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

Abstract

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.

Spindle-Shaped Neurons in the Human Posteromedial (Precuneus) Cortex

“…Taken together, these results underscore the PMC’s relevance for a multitude of interacting, yet dissociable brain networks relevant for higher-level cognition. Notably, the human PC has one of the highest resting metabolic rates in the cerebral cortex and elaborates sensorimotor, visual, and cognitive/associative information ( Margulies et al, 2009 ), also including self-centered mental imagery and consciousness ( Cavanna, 2007 ), empathy and perspective-taking ( Zebarjadi et al, 2021 ), working memory (altered in cases of mild cognitive impairment, MCI, Yokosawa et al, 2020 ), episodic memory retrieval ( Cavanna and Trimble, 2006 ), and metacognition processing ( Ye et al, 2018 ).…”

Neural shifts in alpha rhythm's dual functioning during empathy

“…The second one was "empathic concern" and "perspective taking" subscales in IRI for the assessment of trait empathy (Davis, 1983). We expect to see a negative correlation between subjective sensitivity to pain (measuring by VPQ) and the late alpha enhancement that we found in our recent study (Zebarjadi et al, 2021). Besides, we conducted a phenomenological interview to evaluate the subject's social environment and life experiences.…”

Unraveling Brain Microcircuits, Dendritic Spines, and Synaptic Processing Using Multiple Complementary Approaches

“…On the other hand, high-resolution magnetic resonance imaging (MRI) would locate different nuclei in the brain (Saygin et al, 2017 for human amygdala) and help to identify likely borders for each area of interest (e.g., to separate the medial and cortical amygdaloid nuclei, Dall'Oglio et al, 2013 ; Vásquez et al, 2018 ). These data are relevant for understanding the complex expression of emotion in different species (Quirk et al, 1995 ; Zebarjadi et al, 2021 ; including mice affiliative touch in prosocial interaction, Wu et al, 2021 ) and what feelings are to humans (Zeki, 2007 ; Gendron and Barrett, 2009 ; de Boer et al, 2012 ; Diano et al, 2017 ; LeDoux and Brown, 2017 ; Fogazzi et al, 2020 ; Šimić et al, 2021 ).…”