Driving Oscillatory Activity in the Human Cortex Enhances Motor Performance

Abstract

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 [1Engel A.K. Fries P. Beta-band oscillations—signalling the status quo?.Curr. Opin. Neurobiol. 2010; 20: 156-165Crossref PubMed Scopus (1605) Google Scholar]. 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 [2Gilbertson T. Lalo E. Doyle L. Di Lazzaro V. Cioni B. Brown P. Existing motor state is favored at the expense of new movement during 13-35 Hz oscillatory synchrony in the human corticospinal system.J. Neurosci. 2005; 25: 7771-7779Crossref PubMed Scopus (259) Google Scholar, 3Pogosyan A. Gaynor L.D. Eusebio A. Brown P. Boosting cortical activity at Beta-band frequencies slows movement in humans.Curr. Biol. 2009; 19: 1637-1641Abstract Full Text Full Text PDF PubMed Scopus (439) Google Scholar]. In contrast, activity in the gamma (60–90 Hz) band increases during movement [4Muthukumaraswamy S.D. Functional properties of human primary motor cortex gamma oscillations.J. Neurophysiol. 2010; 104: 2873-2885Crossref PubMed Scopus (182) Google Scholar]. 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 [5Gonzalez Andino S.L. Michel C.M. Thut G. Landis T. Grave de Peralta R. Prediction of response speed by anticipatory high-frequency (gamma band) oscillations in the human brain.Hum. Brain Mapp. 2005; 24: 50-58Crossref PubMed Scopus (118) Google Scholar]. 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.