A quantitative theory of gamma synchronization in macaque V1

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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.

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Eric Lowet

Boston University, Boston, United States

For correspondence
elowet@mailfence.com

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9793-0639
Mark Jonathan Roberts

Psychology and Neuroscience, Maastricht University, Maastricht, Netherlands

Competing interests
The authors declare that no competing interests exist.
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.
Bart Gips

Donders Institute for Brain,Cognition and Behavior, Radboud University, Nijmegen, Netherlands

Competing interests
The authors declare that no competing interests exist.
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).

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.