Frequency-dependent tuning of the human motor system induced by transcranial oscillatory potentials

Abstract

Different corticothalamic brain modules intrinsically oscillate at a "natural frequency" in a topographically organized manner. In "quiescent" human sensorimotor regions, the main detectable oscillatory activity peaks at ∼20 Hz, and partly contributes to determine the state of corticospinal excitability. Here, we showed that the transcranial application of an imperceptible, short-lasting (90 s) electric field oscillating at a physiological range increases corticospinal excitability online, with well defined frequency dependence and regional specificity. Indeed, the size of motor evoked potentials (MEPs) induced by navigated single-pulse TMS over the motor cortex significantly increased only during the local application of transcranial alternating current stimulation (tACS) at 20 Hz (β range). Other tACS frequencies (5, 10, and 40 Hz) applied on the motor cortex did not impact MEPs' size. Moreover, tACS applied on a control site (parietal cortex) and on a peripheral site (ulnar nerve) also failed to modulate MEPs. These results help clarifying the functional significance of the 20 Hz idling β rhythm of sensorimotor regions and suggest potential clinical applications of this approach.

Figure 1.

Experimental design. a, Red (“target”) electrodes are placed on the scalp overlying the left motor cortex and the right parietal cortex (P4 position of the 10-20 International EEG System). The blue (“reference”) electrode is placed on the midline corresponding to the PZ position of the 10–20 International EEG System. b, Navigation of TMS. The coil is held on the sponge electrodes placed over the left motor cortex. The colored triangles indicate the online feedback of the coil displacement from the exact target, with a tolerance of 2 mm (yellow: horizontal plane; red: vertical plane; blue: tangential plane). When the coil is replaced in the same position, colors disappear.

Figure 2.

Results of the main experiment. a, Average MEP amplitude (±SE) values (raw data) obtained through different experimental conditions. Note that only tACS delivered at β range (20 Hz) on the motor cortex increases the corticospinal output versus all the other conditions (baseline, 5 Hz, 10 Hz, 40 Hz, and 20 Hz on the parietal cortex). An asterisk (*) indicates a significant difference of 20 Hz stimulation with respect to all the other conditions. Statistics refer to log-transformed amplitude data (see Results). b, Percentage changes versus baseline of MEP amplitude values (raw data).

Figure 3.

Results of the control peripheral experiment. The three columns indicate the average amplitude (±SE) values (raw data) of the CMAPs obtained by TMS on the ulnar nerve at the elbow during local tACS at 20 Hz and at 5 Hz versus baseline (i.e., no tACS). No changes are observed. Results of statistical tests, performed with log-transformed amplitude data, are in the Results section.