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      The rate of transient beta frequency events predicts behavior across tasks and species

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          Abstract

          Beta oscillations (15-29Hz) are among the most prominent signatures of brain activity. Beta power is predictive of healthy and abnormal behaviors, including perception, attention and motor action. In non-averaged signals, beta can emerge as transient high-power 'events'. As such, functionally relevant differences in averaged power across time and trials can reflect changes in event number, power, duration, and/or frequency span. We show that functionally relevant differences in averaged beta power in primary somatosensory neocortex reflect a difference in the number of high-power beta events per trial, i.e. event rate. Further, beta events occurring close to the stimulus were more likely to impair perception. These results are consistent across detection and attention tasks in human magnetoencephalography, and in local field potentials from mice performing a detection task. These results imply that an increased propensity of beta events predicts the failure to effectively transmit information through specific neocortical representations.

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          Most cited references39

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          Dynamic predictions: oscillations and synchrony in top-down processing.

          Classical theories of sensory processing view the brain as a passive, stimulus-driven device. By contrast, more recent approaches emphasize the constructive nature of perception, viewing it as an active and highly selective process. Indeed, there is ample evidence that the processing of stimuli is controlled by top-down influences that strongly shape the intrinsic dynamics of thalamocortical networks and constantly create predictions about forthcoming sensory events. We discuss recent experiments indicating that such predictions might be embodied in the temporal structure of both stimulus-evoked and ongoing activity, and that synchronous oscillations are particularly important in this process. Coherence among subthreshold membrane potential fluctuations could be exploited to express selective functional relationships during states of expectancy or attention, and these dynamic patterns could allow the grouping and selection of distributed neuronal responses for further processing.
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            The θ-γ neural code.

            Theta and gamma frequency oscillations occur in the same brain regions and interact with each other, a process called cross-frequency coupling. Here, we review evidence for the following hypothesis: that the dual oscillations form a code for representing multiple items in an ordered way. This form of coding has been most clearly demonstrated in the hippocampus, where different spatial information is represented in different gamma subcycles of a theta cycle. Other experiments have tested the functional importance of oscillations and their coupling. These involve correlation of oscillatory properties with memory states, correlation with memory performance, and effects of disrupting oscillations on memory. Recent work suggests that this coding scheme coordinates communication between brain regions and is involved in sensory as well as memory processes. Copyright © 2013 Elsevier Inc. All rights reserved.
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              A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex.

              A basic feature of intelligent systems such as the cerebral cortex is the ability to freely associate aspects of perceived experience with an internal representation of the world and make predictions about the future. Here, a hypothesis is presented that the extraordinary performance of the cortex derives from an associative mechanism built in at the cellular level to the basic cortical neuronal unit: the pyramidal cell. The mechanism is robustly triggered by coincident input to opposite poles of the neuron, is exquisitely matched to the large- and fine-scale architecture of the cortex, and is tightly controlled by local microcircuits of inhibitory neurons targeting subcellular compartments. This article explores the experimental evidence and the implications for how the cortex operates. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                06 November 2017
                2017
                : 6
                : e29086
                Affiliations
                [1 ]deptDepartment of Neuroscience Brown University ProvidenceUnited States
                [2 ]deptCenter for Neurorestoration and Neurotechnology Providence VA Medical Center ProvidenceUnited States
                The Nathan S. Kline Institute for Psychiatric Research United States
                The Nathan S. Kline Institute for Psychiatric Research United States
                Author information
                http://orcid.org/0000-0002-7587-8577
                http://orcid.org/0000-0003-3805-1519
                http://orcid.org/0000-0001-6760-5301
                Article
                29086
                10.7554/eLife.29086
                5683757
                29106374
                5b4678a3-7d2b-473f-a41c-e912f80671ac

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 30 May 2017
                : 03 November 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100011184, Brown Institute for Brain Science;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010629, Fulbright Association;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: R01NS045130
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000025, National Institute of Mental Health;
                Award ID: R01MH106174
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000738, U.S. Department of Veterans Affairs;
                Award ID: Veterans Health Administration, Office of Research and Development, Rehabilitation Research and Development Service; N9228-C
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: Collaborative Research in Computational Neuroscience NSF CRCNS-1131850
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000070, National Institute of Biomedical Imaging and Bioengineering;
                Award ID: RO1EB022889
                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
                Across species, tasks and recording modalities, the rate of transient neocortical beta frequency (15-29Hz) events strongly predicts perceptual ability, providing fundamental mechanistic insight, with implications for tracking and manipulating brain dynamics.

                Life sciences
                beta rhythm,perception,attention,somatosensory,functional homology,transient oscillation,human,mouse

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