Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds

Abstract

Background. Affective touch carries strong significance for social mammals, including humans. Gentle, dynamic touch of a kind that occurs during social interactions is preferentially encoded by a distinct neural pathway involving tactile C (CT) afferents, a type of unmyelinated afferent nerve found exclusively in hairy skin. CT afferents increase firing when the skin is stroked at a pleasant, caress-like speed of~3 cm/s, and their discharge frequency correlates with the subjective hedonic experience of the caress. In humans, the posterior insula is a cortical target for CT afferents. Since the potential social relevance of affective touch extends to the touch interactions of others, we postulated that information from CT afferents in posterior insular cortex provides a basis for encoding observed caresses. Results. In two experiments, we exploited CT afferents' functionally unique tuning curve for stroking speed, demonstrating that a speed optimal for eliciting CT discharge (3 cm/s) also gives rise to higher BOLD responses in posterior insula than a nonoptimal speed (30 cm/s). When participants viewed videos of others' arms being stroked at CT-optimal versus -nonoptimal speeds, the posterior insula showed a similar response as to directly felt touch. Further, this region's response was specific for social interactions, showing no CT-related modulation for nonsocial dynamic-touch videos. Conclusions. These findings provide direct evidence for a functional relationship between CT signaling and processing in posterior insular cortex. Such selective tuning for CT-optimal signals in insula may allow recognition of the hedonic relevance of a merely observed caress. © 2011 the authors.