Threat-induced modulation of hippocampal and striatal memory systems during navigation of a virtual environment

The brain is composed of multiple memory systems that mediate distinct types of navigation. The hippocampus is important for encoding and retrieving allocentric spatial cognitive maps, while the dorsal striatum mediates procedural memories based on stimulus-response (S-R) associations. These memory systems are differentially affected by emotional arousal. In particular, rodent studies show that stress typically impairs hippocampal spatial memory while it spares or sometimes enhances striatal S-R memory. The influence of emotional arousal on these separate navigational memory systems has received less attention in human subjects. We investigated the effect of dynamic changes in anticipatory anxiety on hippocampal spatial and dorsal striatal S-R memory systems while participants attempted to solve a virtual eight-arm radial maze. In Experiment 1, participants completed a hippocampus-dependent spatial version of the eight-arm radial maze that required allocentric spatial memory to successfully navigate the environment. In Experiment 2, participants completed a dorsal striatal S-R version of the maze where no allocentric spatial cues were present, requiring the use of S-R navigation. Anticipatory anxiety was modulated via threat of receiving an unpleasant electrical shock to the wrist during memory retrieval. Results showed that threat of shock was associated with more errors and increased use of non-spatial navigational strategies in the hippocampal spatial task, but did not influence memory performance in the striatal S-R task. Findings indicate a dissociation regarding the influence of anticipatory anxiety on memory systems that has implications for understanding how fear and anxiety contribute to memory-related symptoms in human psychopathologies.