Adolescents' brain-autonomic coupling during emotion processing

Abstract

Autonomic nervous system (ANS) activity is a core component of emotion processing. The limbic system and medial prefrontal cortex play important roles in the regulation of ANS activity. However, the integration of brain activity and ANS activity has yet to be investigated in adolescents despite independent evidence of adolescents' heightened neural and physiological sensitivity to emotional stimuli. The present study examined the relations of ANS activity in the parasympathetic nervous system (PNS) and sympathetic nervous system (SNS) with brain activity during emotional face processing in adolescents. 135 adolescents (65 female; M = 17.15 yr, SD = 0.42) completed an emotional faces task during an fMRI scan while electrocardiography and skin conductance were recorded simultaneously. Using linear mixed-effect modelling, we tested the effect of change in respiratory sinus arrhythmia (RSA), a measure of PNS activity, and number of skin conductance responses (SCRs), a measure of SNS activity, on neural activity while adolescents viewed emotional faces. Greater RSA withdrawal, indicating decreased PNS activity, was associated with increased activation in the ventromedial prefrontal cortex (vmPFC). More SCRs, indicating greater SNS activity, were associated with decreased activation in several regions including the dorsomedial prefrontal cortex and increased activation in the left hippocampus. Left hippocampus-SCR coupling and vmPFC-RSA coupling predicted baseline SCR and RSA respectively. These findings implicate the hippocampus for potentiating SNS activity, document that regulation of SNS and PNS activity are coordinated with distinct regions of the medial prefrontal cortex, and suggest potential developmental differences in vmPFC regulation of PNS activity between adolescents and adults.