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. 2016 Aug 17;36(33):8726-33.
doi: 10.1523/JNEUROSCI.0868-16.2016.

Independent Causal Contributions of Alpha- And Beta-Band Oscillations During Movement Selection

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Free PMC article

Independent Causal Contributions of Alpha- And Beta-Band Oscillations During Movement Selection

Loek Brinkman et al. J Neurosci. .
Free PMC article

Abstract

To select a movement, specific neuronal populations controlling particular features of that movement need to be activated, whereas other populations are downregulated. The selective (dis)inhibition of cortical sensorimotor populations is governed by rhythmic neural activity in the alpha (8-12 Hz) and beta (15-25 Hz) frequency range. However, it is unclear whether and how these rhythms contribute independently to motor behavior. Building on a recent dissociation of the sensorimotor alpha- and beta-band rhythms, we test the hypothesis that the beta-band rhythm governs the disinhibition of task-relevant neuronal populations, whereas the alpha-band rhythm suppresses neurons that may interfere with task performance. Cortical alpha- and beta-band rhythms were manipulated with transcranial alternating current stimulation (tACS) while human participants selected how to grasp an object. Stimulation was applied at either 10 or 20 Hz and was imposed on the sensorimotor cortex contralaterally or ipsilaterally to the grasping hand. In line with task-induced changes in endogenous spectral power, the effect of the tACS intervention depended on the frequency and site of stimulation. Whereas tACS stimulation generally increased movement selection times, 10 Hz stimulation led to relatively faster selection times when applied to the hemisphere ipsilateral to the grasping hand, compared with other stimulation conditions. These effects occurred selectively when multiple movements were considered. These observations functionally differentiate the causal contribution of alpha- and beta-band oscillations to movement selection. The findings suggest that sensorimotor beta-band rhythms disinhibit task-relevant populations, whereas alpha-band rhythms inhibit neuronal populations that could interfere with movement selection.

Significance statement: This study shows dissociable effects of 10 Hz and 20 Hz tACS on the duration of movement selection. These observations have two elements of general relevance. First, the finding that alpha- and beta-band oscillations contribute independently to movement selection provides insight in how oscillations orchestrate motor behavior, which is key to understand movement selection deficits in neurodegenerative disorders. Second, the findings highlight the potential of 10 Hz stimulation as a neurophysiologically grounded intervention to enhance human performance. In particular, this intervention can potentially be exploited to boost rehabilitation after neural damage by targeting the unaffected hemisphere.

Keywords: alpha beta oscillations; motor imagery; movement selection; noninvasive brain stimulation; sensorimotor.

Figures

Figure 1.
Figure 1.
Experimental design and task performance. A, Participants were asked to imagine grasping the middle third of a tilted black-white cylinder (“stimulus”), which could be in 1 of 15 different orientations. As soon as they selected the movement, they indicated with a verbal response (“black” or “white”) whether their thumb was on the cylinder's black or white part. ITI, Intertrial interval. B, While participants selected how to grasp the tilted cylinder, oscillations in the sensorimotor cortex ipsilateral or contralateral to the grasping hand were independently modulated with short blocks (∼1 min) of tACS at either alpha (10 Hz) or beta (20 Hz) frequency. Stimulation was only applied during right hand trials to allow for wash-out of aftereffects of the intervention. There were also right hand trials that did not involve stimulation (“no stim”), which were used for comparison with the stimulation conditions. C, Percentage of trials in which participants reported to have imagined grasping the cylinder with their thumb on the white part, as a function of cylinder orientation, plotted separately for trials involving the left and the right hand. Dotted/dashed segments of the performance curves indicate cylinder orientations that afforded a single grasping configuration (e.g., 135 degrees for right hand trials, low-demand regime) or multiple grasping configurations (e.g., 45 degrees for right hand trials, high-demand regime), respectively. Error bars indicate ± 1 SE. For the line plots, data points were interpolated every 12 degrees and smoothed over 3 consecutive orientations. It can be seen that the preferred manner in which the cylinder was grasped depended on its orientation and followed the biomechanical constraints of the body. D, Duration of action selection (z-scores) as a function of cylinder orientation, plotted separately for trials involving the left and the right hand (all trials). Movement selection took 990 ± 390 ms (left hand; mean ± SE) and 975 ± 400 ms (right hand). Movement selection took longer (110 ± 20 ms, left hand; 105 ± 20 ms, right hand) when the cylinder afforded two different grasping configurations (high-demand trials) than when the cylinder could be grasped in a single manner (low-demand trials). The lines of individual subjects have been realigned based on the individual high demand orientations, before averaging. Other conventions as in C.
Figure 2.
Figure 2.
Effects of tACS on action selection duration. A, B, The four bars represent the effects of tACS on the duration of selecting an action (relative to no tACS, in z-scores) for the different stimulation conditions: stimulation of the contralateral (pink) or ipsilateral (blue) sensorimotor cortex at either alpha (10 Hz) or beta frequency (20 Hz), for high- and low- demand trials. During high-demand trials, action selection was faster when the sensorimotor cortex ipsilateral to the grasping hand was stimulated at 10 Hz. Asterisks indicate the significant post hoc paired-sample t tests (alpha-ipsilateral vs alpha-contralateral, t(32) = 2.2, p < 0.05; alpha-ipsilateral vs beta-ipsilateral, t(32) = 2.8, p < 0.01). C, D, Changes in oscillatory power relative to a prestimulus baseline period recorded using MEG (Brinkman et al., 2014) in an independent group of participants performing the same task with a delayed manual response (same conventions as in A, B).
Figure 3.
Figure 3.
Online and offline effects of tACS on action selection duration. A, B, Duration of action selection (z-scores) as a function of cylinder orientation for trials involving the right hand. Curves represent action selection duration during trials involving tACS to either the contralateral (pink) or the ipsilateral (blue) sensorimotor cortex, at 10 Hz (bold lines), 20 Hz (light lines), or without stimulation (dotted lines). Other conventions as in Figure 1D. It can be seen that the tACS intervention did not alter the dependency of action selection on biomechanical constraints, an indication that the faster response times following 10 Hz stimulation over the ipsilateral sensorimotor cortex during high-demand trials did not arise from a strategic shift toward the selection of a stereotypical grasping configuration. C, D, Same conventions as above, for trials involving the left hand, when no stimulation was applied. These curves were sorted according to the stimulation condition occurring in the preceding block, involving the right hand (see Fig. 1). This sorting procedure was applied to investigate potential offline effects induced by the tACS intervention. It can be seen that trials following tACS epochs had slower responses than trials following no-stimulation epochs (main effect of stimulation: F(1,32) = 15.0, p < 0.0005), but these effects did not depend on the frequency or the site of stimulation, or on task demand.

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