Hippocampus, retrosplenial and parahippocampal cortices encode multi-compartment 3D space in a hierarchical manner

Abstract

Humans commonly operate within 3D environments such as multi-floor buildings and yet there is a surprising dearth of studies that have examined how these spaces are represented in the brain. Here we had participants learn the locations of paintings within a virtual multi-level gallery building and then used behavioural tests and fMRI repetition suppression analyses to investigate how this 3D multi-compartment space was represented, and whether there was a bias in encoding vertical and horizontal information. We found faster response times for within-room egocentric spatial judgments and behavioural priming effects of visiting the same room, providing evidence for a compartmentalised representation of space. At the neural level, we observed a hierarchical encoding of 3D spatial information, with left anterior hippocampus representing local information within a room, while retrosplenial cortex, parahippocampal cortex and posterior hippocampus represented room information within the wider building. Of note, both our behavioural and neural findings showed that vertical and horizontal location information was similarly encoded, suggesting an isotropic representation of 3D space even in the context of a multi-compartment environment. These findings provide much-needed information about how the human brain supports spatial memory and navigation in buildings with numerous levels and rooms.