State-Dependent Effects of Transcranial Oscillatory Currents on the Motor System during Action Observation

Abstract

We applied transcranial alternating current stimulation (tACS) to the primary motor cortex (M1) at different frequencies during an index-thumb pinch-grip observation task. To estimate changes in the corticospinal output, we used the size of motor evoked potentials (MEPs) obtained by transcranial magnetic stimulation (TMS) of M1 using an online MRI-guided simultaneous TMS-tACS approach. The results of the beta-tACS confirm a non-selective increase in corticospinal excitability in subjects at rest; an increase was observed for both of the tested hand muscles, the first dorsal interosseous (FDI) and the abductor digiti minimi (ADM). However, during action observation of the pinch-grip movement, the increase of corticospinal excitability was only observed for the prime mover FDI muscle and took place during alpha-tACS, while gamma-tACS affected both the FDI and control muscle (ADM) responses. These phenomena likely reflect the hypothesis that the mu and gamma rhythms specifically index the downstream modulation of primary sensorimotor areas by engaging mirror neuron activity. The current neuromodulation approach confirms that tACS can be used to induce neurophysiologically detectable state-dependent enhancement effects, even in complex motor-cognitive tasks.

Figure 1

Experimental design. (a) Combined TMS-tACS approach: the TMS coil is placed over the target tACS electrode on the M1 area. The reference tACS electrode is placed over the ipsilateral shoulder. The subject’s task is to observe either a steady hand or a pinch-grip action. (b) Top view of the design: the actor’s body is hidden by white curtains which are placed to the right of the subject so that the subject observes only the hand movement. (c) EMG montage: g–AgCl adhesive electrodes placed on the belly of the right FDI and ADM muscles.

Figure 2

Results. Percentage changes versus baseline MEP amplitude values (raw data) obtained under different experimental conditions. Error bars represent SEM. Asterisks denote significant effects (*p < 0.05, **p < 0.01). Note the frequency- and state-dependent effects of tACS: (a) The effects on the FDI muscle: tACS delivered at β range (20 Hz) on the M1 increases the corticospinal output versus most of the other conditions at rest; α-tACS and γ–tACS increases the AO effect. (b) The effects on the ADM muscle: tACS delivered at β range (20 Hz) on the M1 still increases the corticospinal output versus sham and γ stimulation at rest, while γ–tACS increases the AO effect versus β and sham stimulation during the AO task.

Figure 3

Scheme depicting tACS effects. Red dots represent effects on the FDI muscle while blue dots represent effects on the ADM. Note that the effects of tACS are not only frequency- and state-dependent but also muscle specific.