Distinct medial-temporal lobe mechanisms of encoding and amygdala-mediated memory reinstatement for disgust and fear

Abstract

Current models of episodic memory posit that retrieval involves the reenactment of encoding processes. Recent evidence has shown that this reinstatement process – indexed by subsequent encoding-retrieval similarity of brain activity patterns - is related to the activity in the hippocampus during encoding. However, we tend to re-experience emotional events in memory more richly than dull events. The role of amygdala - a critical hub of emotion processing – in reinstatement of emotional events was poorly understood. To investigate it, we leveraged a previously overlooked divergence in the role of amygdala in memory modulation by distinct emotions - disgust and fear. Here we used a novel paradigm in which participants encoded complex events (word pairs) and their memory was tested after 3 weeks, both phases during fMRI scanning. Using representational similarity analysis and univariate analyses, we show that the strength of amygdala activation during encoding was correlated with memory reinstatement of individual event representations in emotion-specific regions. Critically, amygdala modulated reinstatement more for disgust than fear. This was in line with other differences observed at the level of memory performance and neural mechanisms of encoding. Specifically, amygdala and perirhinal cortex were more involved during encoding of disgust-related events, whereas hippocampus and parahippocampal gyrus during encoding of fear-related events. Together, these findings shed a new light on the role of the amygdala and medial temporal lobe regions in encoding and reinstatement of specific emotional memories.