Audio-Tactile and Peripersonal Space Processing Around the Trunk in Human Parietal and Temporal Cortex: An Intracranial EEG Study

Abstract

Interactions with the environment happen within one's peripersonal space (PPS)-the space surrounding the body. Studies in monkeys and humans have highlighted a multisensory distributed cortical network representing the PPS. However, knowledge about the temporal dynamics of PPS processing around the trunk is lacking. Here, we recorded intracranial electroencephalography (iEEG) in humans while administering tactile stimulation (T), approaching auditory stimuli (A), and the 2 combined (AT). To map PPS, tactile stimulation was delivered when the sound was far, intermediate, or close to the body. The 19% of the electrodes showed AT multisensory integration. Among those, 30% showed a PPS effect, a modulation of the response as a function of the distance between the sound and body. AT multisensory integration and PPS effects had similar spatiotemporal characteristics, with an early response (~50 ms) in the insular cortex, and later responses (~200 ms) in precentral and postcentral gyri. Superior temporal cortex showed a different response pattern with AT multisensory integration at ~100 ms without a PPS effect. These results, represent the first iEEG delineation of PPS processing in humans and show that PPS and multisensory integration happen at similar neural sites and time periods, suggesting that PPS representation is based on a spatial modulation of multisensory integration.

Figure 1.

Locations of all recording sites in 3D MNI space. MNI coordinates of electrodes from all 6 patients (500 electrodes in total) plotted on the Colin27 MRI template (on selected sagittal and axial planes). Note that locations are in 3D MNI space, and not located on the surface of MRI slice shown (thus, recording sites behind the depicted MRI slice are marked with faded color). In black, the implanted electrodes not showing a response (vs. baseline, cluster-corrected) to stimuli, in orange, the electrodes showing a response to audio stimuli only, in yellow, the electrodes showing a response to tactile stimuli only, in red, the electrodes showing a response to audio-tactile stimuli, and in white the electrodes showing a response to at least 2 conditions.

Figure 2.

Locations of electrodes showing an AT multisensory integration and peripersonal space (PPS) effect, in 3D MNI space. MNI coordinates of electrodes from all 6 patients, electrodes showing specifically a significant multisensory integration profile are highlighted in black (20 electrodes, see Table 1 for the position), electrodes showing both an AT multisensory integration and PPS effect are highlighted in white (6 electrodes, see Table 2 for electrodes positions). Note that locations are in 3D MNI space, and not located on the surface of selected MRI slice (thus, recording sites behind the depicted MRI slice are marked with faded color).

Figure 3.

Exemplar LFP for AT multisensory integration. The left panel shows the position of the electrode (in white), on a selected plane. The electrode was located in the postcentral gyrus (PCG). The middle panel shows the LFPs responses for 3 conditions: A (orange), T (yellow) and AT (red). The right panel shows the LFPs for the AT (red) and the SUM of A + T (green), with a multisensory integration at 148–253 ms after the stimulus onset. The lines indicate the average over trials; the shaded areas indicate the 95% CI, and the black lines indicate the time period with a significant AT multisensory integration (P-value <0.05, cluster-corrected).

Figure 4.

Exemplar LFP for AT multisensory integration and PPS effect. The top left panel shows the position of the electrode, on a selected plane. The electrode was located in the parahippocampal gyrus (PHG). The top right panel shows the LFPs responses for 3 conditions: A (orange), T (yellow) and AT (red). The bottom left panel shows the LFPs for the AT (red) and the SUM of A + T (green), with a multisensory integration at 52–170 ms and 193–270 ms after stimulus onset. The bottom right panel shows the LFPs for the PPS effect at 151–298 ms after stimulus onset. The bottom right. The lines indicate the average over trials; the shaded areas indicate the 95% CI, and the black lines indicate the time period with a significant PPS effect (P-value <0.05, cluster-corrected).