Rhythmic Neural Patterns During Empathy to Vicarious Pain: Beyond the Affective-Cognitive Empathy Dichotomy

Empathy is often split into an affective facet for embodied simulation or sometimes sensorial processing, and a cognitive facet for mentalizing and perspective-taking. However, a recent neurophenomenological framework proposes a graded view on empathy (i.e., "Graded Empathy") that extends this dichotomy and considers multiple levels while integrating complex neural patterns and representations of subjective experience. In the current magnetoencephalography study, we conducted a multidimensional investigation of neural oscillatory modulations and their cortical sources in 44 subjects while observing stimuli that convey vicarious pain (vs no-pain) in a broad time window and frequency range to explore rich neural representations of pain empathy. Furthermore, we collected participants' subjective-experience of sensitivity to vicarious pain, as well as their self-reported trait levels of affective and cognitive empathy to examine the possible associations between neural mechanisms and subjective experiences and reports. While extending previous electrophysiological studies that mainly focused on alpha suppression, we found here four significant power modulation patterns corresponding to multiple facets of empathy: an early central (peaking in the paracentral sulcus) alpha (6-11 Hz) suppression pattern plausibly reflecting sensory processing, two early beta (15-23 Hz) suppression patterns in the mid-cingulate cortex (plausibly reflecting the affective component) and in the precuneus (plausibly reflecting the cognitive component), and a late anterior (peaking in the orbitofrontal cortex) alpha-beta (11-19 Hz) enhancement pattern (plausibly reflecting cognitive-control inhibitory response). Interestingly, the latter measure was negatively correlated with the subjective sensitivity to vicarious pain, thereby possibly revealing a novel inhibitory neural mechanism determining the subjective sensitivity to vicarious pain. Altogether, these multilevel findings cannot be accommodated by the dichotomous model of empathy (i.e., affective-cognitive), and provide empirical support to the Graded Empathy neurophenomenological framework. Furthermore, this work emphasizes the importance of examining multiple neural rhythms, their cortical generators, and reports of subjective-experience in the aim of elucidating the complex nature of empathy.