Inter-subject phase synchronization differentiates neural networks underlying physical pain empathy.

Lucina Q Uddin,Keith M Kendrick,Jason S Nomi,Taylor Bolt,Benjamin Becker,Meina Fu,Jialin Li,Xiaoxiao Zheng,Lei Xu

doi:10.1093/scan/nsaa025

Abstract

Recent approaches for understanding the neural basis of pain empathy emphasize the dynamic construction of networks underlying this multifaceted social cognitive process. Inter-subject phase synchronization (ISPS) is an approach for exploratory analysis of task-fMRI data that reveals brain networks dynamically synchronized to task-features across participants. We applied ISPS to task-fMRI data assessing vicarious pain empathy in healthy participants (n = 238). The task employed physical (limb) and affective (face) painful and corresponding non-painful visual stimuli. ISPS revealed two distinct networks synchronized during physical pain observation, one encompassing anterior insula and midcingulate regions strongly engaged in (vicarious) pain and another encompassing parietal and inferior frontal regions associated with social cognitive processes which may modulate and support the physical pain empathic response. No robust network synchronization was observed for affective pain, possibly reflecting high inter-individual variation in response to socially transmitted pain experiences. ISPS also revealed networks related to task onset or general processing of physical (limb) or affective (face) stimuli which encompassed networks engaged in object manipulation or face processing, respectively. Together, the ISPS approach permits segregation of networks engaged in different psychological processes, providing additional insight into shared neural mechanisms of empathy for physical pain, but not affective pain, across individuals.

Highlights

Observing others in pain elicits pain empathic responses in humans
Physical pain compared with the control condition revealed increased activations in bilateral clusters including the inferior parietal lobule (IPL), dorsomedial pre-frontal cortex, insula and inferior frontal gyrus (IFG), as well as right lateralized clusters in the medial temporal lobe (MTL), inferior occipital gyrus (IOG), amygdala and thalamus (FWE peak level corrected, P < 0.05)
Task conditionspecific networks were observed for physical pain, physical control and affective control stimuli, while no robust networks were determined for the affective pain stimuli

Summary

Introduction

Observing others in pain elicits pain empathic responses in humans. Empathy, the ability to understand the feelings of others by connecting with those same feelings in one’s self, is a multifaceted social cognitive process which employs several emotional and cognitive systems, such as affect sharing, simulation, theory of mind and self–other distinction (Shamay-Tsoory, 2011). The anterior insula (AI) and the anterior cingulate cortex (ACC)—which represent core nodes of the pain matrix (Price, 2000; Wager et al, 2013) and larger salience network (Uddin, 2015)—respond both during experiencing first-hand pain as well as observing pain in others (Singer et al, 2004; Jackson et al, 2006; Bernhardt and Singer, 2012). These brain regions are involved when observing the actual infliction of physical pain in. The mirror neuron system which comprises the inferior frontal gyrus (IFG) and inferior parietal lobule (IPL) (Iacoboni and Dapretto, 2006), brain regions related to mentalizing and self-other discrimination such as the temporoparietal junction (TPJ), the medial pre-frontal cortex (mPFC), the posterior cingulate cortex (PCC) and the medial temporal lobe (MTL) (Saxe and Kanwisher, 2003; Uddin et al, 2007; Schurz et al, 2014; Kurczek et al, 2015) are engaged in pain empathy processing

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Conclusion