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. 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. In contrast, activity in the gamma (60-90 Hz) band increases during movement. 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. 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.

Figure 1

Schematic of Paradigm Used for Go/No-Go Task A fixation cross is presented that triggers the onset of sinusoidal stimulation shown below. After 3 s, a square white precue was presented followed quickly (250–750 ms, randomized) by either a square green go cue or red no-go cue, which lasted 250 ms. Subjects were instructed to squeeze as quickly and as hard as they could in response to the go cue and withhold their response on no-go cues. Stimulation had a 0.5 s ramp up and down and lasted for a total of 5 s, which meant that it continued throughout the behavioral response and faded away shortly thereafter. There was then a 6 s delay between the response cue and subsequent fixation cross for the next trial, during which the subject was at rest.

Figure 2

Effect of Stimulation on Go Trials (A–D) In (A) and (B), stimulation is applied at 20 Hz and in (C) and (D) at 70 Hz. Black traces show no-stimulation trials and red traces stimulation trials. Traces are grand averages of all subjects' force rates aligned to the point of first development of 5% peak force rate (A and C) or peak rate of force generation (B and D). Vertical gray bars demonstrate areas of significant difference between stimulation and no stimulation (serial two-tailed paired t tests, p < 0.05). (E–G) The mean differences with confidence intervals of ±2 SEM between stimulation and no-stimulation conditions for 20 Hz (blue) and 70 Hz (red), aligned as above. Vertical lines at time 0 represent the point of first development of 5% peak force rate (E) and point of peak force rate (F). In (G), percent changes for each subject are shown for both initial rate and peak rate, for 20 Hz (blue) and 70 Hz (red) stimulation. Adjacent to individual changes are mean changes with ±2 SEM. See also Figure S1 for example of individual traces.

Figure 3

Effect of Stimulation on No-Go Trials Grand averages for no-go trials aligned to peak force are displayed for 20 Hz (A) and 70 Hz (B), with the gray bar showing an extended period of significant suppression for 20 Hz but not 70 Hz. Individual percent changes are shown in (C) for 20 Hz (blue) and 70 Hz (red) for peak force and peak rate of force generation along with means ±2 SEM (displayed with two outliers not shown from gamma peak force, and one from gamma peak velocity. Outliers are shown in Figure S1). See also Figure S1 for example of individual traces.

Figure 4

Correlation and 95% Confidence Intervals between Go and No-Go Trials with 20 Hz Stimulation Percent change in peak force rate is significantly correlated between go and no-go trials, suggesting a common inhibitory effect of 20 Hz stimulation (r = 0.728, p = 0.0032; n = 14 as errors of commission were absent in no-go trials in four of the 18 subjects).