Multivoxel Pattern Analysis Reveals 3D Place Information in the Human Hippocampus

Abstract

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 2D 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 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 (HC) expressed place information that was sensitive to changes along both horizontal and vertical axes. This is suggestive of isotropic 3D place encoding. In 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 HC 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.SIGNIFICANCE STATEMENT The spatial world is 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 horizontal and vertical information is equally well represented. Here, we measured fMRI response patterns while participants moved within a virtual 3D environment and found that the anterior hippocampus (HC) expressed location information that was sensitive to the vertical and horizontal axes. In contrast, information about heading direction, found in retrosplenial cortex and posterior HC, 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.

Encoding of 3D head direction information in the human brain

“…Our finding of a significant correlation between vertical direction information in the RSC and behavioral accuracy might reflect the functional relevance of RSC for processing 3D direction information (although it is unclear why only vertical direction information and not horizontal direction information in this region correlated with individual differences). The dominance of vertical information in the RSC was concordant with our previous finding of vertical direction encoding when participants moved on a 3D rollercoaster (Kim et al, ). One explanation could be that visual cues might be more salient for the vertical axis compared to the horizontal axis.…”

“…The thalamus ROI was extracted from the AAL atlas (Tzourio‐Mazoyer et al, ). EC and subiculum ROIs were manually delineated on the group‐averaged MRI scans from a previous independent study on 3D space representation (Kim et al, ) following the protocol in Pruessner et al (). Although HD cells have been mainly found in presubiculum in animals, here we used a broader subiculum mask containing pre/parasubiculum because it was not feasible to distinguish these structures in our standard resolution fMRI images.…”

“…The thalamus ROI was extracted from the AAL atlas (Tzourio-Mazoyer et al, 2002). EC and subiculum ROIs were manually delineated on the group-averaged MRI scans from a previous independent study on 3D space representation (Kim et al, 2017) following the protocol in Pruessner et al (2002).…”

“…We computed visual texture similarity using the model of Renninger and Malik (2004). This visual control model was used in previous studies that investigated direction encoding (Kim et al, 2017;Sulpizio, Committeri, & Galati, 2014;Vass & Epstein, 2013).…”

Encoding of 3D head direction information in the human brain

“…These findings provide strong evidence that 3D direction information is present in the bat presubiculum which could be used to generate a mental map of 3D space. In humans, a few functional MRI (fMRI) studies have investigated the neural correlates of vertical heading (Indovina et al, 2013;Indovina et al, 2016;Kim et al, 2017), but in these studies, participants were constrained to a rollercoaster-like track and so the neural basis of complete 3D directional encoding remains unknown.…”