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For episodic memories, reinstating the mental context of a past experience improves retrieval of memories formed during that experience. Does context reinstatement serve a similar role for implicit, associative memories such as fear and extinction? Here, we used a fear extinction paradigm to investigate whether the retrieval of extinction (safety) memories is associated with reactivation of the mental context from extinction memory formation. In a two-day Pavlovian conditioning, extinction, and renewal protocol, we collected functional MRI data while healthy adults and adults with PTSD symptoms learned that conditioned stimuli (CSs) signaled threat through association with an electrical shock. Following acquisition, conceptually related exemplars from the CS category no longer signaled threat (i.e., extinction). Critically, during extinction only, task-irrelevant stimuli were presented between each CS trial to serve as "context tags" for subsequent identification of the possible reinstatement of this extinction context during a test of fear renewal the next day. We found that healthy adults exhibited extinction context reinstatement, as measured via multivariate pattern analysis of fMRI data, in the medial temporal lobe that related to behavioral performance, such that greater reinstatement predicted CSs being rated as safe instead of threatening. Moreover, context reinstatement positively correlated with univariate activity in the ventromedial prefrontal cortex and hippocampus, regions which are thought to be important for extinction learning. These relationships were not observed in the PTSD symptom group. These findings provide new evidence of a contextual reinstatement mechanism that helps resolve competition between the retrieval of opposing associative memories of threat and safety in the healthy adult brain that is dysregulated in PTSD.

An adaptive memory system should prioritize information surrounding a powerful learning event that may prove useful for predicting future meaningful events. The behavioral tagging hypothesis provides a mechanistic framework to interpret how weak experiences persist as durable memories through temporal association with a strong experience. Memories are composed of multiple elements, and different mnemonic aspects of the same experience may be uniquely affected by mechanisms that retroactively modulate a weakly encoded memory. Here, we investigated how emotional learning affects item and source memory for related events encoded close in time. Participants encoded trial-unique category exemplars before, during, and after Pavlovian fear conditioning. Selective retroactive enhancements in 24-h item memory were accompanied by a bias to misattribute items to the temporal context of fear conditioning. The strength of this source memory bias correlated with participants’ retroactive item memory enhancement, and source misattribution to the emotional context predicted whether items were remembered overall. In the framework of behavioral tagging: Memory attribution was biased to the temporal context of the stronger event that provided the putative source of memory stabilization for the weaker event. We additionally found that fear conditioning selectively and retroactively enhanced stimulus typicality ratings for related items, and that stimulus typicality also predicted overall item memory. Collectively, these results provide new evidence that items related to emotional learning are misattributed to the temporal context of the emotional event and judged to be more representative of their semantic category. Both processes may facilitate memory retrieval for related events encoded close in time.

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