Declarative memory modulation in threatening environments: Introducing a cognitive account based on aversive prediction errors

Abstract

Declarative memory aids behavioral adaptation by identifying predictors of important consequences. To ensure an efficient retrieval of such self-relevant information considering the overabundance of everyday impressions, long-lasting memory is formed relatively sparsely. The present work aimed to characterize principles under which this memory modulation operates in threatening environments. Prior studies have repeatedly shown an unspecific modulation of memory for stimuli surrounding salient experiences, but more recent evidence additionally points towards a more specific enhancement of memory that only affects items belonging to a motivationally significant category. In Study 1, we successfully replicated a category-specific `online' memory enhancement, which was characterized by the superior memory for stimuli from a shock-associated category that were encoded during fear conditioning. This effect prospectively carried over to stimuli from the same category that were subsequently encoded without the threat of shock. However, our results cast doubt over claims that this category-specific memory modulation also retroactively affects stimuli from the shock-associated category that were encoded prior to fear conditioning. In Study 2, we proposed an even more specific modulation of memory that operates at the level of unique stimuli. In line with established models, we found that greater physiological arousal elicited by individual trial outcomes was linked with better subsequent memory performance. Critically, we present evidence for a novel cognitive account of memory modulation that goes beyond these influences of physiological arousal and is characterized by an improved memory for stimuli associated with surprising outcomes, which were formalized as aversive prediction errors (PEs). In Study 3, we aimed to characterize the neural basis of this PE-driven account using fMRI. Results suggested a mechanism that is distinct from expectancy-congruent modes of memory formation associated with an activation of medial-temporal structures and instead relies on the recruitment of the salience network. Overall, our results paint a nuanced picture of an adaptive memory system that uses multiple complementary strategies to ensure an efficient storage of self-relevant information.