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...
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Public Library of Science (PLoS)
2021-05-01
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| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001235&type=printable |
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| author | Nicholas A Frost Anna Haggart Vikaas S Sohal |
| author_facet | Nicholas A Frost Anna Haggart Vikaas S Sohal |
| author_sort | Nicholas A Frost |
| collection | DOAJ |
| 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. |
| format | Article |
| id | doaj-art-25e253f7cb8a4faaa660564988debe5c |
| institution | DOAJ |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2021-05-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-25e253f7cb8a4faaa660564988debe5c2025-08-20T02:55:20ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852021-05-01195e300123510.1371/journal.pbio.3001235Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior.Nicholas A FrostAnna HaggartVikaas S SohalNew 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.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001235&type=printable |
| spellingShingle | Nicholas A Frost Anna Haggart Vikaas S Sohal Dynamic patterns of correlated activity in the prefrontal cortex encode information about social behavior. PLoS Biology |
| 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 |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001235&type=printable |
| work_keys_str_mv | AT nicholasafrost dynamicpatternsofcorrelatedactivityintheprefrontalcortexencodeinformationaboutsocialbehavior AT annahaggart dynamicpatternsofcorrelatedactivityintheprefrontalcortexencodeinformationaboutsocialbehavior AT vikaasssohal dynamicpatternsofcorrelatedactivityintheprefrontalcortexencodeinformationaboutsocialbehavior |