A neural compass in the human brain during naturalistic virtual navigation

A central component of wayfinding is the ability to maintain a consistent representation of one's facing direction when moving about the world. In rodents, head direction cells are believed to support this "neural compass", but identifying a similar mechanism in humans during dynamic naturalistic navigation has been challenging. To address this issue, we acquired fMRI data from male and female human participants while they freely navigated through a virtual reality city. Encoding model analyses revealed voxel clusters in posterior-medial cortex (the "retrosplenial complex") and superior parietal lobule that exhibited reliable tuning as a function of facing direction. Crucially, these directional tunings were consistent across perceptually different versions of the city, spatially separated locations within the city, and motivationally distinct phases of the behavioral task. Analysis of the model weights indicated that these regions represent a broad range of possible facing directions, and that they do so by representing heading relative to the principal axis of the environment. These findings reveal specific mechanisms in the human brain that allow us to maintain a sense of direction during naturalistic, dynamic navigation.Significance statement Theories of spatial navigation posit the existence of a "neural compass" that maintains one's sense of direction when moving through the world. Head direction cells are believed to support this representation in rodents, but it has been challenging to identify a similar signal in humans using noninvasive methods. We use an encoding model analysis of fMRI data to show that two brain regions-retrosplenial complex and superior parietal lobe-represent facing direction when people perform a naturalistic task in which they dynamically navigate through a virtual-reality city. Crucially, this directional signal is stable across versions of the city with different visual features, locations within the city, and phases of the behavioral task, thus exhibiting key characteristics of a "neural compass."