Repetition Suppression Reveals Cue-Specific Spatial Representations for Landmarks and Self-Motion Cues in the Human Retrosplenial Cortex.

The efficient use of various spatial cues within a setting is crucial for successful navigation. Two fundamental forms of spatial navigation, landmark-based and self-motion-based, engage distinct cognitive mechanisms. The question of whether these modes invoke shared or separate spatial representations in the brain remains unresolved. While nonhuman animal studies have yielded inconsistent results, human investigation is limited. In our previous work (Chen et al., 2019), we introduced a novel spatial navigation paradigm utilizing ultra-high field fMRI to explore neural coding of positional information. We found that different entorhinal subregions in the right hemisphere encode positional information for landmarks and self-motion cues. The present study tested the generalizability of our previous finding with a modified navigation paradigm. Although we did not replicate our previous finding in the entorhinal cortex, we identified adaptation-based allocentric positional codes for both cue types in the retrosplenial cortex (RSC), which were not confounded by the path to the spatial location. Crucially, the multi-voxel patterns of these spatial codes differed between the cue types, suggesting cue-specific positional coding. The parahippocampal cortex exhibited positional coding for self-motion cues, which was not dissociable from path length. Finally, the brain regions involved in successful navigation differed from our previous study, indicating overall distinct neural mechanisms recruited in our two studies. Taken together, the current findings demonstrate cue-specific allocentric positional coding in the human RSC in the same navigation task for the first time and that spatial representations in the brain are contingent on specific experimental conditions.