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Role of frequency mismatch in neuronal communication through coherence

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Abstract

Neuronal gamma oscillations have been described in local field potentials of different brain regions of multiple species. Gamma oscillations are thought to reflect rhythmic synaptic activity organized by inhibitory interneurons. While several aspects of gamma rhythmogenesis are relatively well understood, we have much less solid evidence about how gamma oscillations contribute to information processing in neuronal circuits. One popular hypothesis states that a flexible routing of information between distant populations occurs via the control of the phase or coherence between their respective oscillations. Here, we investigate how a mismatch between the frequencies of gamma oscillations from two populations affects their interaction. In particular, we explore a biophysical model of the reciprocal interaction between two cortical areas displaying gamma oscillations at different frequencies, and quantify their phase coherence and communication efficiency. We observed that a moderate excitatory coupling between the two areas leads to a decrease in their frequency detuning, up to ∼6 Hz, with no frequency locking arising between the gamma peaks. Importantly, for similar gamma peak frequencies a zero phase difference emerges for both LFP and MUA despite small axonal delays. For increasing frequency detunings we found a significant decrease in the phase coherence (at non-zero phase lag) between the MUAs but not the LFPs of the two areas. Such difference between LFPs and MUAs behavior is due to the misalignment between the arrival of afferent synaptic currents and the local excitability windows. To test the efficiency of communication we evaluated the success of transferring rate-modulations between the two areas. Our results indicate that once two populations lock their peak frequencies, an optimal phase relation for communication appears. However, the sensitivity of locking to frequency mismatch suggests that only a precise and active control of gamma frequency could enable the selection of communication channels and their directionality.

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Acknowledgments

R.V. thanks Luiz Lana, Jaan Aru, and David Eriksson for fruitful discussions. The authors also thank Pascal Fries for early discussions on the problem of frequency detuning for CTC. This work has been financially supported by the Ministerio de Ciencia e Innovación (project FIS2012-37655). J.G.O. also acknowledges financial support from the ICREA Academia program. R.V. acknowledges financial support from the Hertie Foundation and Estonian Research Council (project BioMedIT SMTAT13061T).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Departament of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona Biomedical Research Park, Barcelona, Spain

    Belén Sancristóbal & Jordi Garcia-Ojalvo

  2. Departament de Física i Enginyeria Nuclear, Universitat Politècnica de Catalunya, Edif. Gaia, Terrassa, Spain

    Belén Sancristóbal & Jordi Garcia-Ojalvo

  3. Max-Planck Institute for Brain Research, Frankfurt am Main, Germany

    Raul Vicente

  4. Institute of Computer Science, Faculty of Mathematics and Computer Science, University of Tartu, 50409, Tartu, Estonia

    Raul Vicente

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  1. Belén Sancristóbal
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Correspondence to Belén Sancristóbal.

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Sancristóbal, B., Vicente, R. & Garcia-Ojalvo, J. Role of frequency mismatch in neuronal communication through coherence. J Comput Neurosci 37, 193–208 (2014). https://doi.org/10.1007/s10827-014-0495-7

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  • DOI: https://doi.org/10.1007/s10827-014-0495-7

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