The spatial world is three-dimensional (3D), and humans and other animals move both horizontally and vertically within it. Extant neuroscientific studies have typically investigated spatial navigation on a horizontal two-dimensional plane, leaving much unknown about how 3D spatial information is represented in the brain. Specifically, horizontal and vertical information may be encoded in the same or different neural structures with equal or unequal sensitivity. Here, we investigated these possibilities using functional MRI (fMRI) while participants were passively moved within a 3D lattice structure as if riding a rollercoaster. Multivoxel pattern analysis was used to test for the existence of information relating to where and in which direction participants were heading in this virtual environment. Behaviorally, participants had similarly accurate memory for vertical and horizontal locations, and the right anterior hippocampus expressed place information that was sensitive to changes along both horizontal and vertical axes. This is suggestive of isotropic 3D place encoding. By contrast, participants indicated their heading direction faster and more accurately when they were heading in a tilted-up or tilted-down direction. This direction information was expressed in the right retrosplenial cortex and posterior hippocampus, and was only sensitive to vertical pitch, which could reflect the importance of the vertical (gravity) axis as a reference frame. Overall, our findings extend previous knowledge of how we represent the spatial world and navigate within it, by taking into account the important third dimension.
The spatial world is three-dimensional (3D) -- we can move horizontally across surfaces, but also vertically, going up slopes or stairs. Little is known about how the brain supports representations of 3D space. A key question is whether or not horizontal and vertical information is equally well represented. Here we measured functional MRI response patterns while participants moved within a virtual 3D environment, and found that the anterior hippocampus expressed location information that was sensitive to the vertical and horizontal axes. By contrast, information about heading direction, found in retrosplenial cortex and posterior hippocampus, favored the vertical axis, perhaps due to gravity effects. These findings provide new insights into how we represent our spatial 3D world and navigate within it.
The authors declare no competing financial interests.
E.A.M. is supported by a Wellcome Trust Principal Research Fellowship (101759/Z/13/Z), M.K. by a Wellcome Trust (102263/Z/13/Z) and Samsung PhD Studentship and the Centre by a Strategic Award from the Wellcome Trust (091593/Z/10/Z). K.J.J. is supported by grants from the Biotechnology and Biological Sciences Research Council (BB/J009792/1) and the Wellcome Trust (WT103896AIA)