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

Contains fulltext : 214020.pdf (publisher's version ) (Open Access)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?; and (2) is this type of learning truly implicit and unconscious? We now answer both these questions after closely examining behaviour and recording neural activity using magneto-encephalography (MEG) while observers (male and female) were 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 hippocampus and prefrontal cortex 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 prefrontal cortex. Intriguingly, 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. Taken together, these findings demonstrate (1a) that hippocampus and prefrontal cortex play complementary roles in the implicit, unconscious learning and exploitation of spatial statistical regularities; (1b) that these mechanisms are implemented in the theta frequency band; and (2) that contextual knowledge can indeed be acquired unconsciously, and that awareness of such knowledge can even interfere with the exploitation thereof. SIGNIFICANCE STATEMENTHuman visual perception is determined not just by the light that strikes our eyes, but also strongly by our prior knowledge and expectations. Such expectations, particularly about where to expect certain objects given scene context, might be learned implicitly and unconsciously - although this is hotly debated. Furthermore, it is unknown which brain mechanisms underpin this type of learning. We now show that, indeed, spatial prior expectations can be learned without awareness; in fact, strikingly, awareness seems to hinder the exploitation of the relevant knowledge. Furthermore, we demonstrate that one brain mechanism (hippocampal theta-band activity) is responsible for learning in these settings, while another mechanism (prefrontal theta-band activity) is involved in exploiting the learned associations.10 p