A quantitative theory of gamma synchronization in macaque V1

  1. Eric Lowet  Is a corresponding author
  2. Mark Jonathan Roberts
  3. Alina Peter
  4. Bart Gips
  5. Peter de Weerd
  1. Boston University, United States
  2. Maastricht University, Netherlands
  3. Ernst Strüngmann Institute for Neuroscience in Cooperation with Max PLanck Society, Germany
  4. Radboud University, Netherlands

Abstract

Gamma-band synchronization coordinates brief periods of excitability in oscillating neuronal populations to optimize information transmission during sensation and cognition. Commonly, a stable, shared frequency over time is considered a condition for functional neural synchronization. Here, we demonstrate the opposite: instantaneous frequency modulations are critical to regulate phase relations and synchronization. In monkey visual area V1, nearby local populations driven by different visual stimulation showed different gamma frequencies. When similar enough, these frequencies continually attracted and repulsed each other, which enabled preferred phase relations to be maintained in periods of minimized frequency difference. Crucially, the precise dynamics of frequencies and phases across a wide range of stimulus conditions was predicted from a physics theory that describes how weakly coupled oscillators influence each other’s phase relations. Hence, the fundamental mathematical principle of synchronization through instantaneous frequency modulations applies to gamma in V1, and is likely generalizable to other brain regions and rhythms.

Article and author information

Author details

  1. Eric Lowet

    Boston University, Boston, United States
    For correspondence
    elowet@mailfence.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9793-0639
  2. Mark Jonathan Roberts

    Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. Alina Peter

    Ernst Strüngmann Institute for Neuroscience in Cooperation with Max PLanck Society, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Bart Gips

    Donders Institute for Brain,Cognition and Behavior, Radboud University, Nijmegen, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Peter de Weerd

    Boston University, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (451-09-025)

  • Mark Jonathan Roberts

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (453-04-002)

  • Peter de Weerd

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

Ethics

Animal experimentation: All the procedures were in accordance with the European council directive 684 2010/63/EU, the Dutch 'experiments on animal acts' (1997) and approved by the Radboud 685 University ethical committee on experiments with animals (Dier‐Experimenten‐Commissie, 686 DEC).

Reviewing Editor

  1. Charles E Schroeder, Columbia University College of Physicians and Surgeons, United States

Publication history

  1. Received: March 8, 2017
  2. Accepted: August 21, 2017
  3. Accepted Manuscript published: August 31, 2017 (version 1)
  4. Version of Record published: September 25, 2017 (version 2)
  5. Version of Record updated: November 8, 2017 (version 3)

Copyright

© 2017, Lowet et al.

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.

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  1. Eric Lowet
  2. Mark Jonathan Roberts
  3. Alina Peter
  4. Bart Gips
  5. Peter de Weerd
(2017)
A quantitative theory of gamma synchronization in macaque V1
eLife 6:e26642.
https://doi.org/10.7554/eLife.26642

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