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Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics

Back in 2012, Churchland and his colleagues proposed that “rotational dynamics”, uncovered through linear transformations of multidimensional neuronal data, represent a fundamental type of neuronal population processing in a variety of organisms, from the isolated leech central nervous system to the...

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Autores principales: Lebedev, Mikhail A., Ossadtchi, Alexei, Mill, Nil Adell, Urpí, Núria Armengol, Cervera, Maria R., Nicolelis, Miguel A. L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908571/
https://www.ncbi.nlm.nih.gov/pubmed/31831758
http://dx.doi.org/10.1038/s41598-019-54760-4
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author Lebedev, Mikhail A.
Ossadtchi, Alexei
Mill, Nil Adell
Urpí, Núria Armengol
Cervera, Maria R.
Nicolelis, Miguel A. L.
author_facet Lebedev, Mikhail A.
Ossadtchi, Alexei
Mill, Nil Adell
Urpí, Núria Armengol
Cervera, Maria R.
Nicolelis, Miguel A. L.
author_sort Lebedev, Mikhail A.
collection PubMed
description Back in 2012, Churchland and his colleagues proposed that “rotational dynamics”, uncovered through linear transformations of multidimensional neuronal data, represent a fundamental type of neuronal population processing in a variety of organisms, from the isolated leech central nervous system to the primate motor cortex. Here, we evaluated this claim using Churchland’s own data and simple simulations of neuronal responses. We observed that rotational patterns occurred in neuronal populations when (1) there was a temporal sequence in peak firing rates exhibited by individual neurons, and (2) this sequence remained consistent across different experimental conditions. Provided that such a temporal order of peak firing rates existed, rotational patterns could be easily obtained using a rather arbitrary computer simulation of neural activity; modeling of any realistic properties of motor cortical responses was not needed. Additionally, arbitrary traces, such as Lissajous curves, could be easily obtained from Churchland’s data with multiple linear regression. While these observations suggest that temporal sequences of neuronal responses could be visualized as rotations with various methods, we express doubt about Churchland et al.’s bold assessment that such rotations are related to “an unexpected yet surprisingly simple structure in the population response”, which “explains many of the confusing features of individual neural responses”. Instead, we argue that their approach provides little, if any, insight on the underlying neuronal mechanisms employed by neuronal ensembles to encode motor behaviors in any species.
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spelling pubmed-69085712019-12-16 Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics Lebedev, Mikhail A. Ossadtchi, Alexei Mill, Nil Adell Urpí, Núria Armengol Cervera, Maria R. Nicolelis, Miguel A. L. Sci Rep Article Back in 2012, Churchland and his colleagues proposed that “rotational dynamics”, uncovered through linear transformations of multidimensional neuronal data, represent a fundamental type of neuronal population processing in a variety of organisms, from the isolated leech central nervous system to the primate motor cortex. Here, we evaluated this claim using Churchland’s own data and simple simulations of neuronal responses. We observed that rotational patterns occurred in neuronal populations when (1) there was a temporal sequence in peak firing rates exhibited by individual neurons, and (2) this sequence remained consistent across different experimental conditions. Provided that such a temporal order of peak firing rates existed, rotational patterns could be easily obtained using a rather arbitrary computer simulation of neural activity; modeling of any realistic properties of motor cortical responses was not needed. Additionally, arbitrary traces, such as Lissajous curves, could be easily obtained from Churchland’s data with multiple linear regression. While these observations suggest that temporal sequences of neuronal responses could be visualized as rotations with various methods, we express doubt about Churchland et al.’s bold assessment that such rotations are related to “an unexpected yet surprisingly simple structure in the population response”, which “explains many of the confusing features of individual neural responses”. Instead, we argue that their approach provides little, if any, insight on the underlying neuronal mechanisms employed by neuronal ensembles to encode motor behaviors in any species. Nature Publishing Group UK 2019-12-12 /pmc/articles/PMC6908571/ /pubmed/31831758 http://dx.doi.org/10.1038/s41598-019-54760-4 Text en © The Author(s) 2019 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Lebedev, Mikhail A.
Ossadtchi, Alexei
Mill, Nil Adell
Urpí, Núria Armengol
Cervera, Maria R.
Nicolelis, Miguel A. L.
Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title_full Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title_fullStr Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title_full_unstemmed Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title_short Analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
title_sort analysis of neuronal ensemble activity reveals the pitfalls and shortcomings of rotation dynamics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6908571/
https://www.ncbi.nlm.nih.gov/pubmed/31831758
http://dx.doi.org/10.1038/s41598-019-54760-4
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