Abstract
Humans commonly operate within 3D environments such as multifloor 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 multilevel gallery building and then used behavioral tests and fMRI repetition suppression analyses to investigate how this 3D multicompartment 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 behavioral priming effects of visiting the same room, providing evidence for a compartmentalized 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 behavioral 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 multicompartment environment. These findings provide much-needed information about how the human brain supports spatial memory and navigation in buildings with numerous levels and rooms.
Highlights
We found significant repetition suppression effects for both “same corner, same room” and “different corner, same room” conditions compared with the “different room”
In this study we investigated how a multicompartment 3D space was represented in the human brain using behavioral testing and fMRI repetition suppression analyses
We found evidence of hierarchical encoding of this 3D spatial information, with the left anterior lateral hippocampus containing local corner information within a room, whereas retrosplenial cortex (RSC), parahippocampal cortex and posterior hippocampus contained information about the rooms within the building
Summary
The ideal method to enable navigation in 3D space would be to have a 3D compass or global positioning system (GPS) that identifies direction and distance in relation to all 3 axes in an isotropic manner. Such a 3D compass system would seem to be essential for animals who fly or swim. Behavioral experiments with fish indicated a volumetric 3D representation of space (Burt de Perera et al 2016). When an animal’s movement is restricted on the earth’s surface due to gravity, its position can be identified by 2 coordinates on that surface and a quasiplanar representation could be more efficient than a volumetric 3D representation
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