Distinct amygdalar pathways to frontopolar cortex and medial temporal lobe support temporal memory for emotional events

Abstract

Growing evidence suggests that emotion shapes temporal aspects of memory--such as remembering when an event occurred--yet the neural bases of these effects remain unclear. Prior work indicates that temporal-context representations in memory are supported by the function of medial temporal lobe (MTL) and prefrontal regions with privileged access to amygdala-originated affective signals, which may mediate emotional influences on temporal memory--including hippocampus, perirhinal cortex, and lateral frontopolar cortex (FPl). To test whether these candidate pathways shape temporal memory for emotional events, participants encoded trial-unique negative and positive images in the scanner, followed by a surprise temporal memory task. We found that more negative stimuli were associated with greater amygdala activation and lower temporal-memory error for when emotional images occurred. Replicating and extending prior work, higher stimulus-evoked multivoxel pattern similarity in the hippocampus (between trials) and FPl (within and between trials) was associated with higher temporal memory errors. Notably, greater amygdala responding to emotional images predicted higher between-trial pattern similarity in the hippocampus, but lower within- and between-trial similarity in FPl. Amygdala engagement was also correlated with greater perirhinal activation, which in turn predicted stronger item memory and a recency bias in temporal memory estimates. Collectively, these findings reveal distinct--and opposing--modulatory effects of amygdala-FPl and amygdala-MTL pathways on temporal memory, with the potential to sharpen and blur memory for when emotional events occurred. Significance statementEmotional events influence how we remember time. Prior work implicates function of the lateral frontal pole (FPl) and medial temporal lobe (MTL) regions--including hippocampus and perirhinal cortex--in temporal memory. Yet, whether and how these areas support temporal memory for emotional events remains unclear. Using trial-unique emotional images, we found that negative-emotional valence was associated with stronger amygdala activation and temporal-memory accuracy. Higher pattern similarity in hippocampus and FPl predicted worse temporal memory. Notably, amygdala activation predicted higher between-trial hippocampal pattern similarity but lower within-trial FPl similarity. Perirhinal engagement, which correlated with amygdala activation and item memory, predicted a recency bias in temporal-memory judgments. Together, these findings reveal distinct amygdala-MTL and amygdala-prefrontal pathways through which emotion shapes temporal memory.