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  Multivoxel pattern analysis reveals 3D place information in the human hippocampus

Kim, M., Jeffery, K., & Maguire, E. (2017). Multivoxel pattern analysis reveals 3D place information in the human hippocampus. The Journal of Neuroscience, 37(16), 4270-4279. doi:10.1523/JNEUROSCI.2703-16.2017.

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Item Permalink: http://hdl.handle.net/21.11116/0000-0004-9C27-1 Version Permalink: http://hdl.handle.net/21.11116/0000-0004-D822-2
Genre: Journal Article

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 Creators:
Kim, Misun1, Author              
Jeffery, Kate2, Author
Maguire, Eleanor1, Author
Affiliations:
1Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, United Kingdom, ou_persistent22              
2Institute of Behavioural Neuroscience, University College London, United Kingdom, ou_persistent22              

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Free keywords: 3D; Hippocampus; Isotropic; Navigation; Retrosplenial; Virtual reality
 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.

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Language(s): eng - English
 Dates: 2017-01-102016-08-162017-02-132017-04-192017-04-19
 Publication Status: Published in print
 Pages: -
 Publishing info: -
 Table of Contents: -
 Rev. Type: Peer
 Identifiers: DOI: 10.1523/JNEUROSCI.2703-16.2017
PMID: 28320847
PMC: PMC5413175
Other: Epub 2017
 Degree: -

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Project name : -
Grant ID : 101759/Z/13/Z ; 102263/Z/13/Z ; 091593/Z/10/Z
Funding program : -
Funding organization : Wellcome Trust
Project name : -
Grant ID : WT103896AIA
Funding program : -
Funding organization : Wellcome Trust
Project name : -
Grant ID : BB/J009792/1
Funding program : -
Funding organization : Biotechnology and Biological Sciences Research Council (BBSRC)
Project name : -
Grant ID : -
Funding program : Samsung doctoral studentship
Funding organization : Samsung

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Title: The Journal of Neuroscience
  Other : The Journal of Neuroscience: the Official Journal of the Society for Neuroscience
  Abbreviation : J. Neurosci.
Source Genre: Journal
 Creator(s):
Affiliations:
Publ. Info: Washington, DC : Society of Neuroscience
Pages: - Volume / Issue: 37 (16) Sequence Number: - Start / End Page: 4270 - 4279 Identifier: ISSN: 0270-6474
CoNE: https://pure.mpg.de/cone/journals/resource/954925502187_1