Criticism-evoked rumination is linked to dynamic adjustments of the left superficial amygdala in adolescents

The amygdala is central to processing salient social and emotional information, particularly in response to social-evaluative cues such as interpersonal criticism. Yet, it remains unclear whether perfusion or connectivity changes in specific amygdalar subnuclei track state rumination in adolescents exposed to social-evaluative criticism, and how individual differences in perceived criticism moderates these neural-cognitive responses.

Fifty-nine adolescents completed arterial spin labeling (ASL) perfusion imaging before and after an in-scanner auditory criticism task. Perfusion was quantified for the whole amygdala and anatomically defined subnuclei, followed by seed-based similarity connectivity analyses. Regression models assessed covariation between changes in perfusion/connectivity and state rumination, and moderation models tested whether perceived criticism altered these associations.

Adolescents with greater post-task rumination increases exhibited lower perfusion increases in the left amygdala, most prominently in the left superficial subnucleus (SFA). Additionally, smaller increases in similarity connectivity between the left SFA and the hippocampus/precuneus tracked larger increases in rumination. Perceived criticism moderated these perfusion- and connectivity-rumination associations. Exploratory chemoarchitectonic analyses suggested that serotonergic and dopaminergic systems may facilitate neural network reorganization underlying rumination modulation.

Social-evaluative criticism elicited increases in rumination; however, adolescents who showed greater increases in left SFA perfusion and stronger left SFA coupling with memory and self-referential regions exhibited smaller increase in ruminative responses. Higher perceived criticism dampened these associations, suggesting that interpersonal vulnerability may disrupt dynamic adjustment of SFA systems and constrain the engagement of neural mechanisms supporting cognitive and affective recovery. These findings highlight the left SFA as a subnucleus-level target for understanding and potentially enhancing recovery from negative social evaluation.