The functional architecture of S1 during touch observation described with 7 T fMRI

Abstract

Recent studies indicate that the primary somatosensory cortex (S1) is active not only when touch is physically perceived but also when it is merely observed to be experienced by another person. This social responsivity of S1 has important implications for our understanding of S1 functioning. However, S1 activity during touch observation has not been characterized in great detail to date. We focused on two features of the S1 functional architecture during touch observation, namely the topographical arrangement of index and middle finger receptive fields (RFs), and their dynamic shrinkage during concurrent activation. Both features have important implications for human behavior. We conducted two fMRI studies at 7 T, one where touch was physically perceived, and one where touch was observed. In the two experiments, participants either had their index finger and/or middle finger stimulated using paintbrushes, or just observed similar touch events on video. Our data show that observing and physically experiencing touch elicits overlapping activity changes in S1. In addition, observing touch to the index finger or the middle finger alone evoked topographically arranged activation foci in S1. Importantly, when co-activated, the index and middle finger RFs not only shrank during physical touch perception, but also during touch observation. Our data, therefore, indicate a similarity between the functional architecture of S1 during touch observation and physical touch perception with respect to single-digit topography and RF shrinkage. These results may allow the tentative conclusion that even primary somatosensory experiences, such as physical touch perception, can be shared amongst individuals.

Fig. 1

Design and example trial of the observed touch experiment. a Example trial as shown to participants in the scanner. Each trial started with the same question (“Which paintbrush is rougher?”) followed by two video clips presented in direct succession that belonged to the same experimental condition, but showed two different paintbrush pairs for tactile stimulation; while seeing a question mark on the screen, participants then had to indicate via left-hand button-presses which of the two paintbrush pairs was rougher. Half of the participants responded with their left index finger when they thought the first paintbrush pair was rougher and with their left middle finger when they thought the second was rougher, the other half responded vice versa; the pause between two trials was 6 s in two-thirds of the trials and 20 s in one-third of the trials, and this was counterbalanced across conditions. b Participants saw either their own hand in the first person perspective or another person’s hand in the third person perspective on video; in the observed touch conditions, touch was applied to either the middle finger (MF), the index finger (IF), or to both fingers (BF) of the right hand; in the no-touch condition, the paintbrush pair stroked the white surface on which the hand was positioned

Fig. 2

Selected slices for functional imaging of one example subject. Shown is a sagittal slice of the anatomical MP2RAGE scan which was used to select 30 axial slices covering bilateral S1 on the basis of the individual subject’s brain anatomy (i.e., hand knob area)

Fig. 3

Suppressive interactions (SI) in contralateral S1 during physical touch perception (a) and touch observation (b). a Activity changes of contralateral S1 during physical touch applied to the index finger (IF) and the middle finger (MF); in addition, the suppressive interaction (SI) effect for physical touch is displayed using voxel-wise statistics in the upper panel (IF touch–rest + MF touch–rest − BF touch–rest), and using contrast estimates in the lower panel; the bar labeled “Expected activity” describes the added contrast estimates of physical touch to the IF and MF, whereas the bar labeled “Actual activity” describes the contrast estimates when both fingers were stimulated together; the bar graphs show mean contrast estimates ± standard deviation (SD) of all (N = 15) participants. b Activity changes of contralateral S1 during observed touch to the IF and MF; in addition, the SI effect for observed touch is displayed using voxel-wise statistics in the upper panel (obs. touch IF–no-touch + obs. touch MF–no-touch − obs. touch BF–no-touch), and using contrast estimates in the lower panel; the bar labeled “Expected activity” describes the added contrast estimates of touch observation to the IF and MF, whereas the bar labeled “Actual activity” describes the contrast estimates when touch to both fingers together was observed; the bar graphs show mean contrast estimates ± standard deviation (SD) of n = 10 participants (see “Suppressive interaction” for details on why not all participants were part of this analysis); functional images are masked with an anatomical mask covering contralateral S1 and are thresholded at p < 0.0005 (uncorrected) (a) and p < 0.001 (uncorrected) (b); the data are displayed on a normalized T1-image of an individual subject; Pre precentral gyrus, Post postcentral gyrus

Fig. 4

Overlap between activity changes during physical touch perception and touch observation in contralateral S1. Overlapping voxels between physical touch perception and touch observation are displayed in purple; overlaps are shown separately for the index finger (upper panel) and the middle finger (lower panel); functional images are masked with an anatomical mask covering contralateral S1 and thresholded at p < 0.001 (uncorrected); functional data are visualized on a normalized T1 image of an individual subject; Pre precentral gyrus, Post postcentral gyrus

Fig. 5

Receptive field (RF) topography of the index finger (IF) and middle finger (MF) in contralateral S1 during physical touch perception and touch observation. Shown are five axial slices ordered from inferior (z = 42) to superior (z = 47) of N = 15 participants; the borders of the MF RFs are indicated using blue lines; functional images are masked with an anatomical mask covering contralateral S1 and visualized at an individual’s normalized T1 image; to make both conditions better comparable, a slightly more conservative threshold was chosen for physical touch perception [p < 0.0001 (uncorrected)] than for touch observation [p < 0.001 (uncorrected)]

Fig. 6

Contralateral S1 activity during physical touch perception and touch observation of n = 5 individual subjects. The left side of the figure shows functional data of physical touch to the index finger (IF), the middle finger (MF), and the suppressive interaction (SI) effect for physical touch; the right side of the figure shows functional data of observed touch to the IF, the MF, and the SI effect for observed touch; note that the same axial and coronal slices of the same subjects can here be visually compared; functional data are presented at the individual’s normalized T1-anatomical scans; to make both conditions better comparable, a slightly more conservative threshold was chosen for physical touch perception [p < 0.001 (uncorrected)] than for touch observation [p < 0.005 (uncorrected)]