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Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality
Modulation of interactions among neurons can manifest as dramatic changes in the state of population dynamics in cerebral cortex. How such transitions in cortical state impact the information processing performed by cortical circuits is not clear. Here we performed experiments and computational mode...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4666488/ https://www.ncbi.nlm.nih.gov/pubmed/26623645 http://dx.doi.org/10.1371/journal.pcbi.1004576 |
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author | Gautam, Shree Hari Hoang, Thanh T. McClanahan, Kylie Grady, Stephen K. Shew, Woodrow L. |
author_facet | Gautam, Shree Hari Hoang, Thanh T. McClanahan, Kylie Grady, Stephen K. Shew, Woodrow L. |
author_sort | Gautam, Shree Hari |
collection | PubMed |
description | Modulation of interactions among neurons can manifest as dramatic changes in the state of population dynamics in cerebral cortex. How such transitions in cortical state impact the information processing performed by cortical circuits is not clear. Here we performed experiments and computational modeling to determine how somatosensory dynamic range depends on cortical state. We used microelectrode arrays to record ongoing and whisker stimulus-evoked population spiking activity in somatosensory cortex of urethane anesthetized rats. We observed a continuum of different cortical states; at one extreme population activity exhibited small scale variability and was weakly correlated, the other extreme had large scale fluctuations and strong correlations. In experiments, shifts along the continuum often occurred naturally, without direct manipulation. In addition, in both the experiment and the model we directly tuned the cortical state by manipulating inhibitory synaptic interactions. Our principal finding was that somatosensory dynamic range was maximized in a specific cortical state, called criticality, near the tipping point midway between the ends of the continuum. The optimal cortical state was uniquely characterized by scale-free ongoing population dynamics and moderate correlations, in line with theoretical predictions about criticality. However, to reproduce our experimental findings, we found that existing theory required modifications which account for activity-dependent depression. In conclusion, our experiments indicate that in vivo sensory dynamic range is maximized near criticality and our model revealed an unanticipated role for activity-dependent depression in this basic principle of cortical function. |
format | Online Article Text |
id | pubmed-4666488 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-46664882015-12-10 Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality Gautam, Shree Hari Hoang, Thanh T. McClanahan, Kylie Grady, Stephen K. Shew, Woodrow L. PLoS Comput Biol Research Article Modulation of interactions among neurons can manifest as dramatic changes in the state of population dynamics in cerebral cortex. How such transitions in cortical state impact the information processing performed by cortical circuits is not clear. Here we performed experiments and computational modeling to determine how somatosensory dynamic range depends on cortical state. We used microelectrode arrays to record ongoing and whisker stimulus-evoked population spiking activity in somatosensory cortex of urethane anesthetized rats. We observed a continuum of different cortical states; at one extreme population activity exhibited small scale variability and was weakly correlated, the other extreme had large scale fluctuations and strong correlations. In experiments, shifts along the continuum often occurred naturally, without direct manipulation. In addition, in both the experiment and the model we directly tuned the cortical state by manipulating inhibitory synaptic interactions. Our principal finding was that somatosensory dynamic range was maximized in a specific cortical state, called criticality, near the tipping point midway between the ends of the continuum. The optimal cortical state was uniquely characterized by scale-free ongoing population dynamics and moderate correlations, in line with theoretical predictions about criticality. However, to reproduce our experimental findings, we found that existing theory required modifications which account for activity-dependent depression. In conclusion, our experiments indicate that in vivo sensory dynamic range is maximized near criticality and our model revealed an unanticipated role for activity-dependent depression in this basic principle of cortical function. Public Library of Science 2015-12-01 /pmc/articles/PMC4666488/ /pubmed/26623645 http://dx.doi.org/10.1371/journal.pcbi.1004576 Text en © 2015 Gautam 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, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Gautam, Shree Hari Hoang, Thanh T. McClanahan, Kylie Grady, Stephen K. Shew, Woodrow L. Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title | Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title_full | Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title_fullStr | Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title_full_unstemmed | Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title_short | Maximizing Sensory Dynamic Range by Tuning the Cortical State to Criticality |
title_sort | maximizing sensory dynamic range by tuning the cortical state to criticality |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4666488/ https://www.ncbi.nlm.nih.gov/pubmed/26623645 http://dx.doi.org/10.1371/journal.pcbi.1004576 |
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