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

Kim, M; Jeffery, KJ; Maguire, EA; (2017) Multivoxel Pattern Analysis Reveals 3D Place Information in the Human Hippocampus. J Neurosci , 37 (16) pp. 4270-4279. 10.1523/JNEUROSCI.2703-16.2017. Green open access

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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.

Type: Article
Title: Multivoxel Pattern Analysis Reveals 3D Place Information in the Human Hippocampus.
Location: United States
Open access status: An open access version is available from UCL Discovery
DOI: 10.1523/JNEUROSCI.2703-16.2017
Publisher version: http://dx.doi.org/10.1523/JNEUROSCI.2703-16.2017
Language: English
Additional information: Copyright © 2017 Kim et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in anymedium providedthatthe original work is properly attributed.
Keywords: 3D, hippocampus, isotropic, navigation, retrosplenial, virtual reality, Adult, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Space Perception, Spatial Behavior
UCL classification: UCL > Provost and Vice Provost Offices
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Div of Psychology and Lang Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > Div of Psychology and Lang Sciences > Experimental Psychology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Brain Sciences > UCL Queen Square Institute of Neurology > Imaging Neuroscience
URI: http://discovery.ucl.ac.uk/id/eprint/1547089
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