Abstract
Intrusive memories often take the form of distressing images that emerge into a person's awareness, unbidden. A fundamental goal of clinical neuroscience is to understand the mechanisms allowing people to control these memory intrusions and reduce their emotional impact. Mnemonic control engages a right frontoparietal network that interrupts episodic retrieval by modulating hippocampal activity; less is known, however, about how this mechanism contributes to affect regulation. Here we report evidence in humans (males and females) that stopping episodic retrieval to suppress an unpleasant image triggers parallel inhibition of mnemonic and emotional content. Using fMRI, we found that regulation of both mnemonic and emotional content was driven by a shared frontoparietal inhibitory network and was predicted by a common profile of medial temporal lobe downregulation involving the anterior hippocampus and the amygdala. Critically, effective connectivity analysis confirmed that reduced amygdala activity was not merely an indirect consequence of hippocampal suppression; rather, both the hippocampus and the amygdala were targeted by a top-down inhibitory control signal originating from the dorsolateral prefrontal cortex. This negative coupling was greater when unwanted memories intruded into awareness and needed to be purged. Together, these findings support the broad principle that retrieval suppression is achieved by regulating hippocampal processes in tandem with domain-specific brain regions involved in reinstating specific content, in an activity-dependent fashion.SIGNIFICANCE STATEMENT Upsetting events sometimes trigger intrusive images that cause distress and that may contribute to psychiatric disorders. People often respond to intrusions by suppressing their retrieval, excluding them from awareness. Here we examined whether suppressing aversive images might also alter emotional responses to them, and the mechanisms underlying such changes. We found that the better people were at suppressing intrusions, the more it reduced their emotional responses to suppressed images. These dual effects on memory and emotion originated from a common right prefrontal cortical mechanism that downregulated the hippocampus and amygdala in parallel. Thus, suppressing intrusions affected emotional content. Importantly, participants who did not suppress intrusions well showed increased negative affect, suggesting that suppression deficits render people vulnerable to psychiatric disorders.
Highlights
Sometimes the past intrudes upon the present
We focused on the anterior section of the right middle frontal gyrus (MFG), which encompasses the putative supramodal inhibitory control region spanning motor, memory, and emotion inhibition described by Depue et al (2015)
Modulation of medial temporal lobe (MTL) activity is parallel and reactive the current findings suggest that suppressing intrusive memories disrupts episodic and emotional traces, it does not establish that right MFG modulates MTL activity, nor whether such modulation acts in parallel on both memory and emotion-related sites
Summary
Correspondence should be addressed to Dr Pierre Gagnepain, Inserm-EPHE-UNICAEN U1077, Centre Cyceron, vivid, persistent, and distressing for individuals suffering from post-traumatic stress, anxiety, or obsessive-compulsive disorders (Brewin et al, 2010). Distressing images are thought to both precipitate psychopathological symptoms and contribute to their maintenance
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