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      Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice.

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          Abstract

          Human neocortical 15-29-Hz beta oscillations are strong predictors of perceptual and motor performance. However, the mechanistic origin of beta in vivo is unknown, hindering understanding of its functional role. Combining human magnetoencephalography (MEG), computational modeling, and laminar recordings in animals, we present a new theory that accounts for the origin of spontaneous neocortical beta. In our MEG data, spontaneous beta activity from somatosensory and frontal cortex emerged as noncontinuous beta events typically lasting <150 ms with a stereotypical waveform. Computational modeling uniquely designed to infer the electrical currents underlying these signals showed that beta events could emerge from the integration of nearly synchronous bursts of excitatory synaptic drive targeting proximal and distal dendrites of pyramidal neurons, where the defining feature of a beta event was a strong distal drive that lasted one beta period (∼50 ms). This beta mechanism rigorously accounted for the beta event profiles; several other mechanisms did not. The spatial location of synaptic drive in the model to supragranular and infragranular layers was critical to the emergence of beta events and led to the prediction that beta events should be associated with a specific laminar current profile. Laminar recordings in somatosensory neocortex from anesthetized mice and awake monkeys supported these predictions, suggesting this beta mechanism is conserved across species and recording modalities. These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function.

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          Most cited references 64

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          The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes.

          Neuronal activity in the brain gives rise to transmembrane currents that can be measured in the extracellular medium. Although the major contributor of the extracellular signal is the synaptic transmembrane current, other sources--including Na(+) and Ca(2+) spikes, ionic fluxes through voltage- and ligand-gated channels, and intrinsic membrane oscillations--can substantially shape the extracellular field. High-density recordings of field activity in animals and subdural grid recordings in humans, combined with recently developed data processing tools and computational modelling, can provide insight into the cooperative behaviour of neurons, their average synaptic input and their spiking output, and can increase our understanding of how these processes contribute to the extracellular signal.
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            Magnetoencephalography—theory, instrumentation, and applications to noninvasive studies of the working human brain

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              Beta-band oscillations--signalling the status quo?

              In this review, we consider the potential functional role of beta-band oscillations, which at present is not yet well understood. We discuss evidence from recent studies on top-down mechanisms involved in cognitive processing, on the motor system and on the pathophysiology of movement disorders that suggest a unifying hypothesis: beta-band activity seems related to the maintenance of the current sensorimotor or cognitive state. We hypothesize that beta oscillations and/or coupling in the beta-band are expressed more strongly if the maintenance of the status quo is intended or predicted, than if a change is expected. Moreover, we suggest that pathological enhancement of beta-band activity is likely to result in an abnormal persistence of the status quo and a deterioration of flexible behavioural and cognitive control. (c) 2010 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Proc. Natl. Acad. Sci. U.S.A.
                Proceedings of the National Academy of Sciences of the United States of America
                Proceedings of the National Academy of Sciences
                1091-6490
                0027-8424
                Aug 16 2016
                : 113
                : 33
                Affiliations
                [1 ] Department of Neuroscience, Brown University, Providence, RI 02912; Department of Applied Mathematics, Brown University, Providence, RI 02912;
                [2 ] Department of Neuroscience, Brown University, Providence, RI 02912;
                [3 ] Cognitive Neuroscience and Schizophrenia Program, Nathan Kline Institute, Orangeburg, NY 10962; Department of Neurological Surgery, College of Physicians and Surgeons, Columbia University, New York, NY 10032;
                [4 ] Athinola A. Martinos Center, Massachusetts General Hospital, Boston, MA 02129; Department of Neuroscience and Biomedical Engineering, Aalto University School of Science, 02150 Espoo, Finland; Harvard Medical School, Boston, MA 02115.
                [5 ] Department of Neuroscience, Brown University, Providence, RI 02912; stephanie_jones@brown.edu.
                Article
                1604135113
                10.1073/pnas.1604135113
                4995995
                27469163

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