The neural systems that code for location and facing direction during spatial navigation have been extensively investigated; however, the mechanisms by which these quantities are referenced to external features of the world are not well understood. To address this issue, we examined behavioral priming and fMRI activity patterns while human subjects re-instantiated spatial views from a recently learned virtual environment. Behavioral results indicated that imagined location and facing direction were represented during this task, and multi-voxel pattern analyses indicated the retrosplenial complex (RSC) was the anatomical locus of these spatial codes. Critically, in both cases, location and direction were defined based on fixed elements of the local environment and generalized across geometrically-similar local environments. These results suggest that RSC anchors internal spatial representations to local topographical features, thus allowing us to stay oriented while we navigate and to retrieve from memory the experience of being in a particular place.

Humans, like other mobile organisms, rely on spatial representations to guide navigation from place to place. Although previous work has identified neural systems involved in wayfinding, the specific spatial codes supported by these systems are not well understood. We use functional magnetic resonance imaging (fMRI) to identify regions within the human medial temporal and medial parietal lobes that encode two fundamental spatial quantities – location and facing direction – in a manner that abstracts away from sensory inputs. University students were scanned while viewing photographs taken at several familiar campus locations. Multivoxel pattern analyses indicated that the left presubiculum, retrosplenial complex (RSC), and parietal-occipital sulcus (POS) coded location identity even across non-overlapping views, whereas the right presubiculum coded facing direction even across non-contiguous locations. The location and direction codes supported by these regions may be critical to our ability to navigate within the extended environment and to understand its large-scale spatial structure.

Humans and animals use landmarks during wayfinding to determine where they are in the world and to guide their way to their destination. To implement this strategy, known as landmark-based piloting, a navigator must be able to: (i) identify individual landmarks, (ii) use these landmarks to determine their current position and heading, (iii) access long-term knowledge about the spatial relationships between locations and (iv) use this knowledge to plan a route to their navigational goal. Here, we review neuroimaging, neuropsychological and neurophysiological data that link the first three of these abilities to specific neural systems in the human brain. This evidence suggests that the parahippocampal place area is critical for landmark recognition, the retrosplenial/medial parietal region is centrally involved in localization and orientation, and both medial temporal lobe and retrosplenial/medial parietal lobe regions support long-term spatial knowledge.

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.

Summary Low-frequency (delta/theta band) hippocampal neural oscillations play prominent roles in computational models of spatial navigation but their exact function remains unknown. Some theories propose they are primarily generated in response to sensorimotor processing while others suggest a role in memory-related processing. We directly recorded hippocampal EEG activity in patients undergoing seizure monitoring while they explored a virtual environment containing teleporters. Critically, this manipulation allowed patients to experience movement through space in the absence of visual and self-motion cues. The prevalence and duration of low-frequency hippocampal oscillations were unchanged by this manipulation, indicating that sensorimotor processing was not required to elicit them during navigation. Furthermore, the frequency-wise pattern of oscillation prevalence during teleportation contained spatial information capable of classifying the distance teleported. These results demonstrate that movement-related sensory information is not required to drive spatially informative low-frequency hippocampal oscillations during navigation and suggest a specific function in memory-related spatial updating.