The ability to represent the world accurately relies on simultaneous coarse and fine-grained neural information coding, capturing both gist and detail of an experience. The longitudinal axis of the hippocampus may provide a gradient of representational granularity in spatial and episodic memory in rodents and humans [1-8]. Rodent place cells in the ventral hippocampus exhibit significantly larger place fields and greater autocorrelation than those in the dorsal hippocampus [1, 9-11], which may underlie a coarser and slower changing representation of space [10, 12]. Recent evidence suggests that properties of cellular dynamics in rodents can be captured with fMRI in humans during spatial navigation [13] and conceptual learning [14]. Similarly, mechanisms supporting granularity along the long axis may also be extrapolated to the scale of fMRI signal. Here, we provide the first evidence for separable scales of representation along the human hippocampal anteroposterior axis during navigation and rest by showing (1) greater similarity among voxel time courses and (2) higher temporal autocorrelation in anterior hippocampus (aHPC), relative to posterior hippocampus (pHPC), the human homologs of ventral and dorsal rodent hippocampus. aHPC voxels exhibited more similar activity at each time point and slower signal change over time than voxels in pHPC, consistent with place field organization in rodents. Importantly, similarity between voxels was related to navigational strategy and episodic memory. These findings provide evidence that the human hippocampus supports an anterior-to-posterior gradient of coarse-to-fine spatiotemporal representations, suggesting the existence of a cross-species mechanism, whereby lower neural similarity supports more complex coding of experience.

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Some theories of episodic memory hypothesize that spatial context plays a fundamental role in episodic memory, acting as a scaffold on which episodes are constructed. A prediction based on this hypothesis is that spatial context should play a primary role in the neural representation of an event. To test this hypothesis in humans, male and female participants imagined events, composed of familiar locations, people, and objects, during an fMRI scan. We used multivoxel pattern analysis to determine the neural areas in which events could be discriminated based on each feature. We found that events could be discriminated according to their location in areas throughout the autobiographical memory network, including the parahippocampal cortex and posterior hippocampus, retrosplenial cortex, posterior cingulate cortex, precuneus, and medial prefrontal cortex. Events were also discriminable based on person and object features, but in fewer regions. Comparing classifier performance in regions involved in memory for scenes and events demonstrated that the location of an event was more accurately classified than the person or object involved. These results support theories that suggest that spatial context is a prominent defining feature of episodic memory. Remembered and imagined events are complex, consisting of many elements, including people, objects, and locations. In this study, we sought to determine how these types of elements differentially contribute to how the brain represents an event. Participants imagined events consisting of familiar locations, people, and objects (e.g., kitchen, mom, umbrella) while their brain activity was recorded with fMRI. We found that the neural patterns of activity in brain regions associated with spatial and episodic memory could distinguish events based on their location, and to some extent, based on the people and objects involved. These results suggest that the spatial context of an event plays an important role in how an event is represented in the brain.

Several recent studies have explored the effect of contextual familiarity on remembered and imagined events. The aim of this study was to examine the extent of this effect by comparing the effect of cuing spatial memories, episodic memories, and imagined future events with spatial contextual cues of varying levels of familiarity. We used real-world landmark cues that had all been previously visited by the participants, and we measured the retrieval time, detail-richness, and vividness of remembered scenes, events, and imagined future events based on these cues. Participants consistently rated scenes and events based on more familiar cues as more detailed and more vivid, and they took less time to retrieve them. When the types of details were examined, it was revealed that the effects of increased contextual familiarity carry over to non-spatial details in the case of remembered events but possibly not in imagined events. This study provides evidence regarding how episodic memory and imagination are reliant on spatial context and possibly the process of scene construction.

Spatial context is a defining feature of episodic memories, which are often characterized as being events occurring in specific spatiotemporal contexts. In this review, I summarize research suggesting a common neural basis for episodic and spatial memory and relate this to the role of spatial context in episodic memory. I review evidence that spatial context serves as a scaffold for episodic memory and imagination, in terms of both behavioral and neural effects demonstrating a dependence of episodic memory on spatial representations. These effects are mediated by a posterior-medial set of neocortical regions, including the parahippocampal cortex, retrosplenial cortex, posterior cingulate cortex, precuneus, and angular gyrus, which interact with the hippocampus to represent spatial context in remembered and imagined events. I highlight questions and areas that require further research, including differentiation of hippocampal function along its long axis and subfields, and how these areas interact with the posterior-medial network.

Events always unfold in a spatial context, leading to the claim that it serves as a scaffold for encoding and retrieving episodic memories. The ubiquitous co-occurrence of spatial context with events may induce participants to generate a spatial context when hearing scenarios of events in which it is absent. Spatial context should also serve as an excellent cue for memory retrieval. To test these predictions, participants read event scenarios involving a highly familiar or less familiar spatial context, or person, which they were asked to imagine and remember. At recall, locations were more effective memory cues than people, and both were better when they were highly familiar. Most importantly, when no locations were specified at study, participants exhibited a spontaneous tendency to generate a spatial context for the scenarios, while rarely generating a person. Events with spatial context were remembered more vividly and described in more detail than those without. Together, the results favor the view that spatial context plays a leading role in remembering events.

Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (>2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the distance to the goal in the newly learned campus, as well as in familiar environments when the future route contained many turns. By contrast retrosplenial cortex only tracked the distance to the goal in the familiar campus. All of these responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and underscore the notion that the hippocampus continues to play a role in navigation when detailed processing of the environment is needed for navigation.

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