Neural shifts in alpha rhythm's dual functioning during empathy maturation

Introduction: Empathy is a social–cognitive process that operates by relying mainly on the suppression of the cortical alpha rhythm. This phenomenon has been evidenced in dozens of electrophysiological studies targeting adult human subjects. Yet, recent neurodevelopmental studies indicated that at a younger age, empathy involves reversed brain responses (e.g., alpha enhancement patterns). In this multimodal study, we capture neural activity at the alpha range, and hemodynamic response and target subjects at approximately 20 years old as a unique time window in development that allows investigating both low-alpha suppression and high-alpha enhancement. We aim to further investigate the functional role of low-alpha power suppression and high-alpha power enhancement during empathy development. Methods: Brain data from 40 healthy individuals were recorded in two consecutive sessions of magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) while subjects perceived vicarious physical pain or no pain. Results: MEG revealed that the alpha pattern shift during empathy happens in an all-or-none pattern: power enhancement before 18 and suppression after 18 years of age. Additionally, MEG and fMRI highlight a correspondence between high-alpha power increase and blood-oxygen-level-dependent (BOLD) decrease before 18, but low-alpha power decrease and BOLD increase after 18. Importantly, this neurodevelopmental transition was not revealed by four other measures: self-reported (a) ratings of the task stimuli, (b) ratings of naturalistic vignettes of vicarious pain, (c) trait empathy, or neural data from (d) a control neuroimaging task. Discussion: Findings suggest that at the critical age of around 18, empathy is underpinned by an all-or-none transition from high-alpha power enhancement and functional inhibition to low-alpha power suppression and functional activation in particular brain regions, possibly indicating a marker of maturation in empathic ability. This work advances a recent neurodevelopmental line of studies and provides insight into the functional maturation of empathy at the coming of age.