Dissociable Retrosplenial and Hippocampal Contributions to Successful Formation of Survey Representations

Abstract

During everyday navigation, humans encounter complex environments predominantly from a first-person perspective. Behavioral evidence suggests that these perceptual experiences can be used not only to acquire route knowledge but also to directly assemble map-like survey representations. Most studies of human navigation focus on the retrieval of previously learned environments, and the neural foundations of integrating sequential views into a coherent representation are not yet fully understood. We therefore used our recently introduced virtual-reality paradigm, which provides accuracy and reaction-time measurements precisely indicating the emergence of survey knowledge, and functional magnetic resonance imaging while participants repeatedly encoded a complex environment from a first-person ground-level perspective. Before the experiment, we gave specific instructions to induce survey learning, which, based on the clear evidence for emerging survey knowledge in the behavioral data from 11 participants, proved successful. Neuroimaging data revealed increasing activation across sessions only in bilateral retrosplenial cortices, thus paralleling behavioral measures of map expertise. In contrast, hippocampal activation did not follow absolute performance but rather reflected the amount of knowledge acquired in a given session. In other words, hippocampal activation was most prominent during the initial learning phase and decayed after performance had approached ceiling level. We therefore conclude that, during navigational learning, retrosplenial areas mainly serve to integrate egocentric spatial information with cues about self-motion, whereas the hippocampus is needed to incorporate new information into an emerging memory representation.

Lateralized human hippocampal activity predicts navigation based on sequence or place memory

“…The right hippocampus and the midbrain showed a time-dependent decrease of activity during learning trials, consistent with previous studies showing an important role of both of these regions in novelty detection (54), and with the involvement of the hippocampus in spatial-change detection (16) and learning (22). Furthermore, in agreement with a recent report (55), the time-courses of hippocampal and midbrain activation were highly correlated throughout the experiment.…”

“…Furthermore, in agreement with a recent report (55), the time-courses of hippocampal and midbrain activation were highly correlated throughout the experiment. The left hippocampal activity during egocentric probe trials also decreased over successive trials, again consistent with reducing hippocampal involvement as sequential tasks become familiar (39) and learning reduces (22). These findings may relate to previous fMRI studies of novelty, in that left hippocampal activation is associated with sequential novelty (40) and right hippocampal activation is associated with spatial novelty (16).…”

“…Correspondingly, the pattern of activation in the training trials (bilateral hippocampus, medial prefrontal, and caudate) overlaps with both the allocentric and the sequential egocentric activations during probe trials. Activations that distinguished allocentric from sequential egocentric strategies included the bilateral parietooccipital sulcus: a region previously shown to be related to allocentric spatial processing (22,25,50), retrieval of spatial memories into imagery (24), and navigation (15,51). The reverse pattern (sequential egocentric vs. allocentric strategies) shows activations of the posterior insula, which corresponds to the human analog of the primate vestibular cortex (52) and posterior parietal operculum, which might be related to movement processing (53).…”

“…We hypothesized that we would identify, before the first choice-point, areas of the hippocampal prefrontal striatal loop involved in supporting the allocentric and sequential egocentric representations. In addition, we would expect to see some changes in activation over the time-course of the experiment, including increased hippocampal involvement early in the task, when novelty and learning is maximal (16,22), and increased retrosplenial/ medial parietal regions later in the task, as a detailed internal representation of the environment is formed that can support mental imagery (9,17,(21)(22)(23)(24)(25).…”

Event-Based Prospective Remembering in a Virtual World

“…Considering the three dimensional nature of the EVET a spatial wayfinding task might be more suitable for use in future studies (for example see Wolbers & Buchel, 2005).…”