Multiple Scales of Representation along the Hippocampal Anteroposterior Axis in Humans

Abstract

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.

Constructing and Forgetting Temporal Context in the Human Cerebral Cortex

“…In neuroscience, multiple timescale representations have been proposed for learning value functions (Sutton, 1995), for tracking reward (Bernacchia et al, 2011), and for perceiving and controlling action (Botvinick, 2007;Paine and Tani, 2005). Moreover, the concept of temporal "grain" is influential in theories of hippocampal organization (Brunec et al, 2018;Momennejad and Howard, 2018;Poppenk et al, 2013;Shankar et al, 2016) and cortical organization (Baldassano et al, 2017;Fuster, 1997;Hasson et al, 2015;Lü et al, 1992;Wacongne et al, 2011). Consistent with hierarchical timescale models, we find that more temporally extended representations are learned in higher stages of processing, where dynamics change more slowly.…”

Age-related alterations in functional connectivity along the longitudinal axis of the hippocampus and its subfields

“…(Figure 5A-C). We found a clear pattern consistent with aging modifying the pattern observed by (77). The anterior segments (1-4) exhibited greater FC for young adults than older adults ( Figure 5A), particularly in the right hemisphere ( Figure 5C).…”

“…Having established the FC profiles along the longitudinal axis of the hippocampus with the MTL, we sought to explore FC within the hippocampus itself. A recent investigation in young adults showed greater inter-voxel similarity for the anterior than the posterior hippocampus, indicating greater FC within the anterior portion (77). Similarly, we were interested in how age-related change along the longitudinal axis of the hippocampus may influence the connectivity among these regions.…”

Event conjunction: How the hippocampus integrates episodic memories across event boundaries

“…There is growing evidence to suggest that hippocampal representations of space shift along the longitudinal axis (Poppenk, Evensmoen, Moscovitch, & Nadel, ; Strange, Witter, Lein, & Moser, ). In humans, the most posterior portion of the hippocampus represents local space while the most anterior portion represents the more general environment (Brunec et al, ). If we apply these principles to event models, we would anticipate that the more focal event models are housed in the posterior hippocampus while more overarching models are housed in the anterior hippocampus (Collin, Milivojevic, & Doeller, ).…”