Mental representation of the future is a fundamental component of goal-directed behavior. Computational and animal models highlight prospective spatial coding in the hippocampus, mediated by interactions with the prefrontal cortex, as a putative mechanism for simulating future events. Using whole-brain high-resolution functional magnetic resonance imaging and multi-voxel pattern classification, we tested whether the human hippocampus and interrelated cortical structures support prospective representation of navigational goals. Results demonstrated that hippocampal activity patterns code for future goals to which participants subsequently navigate, as well as for intervening locations along the route, consistent with trajectory-specific simulation. The strength of hippocampal goal representations covaried with goal-related coding in the prefrontal, medial temporal, and medial parietal cortex. Collectively, these data indicate that a hippocampal-cortical network supports prospective simulation of navigational events during goal-directed planning.

The hippocampus is believed to reduce memory interference by disambiguating neural representations of similar events. However, there is limited empirical evidence linking representational overlap in the hippocampus to memory interference. Likewise, it is not fully understood how learning influences overlap among hippocampal representations. Using pattern-based fMRI analyses, we tested for a bidirectional relationship between memory overlap in the human hippocampus and learning. First, we show that learning drives hippocampal representations of similar events apart from one another. These changes are not explained by task demands to discriminate similar stimuli and are fully absent in visual cortical areas that feed into the hippocampus. Second, we show that lower representational overlap in the hippocampus benefits subsequent learning by preventing interference between similar memories. These findings reveal targeted experience-dependent changes in hippocampal representations of similar events and provide a critical link between memory overlap in the hippocampus and behavioural expressions of memory interference.

Summary Across the domains of spatial navigation and episodic memory, the hippocampus is thought to play a critical role in disambiguating (pattern separating) representations of overlapping events. However, it is not fully understood how and why hippocampal patterns become separated. Here, we test the idea that event overlap triggers a ‘repulsion’ among hippocampal representations that develops over the course of learning. Using a naturalistic route-learning paradigm and spatiotemporal pattern analysis of human fMRI data, we found that hippocampal representations of overlapping routes gradually diverged with learning to the point that they became less similar than representations of non-overlapping events. In other words, the hippocampus not only disambiguated overlapping events, but formed representations that ‘reversed’ the objective similarity among routes. This finding, which was selective to the hippocampus, is not predicted by standard theoretical accounts of pattern separation. Critically, because the overlapping route stimuli that we used ultimately diverged (so that each route contained overlapping and non-overlapping segments), we were able to test whether the reversal effect was selective to the overlapping segments. Indeed, once overlapping routes diverged (eliminating spatial and visual similarity), hippocampal representations paradoxically became relatively more similar. Finally, using a novel analysis approach, we show that the degree to which individual hippocampal voxels were initially shared across route representations was predictive of the magnitude of learning-related separation. Collectively, these findings indicate that event overlap triggers a repulsion of hippocampal representations—a finding that provides critical mechanistic insight into how and why hippocampal representations become separated.

In studies of human episodic memory, the phenomenon of reactivation has traditionally been observed in regions of occipitotemporal cortex (OTC) involved in visual perception. However, reactivation also occurs in lateral parietal cortex (LPC), and recent evidence suggests that stimulus-specific reactivation may be stronger in LPC than in OTC. These observations raise important questions about the nature of memory representations in LPC and their relationship to representations in OTC. Here, we report two fMRI experiments that quantified stimulus feature information (color and object category) within LPC and OTC, separately during perception and memory retrieval, in male and female human subjects. Across both experiments, we observed a clear dissociation between OTC and LPC: while feature information in OTC was relatively stronger during perception than memory, feature information in LPC was relatively stronger during memory than perception. Thus, while OTC and LPC represented common stimulus features in our experiments, they preferentially represented this information during different stages. In LPC, this bias toward mnemonic information co-occurred with stimulus-level reinstatement during memory retrieval. In Experiment 2, we considered whether mnemonic feature information in LPC was flexibly and dynamically shaped by top-down retrieval goals. Indeed, we found that dorsal LPC preferentially represented retrieved feature information that addressed the current goal. In contrast, ventral LPC represented retrieved features independent of the current goal. Collectively, these findings provide insight into the nature and significance of mnemonic representations in LPC and constitute an important bridge between putative mnemonic and control functions of parietal cortex. When humans remember an event from the past, patterns of sensory activity that were present during the initial event are thought to be reactivated. Here, we investigated the role of lateral parietal cortex (LPC), a high-level region of association cortex, in representing prior visual experiences. We find that LPC contained stronger information about stimulus features during memory retrieval than during perception. We also found that current task goals influenced the strength of stimulus feature information in LPC during memory. These findings suggest that, in addition to early sensory areas, high-level areas of cortex, such as LPC, represent visual information during memory retrieval, and that these areas may play a special role in flexibly aligning memories with current goals.

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