Affective integration: episodic mechanisms underlying preconditioned threat responses

Whereas many studies have investigated generalization of learned threat across semantic dimensions, little attention has been given to the possibility that Pavlovian threat responses may spread beyond what is directly learned through episodic associations. Here, we increased the demand on episodic memory in a sensory preconditioning task to assess whether and how episodic memory contributes to threat generalization. Participants encoded forty unique episodes, each consisting of two neutral stimuli, after which one of each pair was newly associated with either an aversive or a neutral stimulus on the following day. Another day later, both stimuli of the original memories were found to trigger enhanced pupil dilation if one was indirectly linked with an aversive stimulus. This effect was independent of whether the declarative associations encoded on day one were accurately retained on the day of testing, and confined to trials on which the indirectly associated stimulus was consciously brought to mind, suggesting an important role for relational memory processes. There was no moderating effect of trait-anxiety. The present study demonstrates that the human defensive system is remarkably adept at quickly anticipating threat based on information acquired over separate events, and gives a first glimpse into how this ability is facilitated by episodic memory.