Increased similarity of neural responses to experienced and empathic distress in costly altruism

Abstract

Empathy—affective resonance with others’ sensory or emotional experiences—is hypothesized to be an important precursor to altruism. However, it is not known whether real-world altruists’ heightened empathy reflects true self-other mapping of multi-voxel neural response patterns. We investigated this relationship in adults who had engaged in extraordinarily costly real-world altruism: donating a kidney to a stranger. Altruists and controls completed fMRI testing while anticipating and experiencing pain, and watching as a stranger anticipated and experienced pain. Machine learning classifiers tested for shared representation between experienced and observed distress. Altruists exhibited more similar representations of experienced and observed fearful anticipation spontaneously and following an empathy prompt in anterior insula and anterior/middle cingulate cortex, respectively, suggesting heightened empathic proclivities and abilities for fear. During pain epochs, altruists were distinguished by spontaneous empathic responses in anterior insula, anterior/mid-cingulate cortex and supplementary motor area, but showed no difference from controls after the empathy prompt. These findings (1) link shared multi-voxel representations of the distress of self and others to real-world costly altruism, (2) reinforce distinctions between empathy for sensory states like pain and anticipatory affective states like fear, and (3) highlight the importance of differentiating between the proclivity and ability to empathize.

A feature-based network analysis and fMRI meta-analysis reveal three distinct types of prosocial decisions

“…The second sub-system comprised regions commonly involved in representing and empathizing with the distress of others, and included the dorsal ACC, pre-SMA, and anterior insula (Ashar et al, 2017; Decety & Lamm, 2006; Lamm et al, 2011). Activation in these regions emerged only during altruistic decisions, consistent with the theory that affective resonance with others’ distress give rise to empathic concern and altruistic motivation, which is a primary motivator of prosocial behavior in the absence of cooperative or equity-maintaining goals (Batson, 2009, 2011; Brethel-Haurwitz et al, 2018; Decety et al, 2016; O’Connell et al, 2019). This finding was likely driven by eight out of the fourteen identified altruistic studies including stimuli that depicted or implied the need or distress of beneficiaries.…”

“…Recent work has focused on making neuroimaging paradigms more “naturalistic,” such as viewing or listening to narratives or interacting in real-time with another person in the laboratory (Hasson & Frith, 2016; Redcay & Moraczewski, 2019; Redcay & Schilbach, 2019; Wheatley et al, 2019) or in the real-world (Dikker et al, 2019). Other work has concentrated on characterizing the behavioral and neural features of individuals who engage in extreme forms of real-world prosociality (Brethel-Haurwitz et al, 2018; Marsh et al, 2014; O’Connell et al, 2019; Vekaria et al, 2020). Understanding the neurobiology underlying more ecologically-valid altruistic decisions will be crucial for understanding the broader picture of prosocial decision-making.…”

Healthcare experience affects pain-specific responses to others’ suffering in the anterior insula

“…[8][9][10][11][12][13][14] . Remarkably, these activity patterns are highly similar to those measured when pain is experienced directly by oneself [15][16][17][18][19][20][21][22] , and they are attenuated by those same analgesic procedures that regulate first-hand nociception, such as placebo or hypnosis 17,23,24 . These results suggest that others' pain is at least partly processed in an embodied (or empathetic) fashion, that is, by simulating its somatic and affective properties on one's own body 25,26 .…”

“…Previous studies have reported how AI and middle cingulate cortex (MCC) respond to others' suffering [8][9][10][11][12][13][14] , as conveyed through facial expressions 4,20,21,23,24 , photos/videos of injuries 15,17,18,21,27,28,35,38,50 , symbolic cues 16,19,22,51 , and short narratives 34,36,[42][43][44][45] . Yet the functional interpretation of these neural responses remains debated.…”

“…These were an "Handedness" task where subjects were exposed to pictures of people's injuries, as well as painless neutral and negative control images 15,18,35 ; a "Cognitive and Affective Theory of Mind" task, where participants read short narratives, and subsequently were asked to infer the protagonist's thoughts/beliefs, emotions and pain 34,36 ; a "Pain Localizer", where individuals received noxious or non-noxious thermal stimulations on their own dominant hand. This allowed us to assess whether scholarly and professional healthcare experience affects the neural responses to others' pain 4,27,28 and, most critically, whether such influence operates on state-specific representations shared with first-hand nociception [15][16][17][18][19][20][21][22] or generalizes to other emotional or attentionally salient events.…”