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      Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance

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          Summary

          Voluntary movement is accompanied by changes in the degree to which neurons in the brain synchronize their activity within discrete frequency ranges. Two patterns of movement-related oscillatory activity stand out in human cortical motor areas. Activity in the beta frequency (15–30 Hz) band is prominent during tonic contractions but is attenuated prior to and during voluntary movement [ 1]. Without such attenuation, movement may be slowed, leading to the suggestion that beta activity promotes postural and tonic contraction, possibly at a cost to the generation of new movements [ 2, 3]. In contrast, activity in the gamma (60–90 Hz) band increases during movement [ 4]. The direction of change suggests that gamma activity might facilitate motor processing. In correspondence with this, increased frontal gamma activity is related with reduced reaction times [ 5]. Yet the possibility remains that these functional correlations reflect an epiphenomenal rather than causal relationship. Here we provide strong evidence that oscillatory activities at the cortical level are mechanistically involved in determining motor behavior and can even improve performance. By driving cortical oscillations using noninvasive electrical stimulation, we show opposing effects at beta and gamma frequencies and interactions with motor task that reveal the potential quantitative importance of oscillations in motor behavior.

          Highlights

          ► Cortical driving at 20 and 70 Hz slows and speeds voluntary force generation ► Performance can be enhanced even during contractions made as fast as possible ► Scale of effects of cortical driving depend on the nature of the cued motor task

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          Most cited references11

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          Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG

          Non-invasive electrical stimulation of the human cortex by means of transcranial direct current stimulation (tDCS) has been instrumental in a number of important discoveries in the field of human cortical function and has become a well-established method for evaluating brain function in healthy human participants. Recently, transcranial alternating current stimulation (tACS) has been introduced to directly modulate the ongoing rhythmic brain activity by the application of oscillatory currents on the human scalp. Until now the efficiency of tACS in modulating rhythmic brain activity has been indicated only by inference from perceptual and behavioural consequences of electrical stimulation. No direct electrophysiological evidence of tACS has been reported. We delivered tACS over the occipital cortex of 10 healthy participants to entrain the neuronal oscillatory activity in their individual alpha frequency range and compared results with those from a separate group of participants receiving sham stimulation. The tACS but not the sham stimulation elevated the endogenous alpha power in parieto-central electrodes of the electroencephalogram. Additionally, in a network of spiking neurons, we simulated how tACS can be affected even after the end of stimulation. The results show that spike-timing-dependent plasticity (STDP) selectively modulates synapses depending on the resonance frequencies of the neural circuits that they belong to. Thus, tACS influences STDP which in turn results in aftereffects upon neural activity. The present findings are the first direct electrophysiological evidence of an interaction of tACS and ongoing oscillatory activity in the human cortex. The data demonstrate the ability of tACS to specifically modulate oscillatory brain activity and show its potential both at fostering knowledge on the functional significance of brain oscillations and for therapeutic application.
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            Natural frequencies of human corticothalamic circuits.

            The frequency tuning of a system can be directly determined by perturbing it and by observing the rate of the ensuing oscillations, the so called natural frequency. This approach is used, for example, in physics, in geology, and also when one tunes a musical instrument. In the present study, we employ transcranial magnetic stimulation (TMS) to directly perturb a set of selected corticothalamic modules (Brodmann areas 19, 7, and 6) and high-density electroencephalogram to measure their natural frequency. TMS consistently evoked dominant alpha-band oscillations (8-12 Hz) in the occipital cortex, beta-band oscillations (13-20 Hz) in the parietal cortex, and fast beta/gamma-band oscillations (21-50 Hz) in the frontal cortex. Each cortical area tended to preserve its own natural frequency also when indirectly engaged by TMS through brain connections and when stimulated at different intensities, indicating that the observed oscillations reflect local physiological mechanisms. These findings were reproducible across individuals and represent the first direct characterization of the coarse electrophysiological properties of three associative areas of the human cerebral cortex. Most importantly, they indicate that, in healthy subjects, each corticothalamic module is normally tuned to oscillate at a characteristic rate. The natural frequency can be directly measured in virtually any area of the cerebral cortex and may represent a straightforward and flexible way to probe the state of human thalamocortical circuits at the patient's bedside.
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              Boosting Cortical Activity at Beta-Band Frequencies Slows Movement in Humans

              Summary Neurons have a striking tendency to engage in oscillatory activities. One important type of oscillatory activity prevalent in the motor system occurs in the beta frequency band, at about 20 Hz. It is manifest during the maintenance of tonic contractions and is suppressed prior to and during voluntary movement [1–7]. This and other correlative evidence suggests that beta activity might promote tonic contraction, while impairing motor processing related to new movements [3, 8, 9]. Hence, bursts of beta activity in the cortex are associated with a strengthening of the motor effects of sensory feedback during tonic contraction and with reductions in the velocity of voluntary movements [9–11]. Moreover, beta activity is increased when movement has to be resisted or voluntarily suppressed [7, 12, 13]. Here we use imperceptible transcranial alternating-current stimulation to entrain cortical activity at 20 Hz in healthy subjects and show that this slows voluntary movement. The present findings are the first direct evidence of causality between any physiological oscillatory brain activity and concurrent motor behavior in the healthy human and help explain how the exaggerated beta activity found in Parkinson's disease can lead to motor slowing in this illness [14].
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                06 March 2012
                06 March 2012
                : 22
                : 5
                : 403-407
                Affiliations
                [1 ]Functional Neurosurgery and Experimental Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU, UK
                [2 ]Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, UK
                [3 ]Centre of Excellence in Personalised Healthcare, Institute of Biomedical Engineering, Department of Engineering Sciences, University of Oxford, Oxford OX3 7DQ, UK
                [4 ]Nuffield Department of Surgery, John Radcliffe Hospital, Oxford OX3 9DU, UK
                Author notes
                []Corresponding author peter.brown@ 123456clneuro.ox.ac.uk
                [5]

                These authors contributed equally to this work

                Article
                CURBIO9340
                10.1016/j.cub.2012.01.024
                3343257
                22305755
                30b8f056-e507-45d7-91dd-429f88bd8587
                © 2012 ELL & Excerpta Medica.

                This document may be redistributed and reused, subject to certain conditions.

                History
                : 27 October 2011
                : 5 December 2011
                : 11 January 2012
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                Life sciences
                Life sciences

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