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      Communication between Brain Areas Based on Nested Oscillations

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          Abstract

          Unraveling how brain regions communicate is crucial for understanding how the brain processes external and internal information. Neuronal oscillations within and across brain regions have been proposed to play a crucial role in this process. Two main hypotheses have been suggested for routing of information based on oscillations, namely communication through coherence and gating by inhibition. Here, we propose a framework unifying these two hypotheses that is based on recent empirical findings. We discuss a theory in which communication between two regions is established by phase synchronization of oscillations at lower frequencies (<25 Hz), which serve as temporal reference frame for information carried by high-frequency activity (>40 Hz). Our framework, consistent with numerous recent empirical findings, posits that cross-frequency interactions are essential for understanding how large-scale cognitive and perceptual networks operate.

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          Most cited references 157

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          A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.

           Pascal Fries (2005)
          At any one moment, many neuronal groups in our brain are active. Microelectrode recordings have characterized the activation of single neurons and fMRI has unveiled brain-wide activation patterns. Now it is time to understand how the many active neuronal groups interact with each other and how their communication is flexibly modulated to bring about our cognitive dynamics. I hypothesize that neuronal communication is mechanistically subserved by neuronal coherence. Activated neuronal groups oscillate and thereby undergo rhythmic excitability fluctuations that produce temporal windows for communication. Only coherently oscillating neuronal groups can interact effectively, because their communication windows for input and for output are open at the same times. Thus, a flexible pattern of coherence defines a flexible communication structure, which subserves our cognitive flexibility.
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            The brainweb: phase synchronization and large-scale integration.

            The emergence of a unified cognitive moment relies on the coordination of scattered mosaics of functionally specialized brain regions. Here we review the mechanisms of large-scale integration that counterbalance the distributed anatomical and functional organization of brain activity to enable the emergence of coherent behaviour and cognition. Although the mechanisms involved in large-scale integration are still largely unknown, we argue that the most plausible candidate is the formation of dynamic links mediated by synchrony over multiple frequency bands.
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              EEG alpha oscillations: the inhibition-timing hypothesis.

              The traditional belief is that the event-related alpha response can solely be described in terms of suppression or event-related desynchronization (ERD). Recent research, however, has shown that under certain conditions alpha responds reliably with an increase in amplitudes (event-related synchronization or ERS). ERS is elicited in situations, where subjects withhold or control the execution of a response and is obtained over sites that probably are under, or exert top-down control. Thus, we assume that alpha ERS reflects top-down, inhibitory control processes. This assumption leads over to the timing aspect of our hypothesis. By the very nature of an oscillation, rhythmic amplitude changes reflect rhythmic changes in excitation of a population of neurons. Thus, the time and direction of a change - described by phase - is functionally related to the timing of neuronal activation processes. A variety of findings supports this view and shows, e.g., that alpha phase coherence increases between task-relevant sites and that phase lag lies within a time range that is consistent with neuronal transmission speed. Another implication is that phase reset will be a powerful mechanism for the event-related timing of cortical processes. Empirical evidence suggests that the extent of phase locking is a functionally sensitive measure that is related to cognitive performance. Our general conclusion is that alpha ERS plays an active role for the inhibitory control and timing of cortical processing whereas ERD reflects the gradual release of inhibition associated with the emergence of complex spreading activation processes.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                10 March 2017
                27 March 2017
                Mar-Apr 2017
                : 4
                : 2
                Affiliations
                [1 ]Donders Institute, Centre for Cognitive Neuroimaging, Radboud University , 6525 Nijmegen, Netherlands
                [2 ]Lyon Neuroscience Research Center (CRNL), Brain Dynamics and Cognition Team, INSERM U1028, CNRS UMR5292, Université Claude Bernard Lyon 1, UdL, Lyon, France
                [3 ]Princeton Neuroscience Institute and Department of Psychology, Princeton University , Princeton, New Jersey 08544
                [4 ]University of Birmingham, School of Psychology, Centre for Human Brain Health, Birmingham B15 2TT, UK
                Author notes

                Authors report no conflict of interest.

                Author contributions: MB, SK and OJ wrote the paper.

                Mathilde Bonnefond acknowledges support for the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013)/ERC starting grant agreement no 716862. Ole Jensen and Sabine Kastner acknowledge support from the James S. McDonnell Foundation Understanding Human Cognition Collaborative Award 220020448.

                Correspondence should be addressed to Mathilde Bonnefond. Dycog team CRNL, CH Le Vinatier Bat 452, 95 Boulevard Pinel, 69500 BRON, France. E-mail: mathilde.bonnefond@ 123456inserm.fr .
                Article
                eN-TNC-0153-16
                10.1523/ENEURO.0153-16.2017
                5367085
                Copyright © 2017 Bonnefond et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 156, Pages: 14, Words: 12231
                Product
                Funding
                Funded by: James S. Mc Donnell foundation
                Award ID: 220020448
                Categories
                5
                5.3
                Theory/New Concepts
                Integrative Systems
                Custom metadata
                March/April 2017

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