activity levels. We used microendoscopic GCaMP imaging to measure prefrontal activity while mice were either alone or engaged in social interaction. We developed an approach that combines a neural network classifier and surrogate (shuffled) datasets to characterize how neurons synergistically transmit information about social behavior. Notably, unlike optimal linear classifiers, a neural network classifier with a single linear hidden layer can discriminate network states which differ solely in patterns of coactivity, and not in the activity levels of individual neurons. Using this approach, we found that surrogate datasets which preserve behaviorally specific patterns of coactivity (correlations) outperform those which preserve behaviorally driven changes in activity levels but not correlated activity. Thus, social behavior elicits increases in correlated activity that are not explained simply by the activity levels of the underlying neurons, and prefrontal neurons act collectively to transmit information about socialization via these correlations. Notably, this ability of correlated activity to enhance the information transmitted by neuronal ensembles is diminished in mice lacking the autism-associated gene Shank3. These results show that synergy is an important concept for the coding of social behavior which can be disrupted in disease states, reveal a specific mechanism underlying this synergy (social behavior increases correlated activity within specific ensembles), and outline methods for studying how neurons within an ensemble can work together to encode information.
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spelling pubmed-81186262021-05-24 Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior Frost, Nicholas A. Haggart, Anna Sohal, Vikaas S. PLoS Biol Research Article New technologies make it possible to measure activity from many neurons simultaneously. One approach is to analyze simultaneously recorded neurons individually, then group together neurons which increase their activity during similar behaviors into an “ensemble.” However, this notion of an ensemble ignores the ability of neurons to act collectively and encode and transmit information in ways that are not reflected by their individual activity levels. We used microendoscopic GCaMP imaging to measure prefrontal activity while mice were either alone or engaged in social interaction. We developed an approach that combines a neural network classifier and surrogate (shuffled) datasets to characterize how neurons synergistically transmit information about social behavior. Notably, unlike optimal linear classifiers, a neural network classifier with a single linear hidden layer can discriminate network states which differ solely in patterns of coactivity, and not in the activity levels of individual neurons. Using this approach, we found that surrogate datasets which preserve behaviorally specific patterns of coactivity (correlations) outperform those which preserve behaviorally driven changes in activity levels but not correlated activity. Thus, social behavior elicits increases in correlated activity that are not explained simply by the activity levels of the underlying neurons, and prefrontal neurons act collectively to transmit information about socialization via these correlations. Notably, this ability of correlated activity to enhance the information transmitted by neuronal ensembles is diminished in mice lacking the autism-associated gene Shank3. These results show that synergy is an important concept for the coding of social behavior which can be disrupted in disease states, reveal a specific mechanism underlying this synergy (social behavior increases correlated activity within specific ensembles), and outline methods for studying how neurons within an ensemble can work together to encode information. Public Library of Science 2021-05-03 /pmc/articles/PMC8118626/ /pubmed/33939689 http://dx.doi.org/10.1371/journal.pbio.3001235 Text en © 2021 Frost 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
Frost, Nicholas A.
Haggart, Anna
Sohal, Vikaas S.
Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title_full Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title_fullStr Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title_full_unstemmed Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title_short Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
title_sort dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8118626/
https://www.ncbi.nlm.nih.gov/pubmed/33939689
http://dx.doi.org/10.1371/journal.pbio.3001235
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