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The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping

Our motor commands can be exquisitely timed according to the demands of the environment, and the ability to generate rhythms of different tempos is a hallmark of musical cognition. Yet, the neuronal underpinnings behind rhythmic tapping remain elusive. Here, we found that the activity of hundreds of...

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Autores principales: Gámez, Jorge, Mendoza, Germán, Prado, Luis, Betancourt, Abraham, Merchant, Hugo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6472824/
https://www.ncbi.nlm.nih.gov/pubmed/30958818
http://dx.doi.org/10.1371/journal.pbio.3000054
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author Gámez, Jorge
Mendoza, Germán
Prado, Luis
Betancourt, Abraham
Merchant, Hugo
author_facet Gámez, Jorge
Mendoza, Germán
Prado, Luis
Betancourt, Abraham
Merchant, Hugo
author_sort Gámez, Jorge
collection PubMed
description Our motor commands can be exquisitely timed according to the demands of the environment, and the ability to generate rhythms of different tempos is a hallmark of musical cognition. Yet, the neuronal underpinnings behind rhythmic tapping remain elusive. Here, we found that the activity of hundreds of primate medial premotor cortices (MPCs; pre-supplementary motor area [preSMA] and supplementary motor area [SMA]) neurons show a strong periodic pattern that becomes evident when their responses are projected into a state space using dimensionality reduction analysis. We show that different tapping tempos are encoded by circular trajectories that travelled at a constant speed but with different radii, and that this neuronal code is highly resilient to the number of participating neurons. Crucially, the changes in the amplitude of the oscillatory dynamics in neuronal state space are a signature of duration encoding during rhythmic timing, regardless of whether it is guided by an external metronome or is internally controlled and is not the result of repetitive motor commands. This dynamic state signal predicted the duration of the rhythmically produced intervals on a trial-by-trial basis. Furthermore, the increase in variability of the neural trajectories accounted for the scalar property, a hallmark feature of temporal processing across tasks and species. Finally, we found that the interval-dependent increments in the radius of periodic neural trajectories are the result of a larger number of neurons engaged in the production of longer intervals. Our results support the notion that rhythmic timing during tapping behaviors is encoded in the radial curvature of periodic MPC neural population trajectories.
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spelling pubmed-64728242019-05-03 The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping Gámez, Jorge Mendoza, Germán Prado, Luis Betancourt, Abraham Merchant, Hugo PLoS Biol Research Article Our motor commands can be exquisitely timed according to the demands of the environment, and the ability to generate rhythms of different tempos is a hallmark of musical cognition. Yet, the neuronal underpinnings behind rhythmic tapping remain elusive. Here, we found that the activity of hundreds of primate medial premotor cortices (MPCs; pre-supplementary motor area [preSMA] and supplementary motor area [SMA]) neurons show a strong periodic pattern that becomes evident when their responses are projected into a state space using dimensionality reduction analysis. We show that different tapping tempos are encoded by circular trajectories that travelled at a constant speed but with different radii, and that this neuronal code is highly resilient to the number of participating neurons. Crucially, the changes in the amplitude of the oscillatory dynamics in neuronal state space are a signature of duration encoding during rhythmic timing, regardless of whether it is guided by an external metronome or is internally controlled and is not the result of repetitive motor commands. This dynamic state signal predicted the duration of the rhythmically produced intervals on a trial-by-trial basis. Furthermore, the increase in variability of the neural trajectories accounted for the scalar property, a hallmark feature of temporal processing across tasks and species. Finally, we found that the interval-dependent increments in the radius of periodic neural trajectories are the result of a larger number of neurons engaged in the production of longer intervals. Our results support the notion that rhythmic timing during tapping behaviors is encoded in the radial curvature of periodic MPC neural population trajectories. Public Library of Science 2019-04-08 /pmc/articles/PMC6472824/ /pubmed/30958818 http://dx.doi.org/10.1371/journal.pbio.3000054 Text en © 2019 Gámez 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Gámez, Jorge
Mendoza, Germán
Prado, Luis
Betancourt, Abraham
Merchant, Hugo
The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title_full The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title_fullStr The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title_full_unstemmed The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title_short The amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
title_sort amplitude in periodic neural state trajectories underlies the tempo of rhythmic tapping
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6472824/
https://www.ncbi.nlm.nih.gov/pubmed/30958818
http://dx.doi.org/10.1371/journal.pbio.3000054
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