Neural correlates of emotion processing and regulation dissociate frontal and temporal lobe epilepsy

Abstract When confronted with negative events, regulating emotions is essential for self-management and mental health. Temporal lobe epilepsy (TLE) patients, particularly right TLE (rTLE) patients, show altered responses towards emotional stimuli. However, neural correlates of emotion regulation and its interplay with stimulus-based emotion processing have not been studied in TLE so far. Therefore, we compared functional MRI activity during up- and downregulation of emotions towards negative scenes among 21 left and 18 right TLE patients, 18 frontal lobe epilepsy (FLE) patients and 17 healthy controls. To assess stimulus-based processing, participants were asked to permit their feelings towards negative or neutral pictures. Voxel-based analyses were complemented by network-based analyses, as epilepsy is a network disorder. During stimulus-based emotion processing rTLE patients displayed less activation compared to all other groups. Regions of reduced activity were mostly part of the frontoparietal control network and the default mode network (both pFDR < .05) and included the frontal pole, the superior frontal gyrus, parietal regions and the cerebellum (all pFWE < .05). Activation patterns during emotion regulation were highly similar between controls and left and right TLE patients. Direct group comparisons revealed that during upregulation of emotions controls and left TLE patients displayed higher activity than FLE patients in areas of the left default mode network (all pFWE < .05). Our results dovetail with previous findings of diminished activity towards aversive stimuli in rTLE and show that in the same patients, neural underpinnings of emotion regulation are intact. In contrast, FLE patients displayed the opposite pattern with a largely intact response to aversive stimuli but disrupted neural underpinnings of emotion regulation, pointing to a double dissociation between rTLE and FLE.