Navigating in a three-dimensional world

Jeffery, Kate J.; Jovalekic, Aleksandar; Verriotis, Madeleine; Hayman, Robin

doi:10.1017/s0140525x12002476

Cited by 112 publications

(99 citation statements)

References 302 publications

(443 reference statements)

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“…Together with the behavioral findings of high accuracy regardless of the presence of a vertical or horizontal distractor and the symmetrically perceived length of the 3D environment, multivoxel representational similarity in the right aHC supports an isotropic 3D space encoding hypothesis and is evidence against the anisotropic planar encoding hypothesis (Hayman et al, 2011; Jeffery et al, 2013). …”

Section: Discussionsupporting

confidence: 60%

“…Hayman et al (2011) recorded place and grid cells in the HC and EC of rats moving on a vertical wall and helix staircase. In both apparatuses, place and grid cells expressed less information about the vertical axis, leading the investigators to propose that 3D space representation might be fundamentally planar (Jeffery et al, 2013). In contrast, most place cells recorded in CA1 of flying bats were equally sensitive to all three axes, suggesting isotropic representation of 3D space (Yartsev and Ulanovsky, 2013; for review, see Finkelstein et al, 2016; for a review of fish behavior in 3D, see Burt de Perera et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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

2017

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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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Section: Discussionsupporting

confidence: 60%

Section: Introductionmentioning

confidence: 99%

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

2017

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“…In a three-dimensional world with rich topography, vertically extended surfaces should not be ignored (for a review on navigation in 3D, see Jeffery et al 2013). Terrain slope provides surface-traveling animals with a directional spatial cue that aids navigation in large-scale environments.…”

Section: Discussionmentioning

confidence: 99%

Sex differences and errors in the use of terrain slope for navigation

et al. 2015

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Unlike most of the spatial cues that have received attention, a sloping terrain can be perceived by multimodal sensory inputs (vision, balance, and kinesthesia), making it potentially very salient for navigation. Furthermore, a homogeneous slope can be used like a compass to identify directions (e.g., uphill, downhill, and sideways), but not to determine distances. We briefly review recent evidence on navigation with slope, emphasizing two main findings. On the one hand, we focus on the conspicuous sex difference found in the ability to localize a target in a square, tilted enclosure; this has emerged in human adults and children, and we suggest that it is related to lower awareness of the slope for females. On the other hand, we describe the general pattern of errors that arises when localizing the target during the task; these errors indicate the use of a bi-coordinate representation of the slope. Limitations and ideas for future studies are proposed.

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“…This finding will undoubtedly prompt a careful re-examination of head-direction cells in rodents, and fresh investigations in other species. Other mammals may use different compasses 10 , and if they do, understanding what drives the differences between species (whether they are hard-wired at birth or develop with experience) will lead to insight into the basic principles of the system. ■ …”

Section: A Three-dimensional Neural Compassmentioning

confidence: 99%