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.