Is Empathy for Pain Unique in Its Neural Correlates? A Meta-Analysis of Neuroimaging Studies of Empathy

Abstract

Empathy is an essential component of our social lives, allowing us to understand and share other people's affective and sensory states, including pain. Evidence suggests a core neural network—including anterior insula (AI) and mid-cingulate cortex (MCC)—is involved in empathy for pain. However, a similar network is associated to empathy for non-pain affective states, raising the question whether empathy for pain is unique in its neural correlates. Furthermore, it is yet unclear whether neural correlates converge across different stimuli and paradigms that evoke pain-empathy. We performed a coordinate-based activation likelihood estimation (ALE) meta-analysis to identify neural correlates of empathy, assess commonalities and differences between empathy for pain and for non-pain negative affective states, and differences between pain-empathy evoking stimuli (i.e., facial pain expressions vs. acute pain inflictions) and paradigms (i.e., perceptual/affective vs. cognitive/evaluative paradigms). Following a systematic search, data from 128 functional brain imaging studies presenting whole-brain results of an empathy condition vs. baseline/neutral condition were extracted. Synthesizing neural correlates of empathy confirmed a core network comprising AI, MCC, postcentral gyrus, inferior parietal lobe, thalamus, amygdala, and brainstem. There was considerable overlap in networks for empathy for pain and empathy for non-pain negative affective states. Important differences also arose: empathy for pain uniquely activated bilateral mid-insula and more extensive MCC. Regarding stimuli, painful faces and acute pain inflictions both evoked the core empathy regions, although acute pain inflictions activated additional regions including medial frontal and parietal cortex. Regarding paradigms, both perceptual/affective and cognitive/evaluative paradigms recruited similar neural circuitry, although cognitive/evaluative paradigms activated more left MCC regions while perceptual/affective paradigms activated more right AI. Taken together, our findings reveal that empathy for pain and empathy for non-pain negative affective states share considerable neural correlates, particularly in core empathy regions AI and MCC. Beyond these regions, important differences emerged, limiting generalizability of findings across different affective/sensory states. Within pain-empathy studies, the core regions were recruited robustly irrespective of stimuli or instructions, allowing one to tailor designs according to specific needs to some extent, while ensuring activation of core regions.

Linking brain structure and activation in anterior insula cortex to explain the trait empathy for pain

“…As findings by Gu et al (Gu, Liu, et al, 2013) suggested that the left AI might be a key node in a neural network that serves as the anatomical basis for cognition-emotion integration. Two meta-analyses of empathy studies provide indirect supporting evidence that the left AI might be active both in the affective-perceptual form of empathy and the cognitive-evaluative form of empathy (Fan et al, 2011;Timmers et al, 2018). The present findings do not confirm that the left AI only plays a role in cognitive empathy.…”

“…The present investigation revealed an inverse relationship between GMV in the AI and trait empathy; that is, decreased brain volume in the bilateral AI was associated with increased trait empathy scores. Additionally, in a whole-brain analysis, the peculiar inverse relationship not only show in the AI, but also in other brain regions (e.g., MCC, the precuneus, IFG, the amygdala, MFG, SMA, AG, SMG, and IPL) which is consistent with recent metaanalyses highlighting these regions as core networks involved in empathy (Fan et al, 2011;Timmers et al, 2018).…”

“…Additionally, in a whole-brain analysis, the peculiar inverse relationship not only show in the AI, but also in other brain regions (e.g., MCC, the precuneus, IFG, the amygdala, MFG, SMA, AG, SMG, and IPL) which is consistent with recent metaanalyses highlighting these regions as core networks involved in empathy (Fan et al, 2011;Timmers et al, 2018). The present investigation revealed an inverse relationship between GMV in the AI and trait empathy; that is, decreased brain volume in the bilateral AI was associated with increased trait empathy scores.…”

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

“…The components encompassed a network primarily including the inferior and lateral parietal regions, the postcentral and supramarginal gyrus, AI and adjacent IFG as well as the dmPFC and adjacent MCC regions. Previous metaanalytic results from studies employing subtraction contrasts revealed a highly overlapping network engaged during empathic responses, including pain empathy (Fan et al, 2011;Lamm et al, 2011;Timmers et al, 2018).…”

“…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 (Bernhardt & Singer, 2012;Jackson, Rainville, & Decety, 2006;Singer et al, 2004). Meta-analyses of fMRI studies have furthermore confirmed robust engagement of the AI and cingulate regions, specifically dorsal ACC and anterior portions of the midcingulate cortex (MCC) during empathic processes, including pain empathy (Fan, Duncan, de Greck, & Northoff, 2011;Lamm, Decety, & Singer, 2011;Timmers et al, 2018). Empathy is a multifaceted socialcognitive process which employs several emotional and cognitive systems (Shamay-Tsoory, 2011), such as the mirror-neuron system underlying simulation and affect sharing which comprises the inferior frontal gyrus (IFG) and inferior parietal lobule (IPL) (Iacoboni & Dapretto, 2006), mentalizing and self-other discrimination which additionally engage the temporoparietal junction (TPJ), the medial prefrontal cortex (mPFC), the posterior cingulate cortex (PCC) and the medial temporal lobe (MTL) (Kurczek et al, 2015;Saxe & Kanwisher, 2003;Schurz, Radua, Aichhorn, Richlan, & Perner, 2014;Uddin, Iacoboni, Lange, & Keenan, 2007).…”