Distributed functions of detection and discrimination of vibrotactile stimuli in the hierarchical human somatosensory system

Abstract

According to the hierarchical view of human somatosensory network, somatic sensory information is relayed from the thalamus to primary somatosensory cortex (S1), and then distributed to adjacent cortical regions to perform further perceptual and cognitive functions. Although a number of neuroimaging studies have examined neuronal activity correlated with tactile stimuli, comparatively less attention has been devoted toward understanding how vibrotactile stimulus information is processed in the hierarchical somatosensory cortical network. To explore the hierarchical perspective of tactile information processing, we studied two cases: (a) discrimination between the locations of finger stimulation; and (b) detection of stimulation against no stimulation on individual fingers, using both standard general linear model (GLM) and searchlight multi-voxel pattern analysis (MVPA) techniques. These two cases were studied on the same data set resulting from a passive vibrotactile stimulation experiment. Our results showed that vibrotactile stimulus locations on fingers could be discriminated from measurements of human functional magnetic resonance imaging (fMRI). In particular, it was in case (a) we observed activity in contralateral posterior parietal cortex (PPC) and supramarginal gyrus (SMG) but not in S1, while in case; (b) we found significant cortical activations in S1 but not in PPC and SMG. These discrepant observations suggest the functional specialization with regard to vibrotactile stimulus locations, especially, the hierarchical information processing in the human somatosensory cortical areas. Our findings moreover support the general understanding that S1 is the main sensory receptive area for the sense of touch, and adjacent cortical regions (i.e., PPC and SMG) are in charge of a higher level of processing and may thus contribute most for the successful classification between stimulated finger locations.

Keywords: fMRI; functional specialization; hierarchical tactile processing; somatosensory cortex; vibrotactile stimulation.

Figure 1

Brief sketch of the experimental design and the stimulation device. Each trial consisted of three periods: resting (30 s), stimulation (30 s), and response (9 s). No stimulation was applied during the resting period and 200 Hz of vibrotactile stimulation was applied on the one of three segments of each finger in a random order during the stimulation period. After the finger stimulation, participants were asked to press the button with their left hand if they perceived the stimulation regardless of the stimulus locations. Stimulated locations of each finger are depicted in the same color. Even though each finger was stimulated at three different sites, those were considered as the same finger locations in this study.

Figure 2

Summary of the analysis. (A) In the stimulated finger decoding analysis, searchlight MVPA found two significant clusters located in contralateral PPC and SMG. However, no significant cluster was found from univariate GLM approach. (B) In the contrast analysis of finger stimulation vs. no stimulation, significant clusters in contralateral S1 were observed except ring finger stimulation using searchlight MVPA. On the other hand, univariate GLM revealed the contralateral S1 activations in response to stimulation on the index and middle fingers.

Figure 3

Decoding accuracies of each significant cluster from searchlight MVPA. The rightmost value indicates the average decoding accuracy across all the participants. Error bars indicate standard errors and a chance level is marked by the dashed line (25%).

Figure 4

Decoding performance combining all the voxels of significant clusters. (A) Average decoding accuracies of ten participants from searchlight MVPA. The rightmost value indicates the average accuracy across all the participants. Error bars indicate standard errors and a chance level is marked by the dashed line (25%). (B) Confusion matrix for the stimulated finger decoding analysis. The rows of the matrix indicate the locations of vibrotactile stimulus provided to the participants (i.e., true label) and the columns of the matrix indicate the predictions by the decoder (i.e., predicted label). Each cell shows the percentage of correct prediction.

Figure 5

“Center of mass” coordinates of the each finger representation in MNI space within primary somatosensory cortical area (S1). The “center of mass” coordinates of individual participant are marked with small squares, and the averaged “center of mass” coordinates are marked with circles. Note that the text next to individual “center of mass” indicates its participant number.