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Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled

Several theories have been advanced to explain how cross-frequency coupling, the interaction of neuronal oscillations at different frequencies, could enable item multiplexing in neural systems. The communication-through-coherence theory proposes that phase-matching of gamma oscillations between area...

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Autores principales: McLelland, Douglas, VanRullen, Rufin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5065198/
https://www.ncbi.nlm.nih.gov/pubmed/27741229
http://dx.doi.org/10.1371/journal.pcbi.1005162
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author McLelland, Douglas
VanRullen, Rufin
author_facet McLelland, Douglas
VanRullen, Rufin
author_sort McLelland, Douglas
collection PubMed
description Several theories have been advanced to explain how cross-frequency coupling, the interaction of neuronal oscillations at different frequencies, could enable item multiplexing in neural systems. The communication-through-coherence theory proposes that phase-matching of gamma oscillations between areas enables selective processing of a single item at a time, and a later refinement of the theory includes a theta-frequency oscillation that provides a periodic reset of the system. Alternatively, the theta-gamma neural code theory proposes that a sequence of items is processed, one per gamma cycle, and that this sequence is repeated or updated across theta cycles. In short, both theories serve to segregate representations via the temporal domain, but differ on the number of objects concurrently represented. In this study, we set out to test whether each of these theories is actually physiologically plausible, by implementing them within a single model inspired by physiological data. Using a spiking network model of visual processing, we show that each of these theories is physiologically plausible and computationally useful. Both theories were implemented within a single network architecture, with two areas connected in a feedforward manner, and gamma oscillations generated by feedback inhibition within areas. Simply increasing the amplitude of global inhibition in the lower area, equivalent to an increase in the spatial scope of the gamma oscillation, yielded a switch from one mode to the other. Thus, these different processing modes may co-exist in the brain, enabling dynamic switching between exploratory and selective modes of attention.
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spelling pubmed-50651982016-10-27 Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled McLelland, Douglas VanRullen, Rufin PLoS Comput Biol Research Article Several theories have been advanced to explain how cross-frequency coupling, the interaction of neuronal oscillations at different frequencies, could enable item multiplexing in neural systems. The communication-through-coherence theory proposes that phase-matching of gamma oscillations between areas enables selective processing of a single item at a time, and a later refinement of the theory includes a theta-frequency oscillation that provides a periodic reset of the system. Alternatively, the theta-gamma neural code theory proposes that a sequence of items is processed, one per gamma cycle, and that this sequence is repeated or updated across theta cycles. In short, both theories serve to segregate representations via the temporal domain, but differ on the number of objects concurrently represented. In this study, we set out to test whether each of these theories is actually physiologically plausible, by implementing them within a single model inspired by physiological data. Using a spiking network model of visual processing, we show that each of these theories is physiologically plausible and computationally useful. Both theories were implemented within a single network architecture, with two areas connected in a feedforward manner, and gamma oscillations generated by feedback inhibition within areas. Simply increasing the amplitude of global inhibition in the lower area, equivalent to an increase in the spatial scope of the gamma oscillation, yielded a switch from one mode to the other. Thus, these different processing modes may co-exist in the brain, enabling dynamic switching between exploratory and selective modes of attention. Public Library of Science 2016-10-14 /pmc/articles/PMC5065198/ /pubmed/27741229 http://dx.doi.org/10.1371/journal.pcbi.1005162 Text en © 2016 McLelland, VanRullen 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
McLelland, Douglas
VanRullen, Rufin
Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title_full Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title_fullStr Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title_full_unstemmed Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title_short Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled
title_sort theta-gamma coding meets communication-through-coherence: neuronal oscillatory multiplexing theories reconciled
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5065198/
https://www.ncbi.nlm.nih.gov/pubmed/27741229
http://dx.doi.org/10.1371/journal.pcbi.1005162
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