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Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus

Cortical computations require coordination of neuronal activity within and across multiple areas. We characterized spiking relationships within and between areas by quantifying coupling of single neurons to population firing patterns. Single-neuron population coupling (SNPC) was investigated using e...

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Autores principales: Dorman, Reinder, Bos, Jeroen J, Vinck, Martin A, Marchesi, Pietro, Fiorilli, Julien, Lorteije, Jeanette A M, Reiten, Ingrid, Bjaalie, Jan G, Okun, Michael, Pennartz, Cyriel M A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10425201/
https://www.ncbi.nlm.nih.gov/pubmed/37118890
http://dx.doi.org/10.1093/cercor/bhad111
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author Dorman, Reinder
Bos, Jeroen J
Vinck, Martin A
Marchesi, Pietro
Fiorilli, Julien
Lorteije, Jeanette A M
Reiten, Ingrid
Bjaalie, Jan G
Okun, Michael
Pennartz, Cyriel M A
author_facet Dorman, Reinder
Bos, Jeroen J
Vinck, Martin A
Marchesi, Pietro
Fiorilli, Julien
Lorteije, Jeanette A M
Reiten, Ingrid
Bjaalie, Jan G
Okun, Michael
Pennartz, Cyriel M A
author_sort Dorman, Reinder
collection PubMed
description Cortical computations require coordination of neuronal activity within and across multiple areas. We characterized spiking relationships within and between areas by quantifying coupling of single neurons to population firing patterns. Single-neuron population coupling (SNPC) was investigated using ensemble recordings from hippocampal CA1 region and somatosensory, visual, and perirhinal cortices. Within-area coupling was heterogeneous across structures, with area CA1 showing higher levels than neocortical regions. In contrast to known anatomical connectivity, between-area coupling showed strong firing coherence of sensory neocortices with CA1, but less with perirhinal cortex. Cells in sensory neocortices and CA1 showed positive correlations between within- and between-area coupling; these were weaker for perirhinal cortex. All four areas harbored broadcasting cells, connecting to multiple external areas, which was uncorrelated to within-area coupling strength. When examining correlations between SNPC and spatial coding, we found that, if such correlations were significant, they were negative. This result was consistent with an overall preservation of SNPC across different brain states, suggesting a strong dependence on intrinsic network connectivity. Overall, SNPC offers an important window on cell-to-population synchronization in multi-area networks. Instead of pointing to specific information-coding functions, our results indicate a primary function of SNPC in dynamically organizing communication in systems composed of multiple, interconnected areas.
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spelling pubmed-104252012023-08-15 Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus Dorman, Reinder Bos, Jeroen J Vinck, Martin A Marchesi, Pietro Fiorilli, Julien Lorteije, Jeanette A M Reiten, Ingrid Bjaalie, Jan G Okun, Michael Pennartz, Cyriel M A Cereb Cortex Original Article Cortical computations require coordination of neuronal activity within and across multiple areas. We characterized spiking relationships within and between areas by quantifying coupling of single neurons to population firing patterns. Single-neuron population coupling (SNPC) was investigated using ensemble recordings from hippocampal CA1 region and somatosensory, visual, and perirhinal cortices. Within-area coupling was heterogeneous across structures, with area CA1 showing higher levels than neocortical regions. In contrast to known anatomical connectivity, between-area coupling showed strong firing coherence of sensory neocortices with CA1, but less with perirhinal cortex. Cells in sensory neocortices and CA1 showed positive correlations between within- and between-area coupling; these were weaker for perirhinal cortex. All four areas harbored broadcasting cells, connecting to multiple external areas, which was uncorrelated to within-area coupling strength. When examining correlations between SNPC and spatial coding, we found that, if such correlations were significant, they were negative. This result was consistent with an overall preservation of SNPC across different brain states, suggesting a strong dependence on intrinsic network connectivity. Overall, SNPC offers an important window on cell-to-population synchronization in multi-area networks. Instead of pointing to specific information-coding functions, our results indicate a primary function of SNPC in dynamically organizing communication in systems composed of multiple, interconnected areas. Oxford University Press 2023-04-28 /pmc/articles/PMC10425201/ /pubmed/37118890 http://dx.doi.org/10.1093/cercor/bhad111 Text en © The Author(s) 2023. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Article
Dorman, Reinder
Bos, Jeroen J
Vinck, Martin A
Marchesi, Pietro
Fiorilli, Julien
Lorteije, Jeanette A M
Reiten, Ingrid
Bjaalie, Jan G
Okun, Michael
Pennartz, Cyriel M A
Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title_full Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title_fullStr Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title_full_unstemmed Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title_short Spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
title_sort spike-based coupling between single neurons and populations across rat sensory cortices, perirhinal cortex, and hippocampus
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10425201/
https://www.ncbi.nlm.nih.gov/pubmed/37118890
http://dx.doi.org/10.1093/cercor/bhad111
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