Outside Looking In: Landmark Generalization in the Human Navigational System.

The use of landmarks is central to many navigational strategies. Here we use multivoxel pattern analysis of fMRI data to understand how landmarks are coded in the human brain. Subjects were scanned while viewing the interiors and exteriors of campus buildings. Despite their visual dissimilarity, interiors and exteriors corresponding to the same building elicited similar activity patterns in the parahippocampal place area (PPA), retrosplenial complex (RSC), and occipital place area (OPA), three regions known to respond strongly to scenes and buildings. Generalization across stimuli depended on knowing the correspondences among them in the PPA but not in the other two regions, suggesting that the PPA is the key region involved in learning the different perceptual instantiations of a landmark. In contrast, generalization depended on the ability to freely retrieve information from memory in RSC, and it did not depend on familiarity or cognitive task in OPA. Together, these results suggest a tripartite division of labor, whereby PPA codes landmark identity, RSC retrieves spatial or conceptual information associated with landmarks, and OPA processes visual features that are important for landmark recognition. SIGNIFICANCE STATEMENT: A central element of spatial navigation is the ability to recognize the landmarks that mark different places in the world. However, little is known about how the brain performs this function. Here we show that the parahippocampal place area (PPA), a region in human occipitotemporal cortex, exhibits key features of a landmark recognition mechanism. Specifically, the PPA treats different perceptual instantiations of the same landmark as representationally similar, but only when subjects have enough experience to know the correspondences among the stimuli. We also identify two other brain regions that exhibit landmark generalization, but with less sensitivity to familiarity. These results elucidate the brain networks involved in the learning and recognition of navigational landmarks.