Distinct neural networks underlying empathy for pleasant and unpleasant touch.

Abstract

In spite of considerable progress in the understanding of the neural mechanisms underlying the experience of empathy, the majority of previous investigations have focused on how we share negative affective states (and in particular pain) of others, whereas only few studies have targeted empathy for positive emotions. This bias has precluded addressing one of the central tenets of the shared representations account of empathy, which is that different networks should be engaged when empathizing with emotions that are represented on different neural levels. The aim of the present study was to overcome this limitation and to test whether empathy for pleasant and unpleasant affective touch is underpinned by different neural networks. To this end we used functional magnetic resonance imaging (fMRI), with two independent replication experiments (N = 18, N = 32), and a novel paradigm enabling the joint investigation of first-hand and vicarious responses to pleasant and unpleasant affect induced via visuo-tactile stimulation. This revealed that empathy is subserved by distinct neural networks, with those regions recruited in the first-hand experience of positive or negative affective states also being specifically recruited when empathizing with these respective states in others. More specifically, the first-hand and vicarious experience of pleasant touch commonly recruited medial orbitofrontal cortex (OFC), while unpleasant touch was associated with shared activation in the right fronto-insular cortex. The observation that specifically tailored subsystems of the human brain are engaged to share positive versus negative touch of others brings fresh evidence to one of the major goals of the social neuroscience of empathy: to identify which specific aspects of the affective states of others are shared, and what role this plays in enabling the understanding of the emotions of others.