Different circuits for different pain: Patterns of functional connectivity reveal distinct networks for processing pain in self and others

Abstract

The ability to empathize with the suffering of others is critical for maintaining relationships and engaging in prosocial behavior. Recently, a series of studies have demonstrated that while watching other people experience pain (other pain), participants engage the anterior insula (AI) and anterior cingulate cortex (ACC), brain regions involved in the direct experience of pain (self pain). Here we test the hypothesis that common activity in ACC and AI may reflect the operation of distinct but overlapping networks of regions that support perception of self or other pain. To address this possibility, we scanned participants using fMRI while they received noxious thermal stimulation (self pain) or watched short videos of other people sustaining painful injuries (other pain). We isolated overlapping regions for self and other pain in the ACC and AI and then used them as seed regions for two kinds of functional connectivity analyses. These analyses identified areas whose activity co-varied with ACC and AI activity during self or other pain either across time (intra-individual connectivity) or across participants (inter-individual connectivity). Both connectivity analyses identified clusters in the midbrain and periaqueductal gray with greater connectivity to the AI during self pain as opposed to other pain. The opposite pattern was found in the dorsal medial prefrontal cortex, that showed greater connectivity to the ACC and AI during other pain than during self pain using both types of analysis. Intra-individual connectivity analyses also revealed regions in the superior temporal sulcus, posterior cingulate, and precuneus that became more connected to ACC during other pain as compared to self pain. Together, these data demonstrated that regions showing similar activity during self and other pain may nonetheless be part of distinct functional networks. These networks could not have been detected in prior work that examined overlap between self and other pain in terms of average activity, but not connectivity.

The role of social cognition in emotion

“…Alternatively, it is possible that experiential and reflective processing do work together but only in certain circumstances. This possibility is supported by a recent study examining functional connectivity of mACC and AI regions commonly active during the direct experience and observation of pain [15]. Here, mACC and AI activity was correlated with activity in pain-related brainstem nuclei during self-pain Box 1.…”

“…This 'shared representation' logic guided subsequent studies of the direct experience and observation of pain or emotion that also showed activation of overlapping neural systems, including most prominently the two cortical regions that receive ascending viscerosensory inputs: the anterior insula (AI) and the midportion of the anterior cingulate cortex (mACC) [4,7,[10][11][12][13][14][15]. The AI is believed to support affective experience in part through interoceptive awareness of these body state inputs [16,17], whereas the ACC is thought to code affective attributes of pain, such as the perceived unpleasantness (as opposed to sensory-discriminative properties, such as location and intensity) [18][19][20] and motivate appropriate behavior through projections to motor and autonomic centers [16,21].…”

Functional MRI examination of empathy for pain in people with schizophrenia reveals abnormal activation related to cognitive perspective-taking but typical activation linked to affective sharing

“…19,[46][47][48][49] Our results thus suggest that patients with schizophrenia normally represent and integrate others' pain, corroborating recent fMRI 27 and EEG 50 evidence showing that this affective aspect of empathy is preserved in schizophrenia.…”

“…13,14 The cognitive processes involved in pain empathy have been consistently associated with activation in the bilateral temporoparietal junction (TPJ), [15][16][17][18] sometimes together with the precuneus 16,17 or the medial prefrontal cortex (mPFC). 15,19 The few previous neuroimaging studies of empathy in patients with schizophrenia used various tasks and stimuli, asking participants to infer the emotional states of characters presented in verbal stories, 20 comic strips, [21][22][23] photographs/ static pictures 11,24,25 or video clips. 26 Overall, previous neuroimaging studies reported abnormal activations in patients with schizophrenia in a variety of brain regions that authors interpreted as underlying both the affective and cognitive processes contributing to empathy.…”

Synchronous with Your Feelings: Sensorimotor γ Band and Empathy for Pain

“…Empathic reactivity to others' pain seems associated to the emergence of a sensorimotor functional network Recent functional magnetic resonance imaging evidence suggests that direct and vicarious experiences of pain may depend on patterns of functional connectivity between different areas (Zaki et al, 2007). However, the relations between interareal cross-talk and empathy for pain may be captured optimally by using hightemporal resolution techniques such as MEG.…”