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Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition

The varied cognitive abilities and rich adaptive behaviors enabled by the animal nervous system are often described in terms of information processing. This framing raises the issue of how biological neural circuits actually process information, and some of the most fundamental outstanding questions...

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Autores principales: Newman, Ehren L., Varley, Thomas F., Parakkattu, Vibin K., Sherrill, Samantha P., Beggs, John M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9319160/
https://www.ncbi.nlm.nih.gov/pubmed/35885153
http://dx.doi.org/10.3390/e24070930
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author Newman, Ehren L.
Varley, Thomas F.
Parakkattu, Vibin K.
Sherrill, Samantha P.
Beggs, John M.
author_facet Newman, Ehren L.
Varley, Thomas F.
Parakkattu, Vibin K.
Sherrill, Samantha P.
Beggs, John M.
author_sort Newman, Ehren L.
collection PubMed
description The varied cognitive abilities and rich adaptive behaviors enabled by the animal nervous system are often described in terms of information processing. This framing raises the issue of how biological neural circuits actually process information, and some of the most fundamental outstanding questions in neuroscience center on understanding the mechanisms of neural information processing. Classical information theory has long been understood to be a natural framework within which information processing can be understood, and recent advances in the field of multivariate information theory offer new insights into the structure of computation in complex systems. In this review, we provide an introduction to the conceptual and practical issues associated with using multivariate information theory to analyze information processing in neural circuits, as well as discussing recent empirical work in this vein. Specifically, we provide an accessible introduction to the partial information decomposition (PID) framework. PID reveals redundant, unique, and synergistic modes by which neurons integrate information from multiple sources. We focus particularly on the synergistic mode, which quantifies the “higher-order” information carried in the patterns of multiple inputs and is not reducible to input from any single source. Recent work in a variety of model systems has revealed that synergistic dynamics are ubiquitous in neural circuitry and show reliable structure–function relationships, emerging disproportionately in neuronal rich clubs, downstream of recurrent connectivity, and in the convergence of correlated activity. We draw on the existing literature on higher-order information dynamics in neuronal networks to illustrate the insights that have been gained by taking an information decomposition perspective on neural activity. Finally, we briefly discuss future promising directions for information decomposition approaches to neuroscience, such as work on behaving animals, multi-target generalizations of PID, and time-resolved local analyses.
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spelling pubmed-93191602022-07-27 Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition Newman, Ehren L. Varley, Thomas F. Parakkattu, Vibin K. Sherrill, Samantha P. Beggs, John M. Entropy (Basel) Review The varied cognitive abilities and rich adaptive behaviors enabled by the animal nervous system are often described in terms of information processing. This framing raises the issue of how biological neural circuits actually process information, and some of the most fundamental outstanding questions in neuroscience center on understanding the mechanisms of neural information processing. Classical information theory has long been understood to be a natural framework within which information processing can be understood, and recent advances in the field of multivariate information theory offer new insights into the structure of computation in complex systems. In this review, we provide an introduction to the conceptual and practical issues associated with using multivariate information theory to analyze information processing in neural circuits, as well as discussing recent empirical work in this vein. Specifically, we provide an accessible introduction to the partial information decomposition (PID) framework. PID reveals redundant, unique, and synergistic modes by which neurons integrate information from multiple sources. We focus particularly on the synergistic mode, which quantifies the “higher-order” information carried in the patterns of multiple inputs and is not reducible to input from any single source. Recent work in a variety of model systems has revealed that synergistic dynamics are ubiquitous in neural circuitry and show reliable structure–function relationships, emerging disproportionately in neuronal rich clubs, downstream of recurrent connectivity, and in the convergence of correlated activity. We draw on the existing literature on higher-order information dynamics in neuronal networks to illustrate the insights that have been gained by taking an information decomposition perspective on neural activity. Finally, we briefly discuss future promising directions for information decomposition approaches to neuroscience, such as work on behaving animals, multi-target generalizations of PID, and time-resolved local analyses. MDPI 2022-07-05 /pmc/articles/PMC9319160/ /pubmed/35885153 http://dx.doi.org/10.3390/e24070930 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Review
Newman, Ehren L.
Varley, Thomas F.
Parakkattu, Vibin K.
Sherrill, Samantha P.
Beggs, John M.
Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title_full Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title_fullStr Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title_full_unstemmed Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title_short Revealing the Dynamics of Neural Information Processing with Multivariate Information Decomposition
title_sort revealing the dynamics of neural information processing with multivariate information decomposition
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9319160/
https://www.ncbi.nlm.nih.gov/pubmed/35885153
http://dx.doi.org/10.3390/e24070930
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