Development of brain mechanisms for processing affective touch

Abstract

Affective tactile stimulation plays a key role in the maturation of neural circuits, but the development of brain mechanisms processing touch is poorly understood. We therefore used functional magnetic resonance imaging (fMRI) to study brain responses to soft brush stroking of both glabrous (palm) and hairy (forearm) skin in healthy children (5-13 years), adolescents (14-17 years), and adults (25-35 years). Adult-defined regions-of-interests in the primary somatosensory cortex (SI), secondary somatosensory cortex (SII), insular cortex and right posterior superior temporal sulcus (pSTS) were significantly and similarly activated in all age groups. Whole-brain analyses revealed that responses in the ipsilateral SII were positively correlated with age in both genders, and that responses in bilateral regions near the pSTS correlated significantly and strongly with age in females but not in males. These results suggest that brain mechanisms associated with both sensory-discriminative and affective-motivational aspects of touch are largely established in school-aged children, and that there is a general continuing maturation of SII and a female-specific increase in pSTS sensitivity with age. Our work establishes a groundwork for future comparative studies of tactile processing in developmental disorders characterized by disrupted social perception such as autism.

Keywords: brain; children; development; fMRI; touch.

Figure 1

Experimental paradigm.

Figure 2

Whole-brain activations to touch in children, adolescents and adults. Adolescent and child maps are thresholded at p < 0.01, uncorrected for multiple comparisons. Adult maps are shown at a thresholded of p < 0.001, uncorrected.

Figure 3

(A) Adult somatosensory ROIs for main effect of touch (Arm touch + Palm touch > Rest, p < 0.001, k = 12). (B) Group mean ROI event-related brain responses (to Arm touch + Palm touch). (C) Group mean ROI-average brain responses. The error bars show standard deviations. (D) Correlations between age and individual brain ROI-average response. Abbreviations: primary somatosensory cortex (SI), secondary somatosensory cortex (SII).

Figure 4

(A) Adult affective-motivational ROIs (Arm touch > Rest, p < 0.001, k = 11). (B) Group mean ROI event-related brain responses to Arm touch. (C) Group mean ROI-average brain responses. The error bars show standard deviations. (D) Correlations between age and individual brain ROI-average response. Abbreviations: middle temporal gyrus (MTG), superior temporal sulcus (STS), frontal gyrus (FG).

Figure 5

Correlations between brain responses to tactile stimuli (β values) and age in (A) ipsilateral SII (p < 0.01, k = 12) (both genders combined) and (B) bilateral pSTS/MTG in females (p < 0.01, k = 15). The correlation plots show male brain responses extracted from the female regions, and include all males (including those excluded from the statistical analysis).