State-dependent effects of transcranial oscillatory currents on the motor system: what you think matters

Abstract

Imperceptible transcranial alternating current stimulation (tACS) changes the endogenous cortical oscillatory activity in a frequency-specific manner. In the human motor system, tACS coincident with the idling beta rhythm of the quiescent motor cortex increased the corticospinal output. We reasoned that changing the initial state of the brain (i.e., from quiescence to a motor imagery task that desynchronizes the local beta rhythm) might also change the susceptibility of the corticospinal system to resonance effects induced by beta-tACS. We tested this hypothesis by delivering tACS at different frequencies (theta, alpha, beta, and gamma) on the primary motor cortex at rest and during motor imagery. Motor-evoked potentials (MEPs) were obtained by transcranial magnetic stimulation (TMS) on the primary motor cortex with an online-navigated TMS-tACS setting. During motor imagery, the increase of corticospinal excitability was maximal with theta-tACS, likely reflecting a reinforcement of working memory processes required to mentally process and "execute" the cognitive task. As expected, the maximal MEPs increase with subjects at rest was instead obtained with beta-tACS, substantiating previous evidence. This dissociation provides new evidence of state and frequency dependency of tACS effects on the motor system and helps discern the functional role of different oscillatory frequencies of this brain region. These findings may be relevant for rehabilitative neuromodulatory interventions.

Figures

Figure 1.

a, Experimental design, with the 14 pseudorandom conditions during rest (red) and MI (green) of a pinch-grip action. b, Red (“target”) electrodes are placed on the scalp overlying the left motor cortex and the right PC (P4 position of the International 10–20 EEG System). The blue (“reference”) electrode is placed on the midline corresponding to the Pz position of the International 10–20 EEG System. The coil for TMS is positioned over the “active” electrode on the motor cortex. The stereotaxic navigation system allowed to keep constant the coil positioning throughout the experiment, by using a three-dimensional online feedback.

Figure 2.

Changes of corticospinal reactivity (indexed by MEP size) in response to ongoing tACS at different frequencies, during rest (white bars) or MI (black bars). Error bars represent SEM. *p < 0.05, **p < 0.01. a represents the effects of both MEP modulating factors (stimulation and MI). Note the consistent increase of MEP size during MI versus the quiescence state, regardless of the type of tACS applied (MI vs resting for no-tACS, θ-tACS, α-tACS, γ-tACS, PC, p < 0.001; and for β-tACS, p = 0.002). b represents a zoom-in into the effects of the different tACS frequencies, after removing the average facilitatory main effect of MI [amplitude values are expressed both as log (left y-axis) and raw microvolt scale (left y-axis)]. Note the dissociation between conditions of θ-tACS (5 Hz) and β-tACS (20 Hz) (see bar graph within the 2 rectangles), which highlights the state dependency of tACS effects: the corticospinal facilitation induced by MI, which was maximal during θ-tACS, was lost during β-tACS; a reversal pattern was observed when subjects were at rest.