Implicit learning and exploitation of regularities involve hippocampal and prefrontal theta activity

Observers rapidly and seemingly automatically learn to predict where to expect relevant items when those items are repeatedly presented in the same spatial context. This form of statistical learning in visual search has been studied extensively using a paradigm known as contextual cueing. The neural mechanisms underlying the learning and exploiting of such regularities remain unclear. We sought to elucidate these by examining behaviour and recording neural activity using magneto-encephalography (MEG) while observers were implicitly acquiring and exploiting statistical regularities. Computational modelling of behavioural data suggested that after repeated exposures to a spatial context, participants behaviour was marked by an abrupt switch to an exploitation strategy of the learnt regularities. MEG recordings showed that the initial learning phase was associated with larger hippocampal theta band activity for repeated scenes, while the subsequent exploitation phase showed larger prefrontal theta band activity for these repeated scenes. Strikingly, the behavioural benefit of repeated exposures to certain scenes was inversely related to explicit awareness of such repeats, demonstrating the implicit nature of the expectations acquired. This elucidates how theta activity in the hippocampus and prefrontal cortex underpins the implicit learning and exploitation of spatial statistical regularities to optimize visual search behaviour.