Multiple time courses of somatosensory responses in human cortex

Abstract

Here we show how anatomical and functional data recorded from patients undergoing stereo-EEG can be used to decompose the cortical processing following nerve stimulation in different stages characterized by specific topography and time course. Tibial, median and trigeminal nerves were stimulated in 96 patients, and the increase in gamma power was evaluated over 11878 cortical sites. All three nerve datasets exhibited similar clusters of time courses: phasic, delayed/prolonged and tonic, which differed in topography, temporal organization and degree of spatial overlap. Strong phasic responses of the three nerves followed the classical somatotopic organization of SI, with no overlap in either time or space. Delayed responses presented overlaps between pairs of body parts in both time and space, and were confined to the dorsal motor cortices. Finally, tonic responses occurred in the perisylvian region including posterior insular cortex and were evoked by the stimulation of all three nerves, lacking any spatial and temporal specificity. These data indicate that the somatosensory processing following nerve stimulation is a multi-stage hierarchical process common to all three nerves, with the different stages likely subserving different functions. While phasic responses represent the neural basis of tactile perception, multi-nerve tonic responses may represent the neural signature of processes sustaining the capacity to become aware of tactile stimuli.

Keywords: Cerebral cortex; Electrical stimulation; Human; Peripheral nerves; Stereo EEG; Touch.

Fig. 1

Overall Responsiveness maps for tibial nerve stimulation. Overall responsiveness (responsive leads as a percent of total explored leads per disc) maps for left (A) and right (B) hemispheres. Only surface nodes with values exceeding 10% are shown. Panels C and D show the same datasets, respectively, but shown from a medial perspective onto the inflated hemispheres, allowing to appreciate the continuity of maps in the mesial regions without the cuts inherent to the flat maps. White borders refer to cytoarchitectonic areas of sensorimotor regions (Geyer et al., 1999, Geyer et al., 2000, Grefkes et al., 2001), superior and inferior parietal cortex (Scheperjans et al., 2008a, Scheperjans et al., 2008b, Caspers et al., 2006, Caspers et al., 2008, Choi et al., 2006), parietal operculum (Eickhoff et al., 2006), and areas 44 and 45 (Amunts et al., 1999). The subdivision between dorsal and ventral premotor areas was defined according to Tomassini et al. (2007). The separation between mesial and dorsal premotor cortices (PMm and PMd) follows the crown of the hemisphere. In addition, long and short gyri of insula were anatomically defined using the gyral pattern. Black hatchings indicate under-sampled regions.

Fig. 2

Overall Responsiveness maps for trigeminal nerve stimulation. Overall responsiveness (responsive leads as a percent of total explored leads per disc) maps for left (A) and right (B) hemispheres. Only surface nodes with values exceeding 10% are shown. Same conventions as in Fig. 1. LgI: long insular gyri. White hatchings indicate under-sampled regions.

Fig. 3

Overall somatotopic organization. Overall responsiveness to the three nerve stimulations are superimposed on the same map for left (panel A) and right (panel B) hemisphere by using the three components of the RGB color map. Tibial responses are rendered by the intensity of the green palette, median responses in red and trigeminal in blue. Yellow regions correspond to overlap of hand and foot representations, purple regions indicate joint hand and mouth representations. Finally, cortical areas responsive to all three stimulations are colored white. Only surface nodes with values exceeding 10% are shown. Same conventions as in Fig. 1. Refer to Fig. S1 for the full description of cytoarchitectonic boundaries.

Fig. 4

Clustering of time courses. Results of clustering on gamma power time course are shown for all the three datasets (tibial in panel A, median in B, trigeminal in C). All curves (color code, see inset) represent the cluster centroid ± standard deviation. The time window is limited to [-20; 300] ms relative to the stimulus delivery.

Fig. 5

Strong phasic cluster maps. A & C: relative responsiveness (leads belonging to one cluster as a percentage of total number of responsive leads per disc) maps of left (A) and right (C) hemispheres for strong phasic cluster. Color code as in Fig. 3. Only nodes with values exceeding the chance level (20% with 5 clusters, 16.6% with 6 clusters) are shown. Same anatomical conventions as in Fig. 1. B: cluster centroids for the three datasets, with all curves in grey except the strong phasic ones, colored code as in the maps. Black hatchings indicate under-sampled regions.

Fig. 6

Delayed/prolonged cluster maps. A & C: relative responsiveness (leads belonging to one cluster as a percentage of total number of responsive leads per disc) maps of left (A) and right (C) hemispheres for delayed/prolonged cluster. Color code as in Fig. 3. Only nodes with values exceeding the chance level (20% with 5 clusters, 16.6% with 6 clusters) are shown. Same anatomical conventions as in Fig. 1. B: cluster centroids for the three datasets, with all curves in grey except the delayed/prolonged ones, colored code as in the maps. PMd: dorsal premotor cortex.

Fig. 7

Tonic cluster. A & C: relative responsiveness (leads belonging to one cluster as a percentage of total number of responsive leads per disc) maps of left (A) and right (C) hemispheres for tonic cluster. Color code as in Fig. 3. Only nodes with values exceeding the chance level (20% with 5 clusters, 16.6% with 6 clusters) are shown. Same anatomical conventions as in Fig. 1. B: cluster centroids for the three datasets, with all curves in grey except the tonic ones, colored code as in the maps. SgI and LgI: short and long insular gyri, respectively.