No 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.

There is an inconsistency regarding the relationship between thinking about personal past experiences during autobiographical memory (AM) and thinking about other people's mental states during theory of mind (ToM). Neuroimaging studies of AM and ToM consistently report overlap in the brain regions recruited. Lesion data, however, show that amnesic people with AM impairment can have intact ToM, suggesting that distinct neural mechanisms support these abilities [Rosenbaum, R. S., Stuss, D. T., Levine, B., & Tulving, E. Theory of mind is independent of episodic memory. Science, 318, 1257, 2007]. The current fMRI study examined the functional and neural correlates of remembering one's own experiences in response to personal photos (AM condition) and imagining others' experiences in response to strangers' photos (ToM condition). AM and ToM conditions were matched in terms of content and vividness, and were compared directly and to a common baseline. Analyses revealed common activity within frontal and temporal–parietal regions, yet midline structures exhibited greater activity during AM. More specific analyses of event construction and detail elaboration revealed unique activation of the right hippocampus during AM construction, and of lateral regions, such as the right temporo-parietal junction (TPJ) during ToM elaboration. Moreover, a region of left hippocampus/perirhinal cortex appeared to be driven by event vividness. Thus, differences in AM and ToM emerge when a common baseline is used and temporal dynamics are taken into account. Furthermore, the right TPJ and related lateral regions, and not the hippocampus, may be needed for ToM, given that this ability is intact in amnesic people.