Hippocampal and prefrontal theta-band mechanisms underpin implicit spatial context learning

Abstract

Humans can rapidly and seemingly implicitly learn to predict typical locations of relevant items when those items are encountered in familiar spatial contexts. Two important questions remain, however, concerning this type of learning: (1) which neural structures and mechanisms are involved in acquiring and exploiting such contextual knowledge? (2) Is this type of learning truly implicit and unconscious? We now answer both these questions after closely examining behavior and recording neural activity using MEG while observers (male and female) were acquiring and exploiting statistical regularities. Computational modeling of behavioral data suggested that, after repeated exposures to a spatial context, participants' behavior was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that hippocampus and prefrontal cortex (PFC) were involved in the task and furthermore revealed a striking dissociation: only the initial learning phase was associated with hippocampal theta band activity, while the subsequent exploitation phase showed a shift in theta band activity to the PFC. Intriguingly, the behavioral benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. Together, these findings demonstrate that (1a) hippocampus and PFC play complementary roles in the implicit, unconscious learning and exploitation of spatial statistical regularities; (1b) these mechanisms are implemented in the theta frequency band; and (2) contextual knowledge can indeed be acquired unconsciously, and awareness of such knowledge can even interfere with the exploitation thereof.