Human primary somatosensory cortex is differentially involved in vibrotaction and nociception

Abstract

The role of the primary somatosensory cortex (S1) in vibrotaction is well established. In contrast, its involvement in nociception is still debated. Here we test whether S1 is similarly involved in the processing of nonnociceptive and nociceptive somatosensory input in humans by comparing the aftereffects of high-definition transcranial direct current stimulation (HD-tDCS) of S1 on the event-related potentials (ERPs) elicited by nonnociceptive and nociceptive somatosensory stimuli delivered to the ipsilateral and contralateral hands. Cathodal HD-tDCS significantly affected the responses to nonnociceptive somatosensory stimuli delivered to the contralateral hand: both early-latency ERPs from within S1 (N20 wave elicited by transcutaneous electrical stimulation of median nerve) and late-latency ERPs elicited outside S1 (N120 wave elicited by short-lasting mechanical vibrations delivered to index fingertip, thought to originate from bilateral operculo-insular and cingulate cortices). These results support the notion that S1 constitutes an obligatory relay for the cortical processing of nonnociceptive tactile input originating from the contralateral hemibody. Contrasting with this asymmetric effect of HD-tDCS on the responses to nonnociceptive somatosensory input, HD-tDCS over the sensorimotor cortex led to a bilateral and symmetric reduction of the magnitude of the N240 wave of nociceptive laser-evoked potentials elicited by stimulation of the hand dorsum. Taken together, our results demonstrate in humans a differential involvement of S1 in vibrotaction and nociception.NEW & NOTEWORTHY Whereas the role of the primary somatosensory cortex (S1) in vibrotaction is well established, its involvement in nociception remains strongly debated. By assessing, in healthy volunteers, the effect of high-definition transcranial direct current stimulation over S1, we demonstrate a differential involvement of S1 in vibrotaction and nociception.

Keywords: evoked potentials; nociception; primary somatosensory cortex; touch; transcranial direct current stimulation.

Fig. 1.

In 2 separate groups, we assessed the effects of 20 min of HD-tDCS vs. sham HD-tDCS over the sensorimotor cortex on the perception and ERPs elicited by nonnociceptive and nociceptive stimuli delivered to the ipsilateral and contralateral hands. The 2 experiments consisted of 2 EEG recording sessions, immediately before and immediately after 20 min of real HD-tDCS (HD-tDCS experiment) or sham HD-tDCS (sham experiment) of the left or right sensorimotor cortex. During each EEG session, ERPs elicited by nonnociceptive and nociceptive stimuli delivered to the ipsilateral and contralateral hands were recorded. Nonnociceptive stimuli were transcutaneous electrical stimuli delivered to the median nerve at the level of the wrist and vibrotactile stimuli delivered to the index fingertip. Nociceptive heat stimuli were laser pulses delivered to the hand dorsum. The second recording session always began within 5 min after the end of HD-tDCS or sham stimulation and was completed within 25 min.

Fig. 2.

Nonnociceptive and nociceptive somatosensory ERPs recorded before and after real HD-tDCS (HD-tDCS experiment, left) and sham HD-tDCS (sham experiment, right) of the left or right sensorimotor cortex (group-level average waveforms). The N120 and P250 waves elicited by vibrotactile stimulation and the N240 and P350 waves elicited by laser stimulation of the ipsilateral and contralateral hand are shown at Cz vs. M1M2. The N20 waves elicited by transcutaneous electrical stimulation of the median nerve are shown at the contralateral parietal electrode (Pc: P3 or P4) vs. Fz. The N160 wave elicited by laser stimulation is shown at the contralateral central electrode (Cc: C3 or C4) vs. Fz. Head plots show the scalp topographies of the different components of nonnociceptive and nociceptive ERPs recorded before (blue frames) and after (red frames) HD-tDCS or sham stimulation. Note the marked reduction of the N120 wave elicited by tactile stimulation of the contralateral hand in the HD-tDCS experiment, the reduction of amplitude and increase of latency of the N20 wave elicited by electrical stimulation of the contralateral median nerve, and the absence of such changes in the sham experiment. Also note the symmetric reduction of the N240 wave in the HD-tDCS experiment and the lack of such a reduction in the sham experiment.

Fig. 3.

A: high-frequency oscillations (HFOs) elicited by nonnociceptive electrical stimulation of the median nerve can be separated into an early component (−5 to 0 ms relative to the latency of the N20 wave) and a late component (0 to +8 ms relative to the latency of the N20 wave). Dashed line represents the EEG signal band-pass filtered with a 400- to 1,000-Hz Butterworth zero-phase filter; solid line represents its Hilbert transform (average waveform from 1 recording performed in 1 subject while stimulating the right hand; contralateral central-parietal electrode CP5 vs. Fz). An estimate of the magnitude of early and late HFOs components was computed by calculating the area under the curve of the Hilbert transform, from −5 to 0 ms (early subcomponent) and from 0 to +8 ms (late subcomponent). B: scalp topography of the maximum peak amplitude of HFOs averaged across all participants and all conditions. The amplitude of HFOs was maximal at the contralateral central-parietal electrode (CP5 or CP6 vs. Fz). C: magnitudes of early and late components of HFOs in the HD-tDCS experiment and the sham experiment. Scatterplots represent for each subject the change in amplitude of the responses elicited by stimulation of the contralateral and ipsilateral hands, after vs. before treatment. Box plots show group-level average ± SD. Note in the HD-tDCS experiment as compared with the sham experiment the increase in magnitude of late-latency HFOs most evident when stimulating the contralateral hand.

Fig. 4.

Effect of real HD-tDCS (HD-tDCS experiment) and sham HD-tDCS (sham experiment) on the intensity of the perception elicited by nonnociceptive vibrotactile and nociceptive laser stimuli delivered to the contralateral and ipsilateral hands. Scatterplots represent for each subject the average % change in percept before vs. after HD-tDCS or sham stimulation. Box plots show the group-level average ± SD. Note the bilateral reduction of the perception elicited by nociceptive laser stimulation, which is most pronounced after real HD-tDCS.

Fig. 5.

Single-subject and group-level average change in the magnitude of nonnociceptive (N20, N120, P250) and nociceptive (N160, N240, P350) ERPs before vs. after real HD-tDCS (HD-tDCS experiment) and sham HD-tDCS (sham experiment). Black connected lines show the single-subject differences in amplitude (after − before HD-tDCS or sham stimulation) of the responses elicited by stimulation of the ipsilateral and contralateral hands. Box plots show the group-level average ± SD. Note in the HD-tDCS experiment the asymmetric reduction of the N20 and N120 waves elicited by nonnociceptive stimulation of the contralateral hand and the symmetric reduction of the N160 and N240 waves elicited by nociceptive stimulation of the contralateral and ipsilateral hands.