Entrainment and maintenance of an internal metronome in supplementary motor area

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Cite this article as: eLife 2018;7:e38983 doi: 10.7554/eLife.38983

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Abstract

To prepare timely motor actions we constantly predict future events. Regularly repeating events are often perceived as a rhythm to which we can readily synchronize our movements, just as in dancing to music. However, the neuronal mechanisms underlying the capacity to encode and maintain rhythms are not understood. We trained nonhuman primates to maintain the rhythm of a visual metronome of diverse tempos and recorded neural activity in the supplementary motor area (SMA). SMA exhibited rhythmic bursts of gamma band (30-40 Hz) reflecting an internal tempo that matched the extinguished visual metronome. Moreover, gamma amplitude increased throughout the trial, providing an estimate of total elapsed time. Notably, the timing of gamma bursts and firing rate modulations allowed predicting whether monkeys were ahead or behind the correct tempo. Our results indicate that SMA uses dynamic motor plans to encode a metronome for rhythms and a stopwatch for total elapsed time.

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Author details

Jaime Cadena-Valencia

Institute of Neurobiology, National Autonomous University of Mexico, Querétaro, Mexico

Competing interests
The authors declare that no competing interests exist.
Otto García-Garibay

Institute of Neurobiology, National Autonomous University of Mexico, Querétaro, Mexico

Competing interests
The authors declare that no competing interests exist.
Hugo Merchant

Institute of Neurobiology, National Autonomous University of Mexico, Queretaro, Mexico

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-3488-9501
Mehrdad Jazayeri

McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
The authors declare that no competing interests exist.
Victor de Lafuente

Institute of Neurobiology, National Autonomous University of Mexico, Queretaro, Mexico

For correspondence
lafuente@unam.mx

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1047-1354

Funding

Consejo Nacional de Ciencia y Tecnología (Fronteras de la Ciencia 196)

Hugo Merchant

Universidad Nacional Autónoma de México (PAPIIT IN207818)

Victor de Lafuente

Consejo Nacional de Ciencia y Tecnología (Ciencia Básica 254313)

Victor de Lafuente

Consejo Nacional de Ciencia y Tecnología (Ciencia Básica 236836)

Hugo Merchant

Consejo Nacional de Ciencia y Tecnología (Fronteras de la Ciencia 245)

Victor de Lafuente

Universidad Nacional Autónoma de México (PAPIIT IN202317)

Hugo Merchant

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Experimental procedures were approved by the Ethics in Research Committee of the Institute of Neurobiology (protocol number 046) and were in agreement with the principles outlined in the Guide for Care and Use of Laboratory Animals (National Institutes of Health).

Reviewing Editor

Richard B Ivry, University of California, Berkeley, United States

Publication history

Received: June 7, 2018
Accepted: October 21, 2018
Accepted Manuscript published: October 22, 2018 (version 1)
Version of Record published: November 21, 2018 (version 2)

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.