Parallel striatal and hippocampal systems for landmarks and boundaries in spatial memory

TLDR

The interaction between hippocampal and dorsal striatal memory systems is controversial, with landmark learning driven by associative reinforcement and boundary learning occurring incidentally. Participants performed fMRI while learning object locations in a virtual environment containing a landmark, a circular boundary, and distant cues, with occasional changes in landmark‑boundary relative positions to dissociate learning and performance relative to each cue. Right posterior hippocampal activity tracked boundary‑related learning and memory, while right dorsal striatal activity tracked landmark‑related learning and memory; hippocampal anterior regions processed spatial novelty separately from posterior location encoding, supporting a geometric module for incidental learning, whereas striatal activity underlies trial‑and‑error procedural learning, and the two systems influence behavior in a bottom‑up manner with ventromedial prefrontal top‑down modulation when both are active.

Abstract

How the memory systems centered on the hippocampus and dorsal striatum interact to support behavior remains controversial. We used functional MRI while people learned the locations of objects by collecting and replacing them over multiple trials within a virtual environment comprising a landmark, a circular boundary, and distant cues for orientation. The relative location of landmark and boundary was occasionally changed, with specific objects paired with one or other cue, allowing dissociation of learning and performance relative to either cue. Right posterior hippocampal activation reflected learning and remembering of boundary-related locations, whereas right dorsal striatal activation reflected learning and remembering of landmark-related locations. Within the right hippocampus, anterior processing of environmental change (spatial novelty) was dissociated from posterior processing of location. Behavioral studies show that landmark-related learning obeys associative reinforcement, whereas boundary-related learning is incidental [Doeller CF, Burgess N (2008) Proc Natl Acad Sci USA 105:5909-5914]. The distinct incidental hippocampal processing of boundaries is suggestive of a "geometric module" or "cognitive map" and may explain the hippocampal support of incidental/observational learning in "declarative" or "episodic" memory versus the striatal support of trial-and-error learning in "procedural" memory. Finally, the hippocampal and striatal systems appear to combine "bottom-up," simply influencing behavior proportional to their activations, without direct interaction, with "top-down" ventromedial prefrontal involvement when both are similarly active.