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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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
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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. |
format | Online Article Text |
id | pubmed-6472824 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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