Input-dependent frequency modulation of cortical gamma oscillations shapes spatial synchronization and enables phase coding

  • Abstract: Fine-scale temporal organization of cortical activity in the gamma range (∼25–80Hz) may play a significant role in information processing, for example by neural grouping ('binding') and phase coding. Recent experimental studies have shown that the precise frequency of gamma oscillations varies with input drive (e.g. visual contrast) and that it can differ among nearby cortical locations. This has challenged theories assuming widespread gamma synchronization at a fixed common frequency. In the present study, we investigated which principles govern gamma synchronization in the presence of input-dependent frequency modulations and whether they are detrimental for meaningful input-dependent gamma-mediated temporal organization. To this aim, we constructed a biophysically realistic excitatory-inhibitory network able to express different oscillation frequencies at nearby spatial locations. Similarly to cortical networks, the model was topographically organized with spatially local connectivity and spatially-varying input drive. We analyzed gamma synchronization with respect to phase-locking, phase-relations and frequency differences, and quantified the stimulus-related information represented by gamma phase and frequency. By stepwise simplification of our models, we found that the gamma-mediated temporal organization could be reduced to basic synchronization principles of weakly coupled oscillators, where input drive determines the intrinsic (natural) frequency of oscillators. The gamma phase-locking, the precise phase relation and the emergent (measurable) frequencies were determined by two principal factors: the detuning (intrinsic frequency difference, i.e. local input difference) and the coupling strength. In addition to frequency coding, gamma phase contained complementary stimulus information. Crucially, the phase code reflected input differences, but not the absolute input level. This property of relative input-to-phase conversion, contrasting with latency codes or slower oscillation phase codes, may resolve conflicting experimental observations on gamma phase coding. Our modeling results offer clear testable experimental predictions. We conclude that input-dependency of gamma frequencies could be essential rather than detrimental for meaningful gamma-mediated temporal organization of cortical activity. Author Summary: Almost 350 years ago the physicist and polymath Christiaan Huygens first observed the synchronization between two pendulum clocks attached to a common support. Since then synchronization has been recognized as a universal phenomenon from astronomy to biology. The phase-locking (synchrony) and the phase-relation between the two pendulums are determined by two principal forces: the synchronization force exerted over the connection and the tendency to desynchronize due to frequency (speed) differences. We propose that gamma synchronization (25–80Hz) among oscillating cortical neurons in the brain can be understood according to the same principles—like a field of many connected pendula—with the critical addition that input changes the frequency of gamma oscillations, as shown by recent experimental studies. It has been assumed that input-dependent changes in oscillation frequency are detrimental for a meaningful role of gamma synchronization in neural processing. To the contrary, our theoretical analysis demonstrates that because input can change the frequency of the oscillation, phase-locking and phase-relations among neurons relate systematically to input. By analogy, it is because a local push to a pendulum will change its frequency, that resulting changes in phase-locking and phase-relation among the pendula can be used to derive the external force applied.
Metadaten
Author:Eric Lowet, Mark Roberts, Avgis Hadjipapas, Alina Peter, Jan van der Eerden, Peter De Weerd
URN:urn:nbn:de:hebis:30:3-391797
DOI:https://doi.org/10.1371/journal.pcbi.1004072
ISSN:1553-7358
ISSN:1553-734X
Parent Title (English):PLoS Computational Biology, volume 11, issue 2, e1004072 (2015)
Publisher:PLoS
Place of publication:Lawrence, Kan.
Document Type:Article
Language:English
Date of Publication (online):2015/02/13
Date of first Publication:2015/02/13
Publishing Institution:Universitätsbibliothek Johann Christian Senckenberg
Release Date:2016/02/04
Volume:11
Issue:(2): e1004072
Page Number:44
First Page:1
Last Page:44
Note:
Copyright: © 2015 Lowet et al. 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.
HeBIS-PPN:376430052
Dewey Decimal Classification:5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie
Sammlungen:Universitätspublikationen
Licence (German):License LogoCreative Commons - Namensnennung 4.0