Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI

Abstract

Transcranial magnetic stimulation (TMS) has been used to document some apparent interhemispheric influences behaviorally, with TMS over the right parietal cortex reported to enhance processing of touch for the ipsilateral right hand (Seyal et al., 1995). However, the neural bases of such apparent interhemispheric influences from TMS remain unknown. Here, we studied this directly by combining TMS with concurrent functional magnetic resonance imaging (fMRI). We applied bursts of 10 Hz TMS over right parietal cortex, at a high or low intensity, during two sensory contexts: either without any other stimulation, or while participants received median nerve stimulation to the right wrist, which projects to left primary somatosensory cortex (SI). TMS to right parietal cortex affected the blood oxygenation level-dependent signal in left SI, with high- versus low-intensity TMS increasing the left SI signal during right-wrist somatosensory input, but decreasing this in the absence of somatosensory input. This state-dependent modulation of SI by parietal TMS over the other hemisphere was accompanied by a related pattern of TMS-induced influences in the thalamus, as revealed by region-of-interest analyses. A behavioral experiment confirmed that the same right parietal TMS protocol of 10 Hz bursts led to enhanced detection of perithreshold electrical stimulation of the right median nerve, which is initially processed in left SI. Our results confirm directly that TMS over right parietal cortex can affect processing in left SI of the other hemisphere, with rivalrous effects (possibly transcallosal) arising in the absence of somatosensory input, but facilitatory effects (possibly involving thalamic circuitry) in the presence of driving somatosensory input.

Figure 1.

A–C, Main effect of the presence minus absence of right-hand somatosensory stimulation (electrical stimulation of the right median nerve) shows highly significant activations (p < 0.05, FWE corrected) in contralateral SI (the dorsal activation visible in A–C) and SII (ventral activation visible here in A only). The activations are projected onto coronal (A), sagittal (B), and transverse (C) slices of the averaged structural scans of all subjects.

Figure 2.

A–C, Areas showing an interaction between high- minus low-intensity right parietal TMS, and the presence minus absence of right median nerve sensory stimulation, within regions responding to right median nerve stimulation overall (compare Fig. 1). Significant (p < 0.05, FWE corrected) interaction effects are shown on coronal (A), sagittal (B), and transverse (C) slices of the averaged structural scans. The left SI is clearly implicated. D, Plot of the mean percentage of BOLD signal change extracted from the left SI cluster of the interaction contrast shown in A–C. High- versus low-intensity TMS over right parietal cortex increased the BOLD signal for left SI during right median nerve stimulation (compare third and fourth bars), but the same high TMS decreased the BOLD signal for left SI in the absence of somatosensory input (compare first and second bars). Restated, high-intensity right parietal TMS increased the differential response of left SI to the presence versus absence of right-hand stimulation (compare fourth and second bars in the histogram), compared with low-intensity TMS (compare third and first bars).

Figure 3.

VOI analysis of the thalamus, as defined by a cytoarchitechtonic postmortem atlas (see Materials and Methods). A–C, Statistical parametric maps for the interaction of TMS and median nerve stimulation within the thalamus (p < 0.05, FWE corrected for that volume of interest) overlaid onto the mean structural scan. D, E, Plots of the group mean percentage of BOLD signal change from the left (D) and right (E) thalamic clusters for each condition in the interaction of TMS intensity and right-wrist stimulation. BOLD signal in the thalamus was highest during combined right-hand somatosensory stimulation and high-intensity TMS over right parietal cortex (fourth bar in each histogram).