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Preserved neural dynamics across animals performing similar behaviour

Animals of the same species exhibit similar behaviours that are advantageously adapted to their body and environment. These behaviours are shaped at the species level by selection pressures over evolutionary timescales. Yet, it remains unclear how these common behavioural adaptations emerge from the...

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Autores principales: Safaie, Mostafa, Chang, Joanna C., Park, Junchol, Miller, Lee E., Dudman, Joshua T., Perich, Matthew G., Gallego, Juan A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665198/
https://www.ncbi.nlm.nih.gov/pubmed/37938772
http://dx.doi.org/10.1038/s41586-023-06714-0
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author Safaie, Mostafa
Chang, Joanna C.
Park, Junchol
Miller, Lee E.
Dudman, Joshua T.
Perich, Matthew G.
Gallego, Juan A.
author_facet Safaie, Mostafa
Chang, Joanna C.
Park, Junchol
Miller, Lee E.
Dudman, Joshua T.
Perich, Matthew G.
Gallego, Juan A.
author_sort Safaie, Mostafa
collection PubMed
description Animals of the same species exhibit similar behaviours that are advantageously adapted to their body and environment. These behaviours are shaped at the species level by selection pressures over evolutionary timescales. Yet, it remains unclear how these common behavioural adaptations emerge from the idiosyncratic neural circuitry of each individual. The overall organization of neural circuits is preserved across individuals(1) because of their common evolutionarily specified developmental programme(2–4). Such organization at the circuit level may constrain neural activity(5–8), leading to low-dimensional latent dynamics across the neural population(9–11). Accordingly, here we suggested that the shared circuit-level constraints within a species would lead to suitably preserved latent dynamics across individuals. We analysed recordings of neural populations from monkey and mouse motor cortex to demonstrate that neural dynamics in individuals from the same species are surprisingly preserved when they perform similar behaviour. Neural population dynamics were also preserved when animals consciously planned future movements without overt behaviour(12) and enabled the decoding of planned and ongoing movement across different individuals. Furthermore, we found that preserved neural dynamics extend beyond cortical regions to the dorsal striatum, an evolutionarily older structure(13,14). Finally, we used neural network models to demonstrate that behavioural similarity is necessary but not sufficient for this preservation. We posit that these emergent dynamics result from evolutionary constraints on brain development and thus reflect fundamental properties of the neural basis of behaviour.
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spelling pubmed-106651982023-11-08 Preserved neural dynamics across animals performing similar behaviour Safaie, Mostafa Chang, Joanna C. Park, Junchol Miller, Lee E. Dudman, Joshua T. Perich, Matthew G. Gallego, Juan A. Nature Article Animals of the same species exhibit similar behaviours that are advantageously adapted to their body and environment. These behaviours are shaped at the species level by selection pressures over evolutionary timescales. Yet, it remains unclear how these common behavioural adaptations emerge from the idiosyncratic neural circuitry of each individual. The overall organization of neural circuits is preserved across individuals(1) because of their common evolutionarily specified developmental programme(2–4). Such organization at the circuit level may constrain neural activity(5–8), leading to low-dimensional latent dynamics across the neural population(9–11). Accordingly, here we suggested that the shared circuit-level constraints within a species would lead to suitably preserved latent dynamics across individuals. We analysed recordings of neural populations from monkey and mouse motor cortex to demonstrate that neural dynamics in individuals from the same species are surprisingly preserved when they perform similar behaviour. Neural population dynamics were also preserved when animals consciously planned future movements without overt behaviour(12) and enabled the decoding of planned and ongoing movement across different individuals. Furthermore, we found that preserved neural dynamics extend beyond cortical regions to the dorsal striatum, an evolutionarily older structure(13,14). Finally, we used neural network models to demonstrate that behavioural similarity is necessary but not sufficient for this preservation. We posit that these emergent dynamics result from evolutionary constraints on brain development and thus reflect fundamental properties of the neural basis of behaviour. Nature Publishing Group UK 2023-11-08 2023 /pmc/articles/PMC10665198/ /pubmed/37938772 http://dx.doi.org/10.1038/s41586-023-06714-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Safaie, Mostafa
Chang, Joanna C.
Park, Junchol
Miller, Lee E.
Dudman, Joshua T.
Perich, Matthew G.
Gallego, Juan A.
Preserved neural dynamics across animals performing similar behaviour
title Preserved neural dynamics across animals performing similar behaviour
title_full Preserved neural dynamics across animals performing similar behaviour
title_fullStr Preserved neural dynamics across animals performing similar behaviour
title_full_unstemmed Preserved neural dynamics across animals performing similar behaviour
title_short Preserved neural dynamics across animals performing similar behaviour
title_sort preserved neural dynamics across animals performing similar behaviour
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10665198/
https://www.ncbi.nlm.nih.gov/pubmed/37938772
http://dx.doi.org/10.1038/s41586-023-06714-0
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