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      A quantitative theory of gamma synchronization in macaque V1

      research-article
      1 , , 1 , 2 ,   3 , 1 , 4
      eLife
      eLife Sciences Publications, Ltd
      visual cortex, gamma rhythm, synchronization, weakly coupled oscillators, Rhesus macaque

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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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          Simple model of spiking neurons.

          A model is presented that reproduces spiking and bursting behavior of known types of cortical neurons. The model combines the biologically plausibility of Hodgkin-Huxley-type dynamics and the computational efficiency of integrate-and-fire neurons. Using this model, one can simulate tens of thousands of spiking cortical neurons in real time (1 ms resolution) using a desktop PC.
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            Theta oscillations in the hippocampus.

            Theta oscillations represent the "on-line" state of the hippocampus. The extracellular currents underlying theta waves are generated mainly by the entorhinal input, CA3 (Schaffer) collaterals, and voltage-dependent Ca(2+) currents in pyramidal cell dendrites. The rhythm is believed to be critical for temporal coding/decoding of active neuronal ensembles and the modification of synaptic weights. Nevertheless, numerous critical issues regarding both the generation of theta oscillations and their functional significance remain challenges for future research.
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              Mechanisms of gamma oscillations.

              Gamma rhythms are commonly observed in many brain regions during both waking and sleep states, yet their functions and mechanisms remain a matter of debate. Here we review the cellular and synaptic mechanisms underlying gamma oscillations and outline empirical questions and controversial conceptual issues. Our main points are as follows: First, gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition. Second, gamma oscillations are short-lived and typically emerge from the coordinated interaction of excitation and inhibition, which can be detected as local field potentials. Third, gamma rhythm typically concurs with irregular firing of single neurons, and the network frequency of gamma oscillations varies extensively depending on the underlying mechanism. To document gamma oscillations, efforts should be made to distinguish them from mere increases of gamma-band power and/or increased spiking activity. Fourth, the magnitude of gamma oscillation is modulated by slower rhythms. Such cross-frequency coupling may serve to couple active patches of cortical circuits. Because of their ubiquitous nature and strong correlation with the "operational modes" of local circuits, gamma oscillations continue to provide important clues about neuronal population dynamics in health and disease.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                September 25 2017
                31 August 2017
                2017
                : 6
                : e26642
                Affiliations
                [1 ]deptFaculty of Psychology and Neuroscience Maastricht University MaastrichtNetherlands
                [2 ]Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society FrankfurtGermany
                [3 ]deptDonders Institute for Brain, Cognition and Behaviour Radboud University Nijmegen NijmegenNetherlands
                [4 ]deptMaastricht Centre for Systems Biology Maastricht University MaastrichtNetherlands
                Columbia University College of Physicians and Surgeons United States
                Columbia University College of Physicians and Surgeons United States
                Author notes
                [†]

                McGovern Institute, Massachusetts Institute of Technology, Cambridge, United States.

                [‡]

                Boston University, Boston, United States.

                Author information
                http://orcid.org/0000-0002-9793-0639
                Article
                26642
                10.7554/eLife.26642
                5779232
                28857743
                9298172b-5c14-420e-a72a-0765ddb63dd5
                © 2017, Lowet et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 08 March 2017
                : 21 August 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek;
                Award ID: 451-09-025
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek;
                Award ID: 453-04-002
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Gamma-band synchronization behavior in area V1 was predicted by weakly coupled oscillator principles.

                Life sciences
                visual cortex,gamma rhythm,synchronization,weakly coupled oscillators,rhesus macaque
                Life sciences
                visual cortex, gamma rhythm, synchronization, weakly coupled oscillators, rhesus macaque

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