Distinct hippocampus codes for contextual cueing: learning contexts and their predictive associations with targets in...

Humans can learn to exploit repeated distractor arrangements to optimize attentional selection of targets, producing contextual facilitation. The hippocampus is thought to support context representations acquired from repeatedly searching a given scene layout. However, it remains unclear whether the hippocampus primarily encodes context-target associations, in which the distractor layout directly predicts the target location, or whether it additionally encodes associations among distractors, enabling target prioritization indirectly via context suppression. To examine the neural mechanisms of contextual learning, we combined functional magnetic resonance imaging with a two-phase visual search paradigm: Phase 1 presented predictive (repeated) distractor layouts with consistent target locations, affording contextual cueing; Phase 2 rendered these layouts non-predictive by randomizing target locations, fostering context suppression. Contextual facilitation was compared against a baseline of non-repeated arrangements. We found that both context-target (Phase 1) and distractor-distractor (Phase 2) associations were reliably decoded from the hippocampus using correlation-based multi-voxel pattern analysis. A functional dissociation emerged along the hippocampal axis: anterior and posterior hippocampal regions identified in the whole-brain univariate analyses exhibited relatively greater contributions to Phase 1 context-target and Phase 2 distractor-distractor associations, respectively, indicating their stronger involvement in the corresponding memory representations. Connectivity modeling showed the temporoparietal junction (TPJ) interacted with the hippocampus in different ways depending on context predictivity. These findings indicate anatomically separable hippocampal circuits represent predictive context-target and non-predictive distractor-distractor relations, with their attentional effects gated by the TPJ. SIGNIFICANCE STATEMENT: Although the hippocampus supports the encoding and retrieval of recurrent spatial distractor-target relations in visual search, its distinct roles in representing context-target relations (associating the target location with the configuration of distractors) versus sole-context (distractor-distractor) configurations has not been dissociated. The present study decoded both forms of contextual representation in the hippocampus: the anterior hippocampus preferentially encoded context-target associations, whereas the posterior hippocampus maintained sole-context memory. The signals generated by these distinct hippocampal regions regulate how the target is prioritized for attentional selection, with the temporoparietal junction (TPJ) dynamically adjusting the mode of prioritization in response to the learnt configural structure and how reliably it predicts the target location.