Rats are able to navigate in virtual environments

Hölscher, Christian; Schnee, Alexander; Dahmen, Hansjürgen; Setia, Lokesh; Mallot, Hanspeter A.

doi:10.1242/jeb.01371

Cited by 173 publications

(193 citation statements)

References 19 publications

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“…In contrast, in two-dimensional random foraging in VR with or without pillars, the distal visual cues are not paired repeatedly with any other cue, leading to a lack of spatial selectivity. Contrary to our VR system and results, a recent study found that during twodimensional random foraging in a VR system allowing full, 360° body rotation 35,37 , hippocampal neurons showed intact spatial selectivity 37 . This result could arise solely from the presence of a larger range of vestibular cues, which were diminished in our study; however, this explanation is incompatible with the presence of spatial selectivity in our tasks involving systematic paths.…”

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Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

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During real-world (RW) exploration, rodent hippocampal activity shows robust spatial selectivity, which is hypothesized to be governed largely by distal visual cues, although other sensory-motor cues also contribute. Indeed, hippocampal spatial selectivity is weak in primate and human studies that use only visual cues. To determine the contribution of distal visual cues only, we measured hippocampal activity from body-fixed rodents exploring a two-dimensional virtual reality (VR). Compared to that in RW, spatial selectivity was markedly reduced during random foraging and goal-directed tasks in VR. Instead we found small but significant selectivity to distance traveled. Despite impaired spatial selectivity in VR, most spikes occurred within ~2-s-long hippocampal motifs in both RW and VR that had similar structure, including phase precession within motif fields. Selectivity to space and distance traveled were greatly enhanced in VR tasks with stereotypical trajectories. Thus, distal visual cues alone are insufficient to generate a robust hippocampal rate code for space but are sufficient for a temporal code. npg © 2015 Nature America, Inc. All rights reserved.1 2 2 VOLUME 18 | NUMBER 1 | JANUARY 2015 nature neurOSCIenCe a r t I C l e S same physical location in space can be approached from multiple different directions at different speeds. We thus investigated the contribution of distal visual cues only in determining selectivity in such an experimental setup. RESULTS Nature of spatial selectivity of hippocampal responsesWe measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a). In VR, the rats were body-fixed, i.e., their bodies were held in place, with a harness on a floating ball, allowing for head movements but precluding full-body turns, thus minimizing vestibular cues (Online Methods) 21,36 . Rats quickly learned to avoid the virtual edges entirely on the basis of visual cues 36 and spent a similar amount of time away from the edges and in the center of the platform (Fig. 1a) compared to in RW. We measured the activity of 1,066 and 1,238 principal neurons in RW and VR, respectively, in the dorsal CA1 of four rats under a variety of conditions (Online Methods). Neurons fired vigorously in restricted regions of space in RW, as expected (Fig. 1b,c, Supplementary Fig. 1a and Supplementary Video 1) 1 . In contrast, the neurons showed little spatial selectivity in VR during random foraging (Fig. 1b,d and Supplementary Fig. 1b).Across the ensemble, neurons had moderately reduced (25%) mean firing rates but greatly reduced (68%) peak firing rates in VR ( Fig. 2a and Supplementary Fig. 2a). Neurons in VR also had greatly reduced spatial information content (75%), stability (59%), sparsity (42%) and coherence (40%) (Fig. 2b-d and Supplementary Fig. 2b,c) compared to spatially localized, stable and sparse RW rate maps (Fig. 2c). Although the mean firing rate was inversely correlated with information content (Supplementary Fig. 2d)...

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“…We measured hippocampal activity during a two-dimensional randomforaging task in RW and VR [35][36][37] with similar distal visual cues (Fig. 1a).…”

Section: Nature Of Spatial Selectivity Of Hippocampal Responsesmentioning

confidence: 99%

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

et al. 2014

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“…resent position. Another possibility is recordings in a virtual reality setting, where the available space for exploration is infinite (Holscher et al, 2005;Dombeck et al, 2007).…”

Section: Open Questionsmentioning

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Grid cells: The position code, neural network models of activity, and the problem of learning

2008

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ABSTRACT:We review progress on the modeling and theoretical fronts in the quest to unravel the computational properties of the grid cell code and to explain the mechanisms underlying grid cell dynamics. The goals of the review are to outline a coherent framework for understanding the dynamics of grid cells and their representation of space; to critically present and draw contrasts between recurrent network models of grid cells based on continuous attractor dynamics and independentneuron models based on temporal interference; and to suggest open questions for experiment and theory. V

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“…However, there is no agreement on which is more important and how these signals combine to generate spatially localized place cell firing and its temporal organization with respect to the theta rhythm (24). Recent studies showed that mice could navigate in a virtual environment (VE) and a small sample of place cells has been recorded in mice running on a virtual linear track (25)(26)(27). VE affords the opportunity to isolate the visual environment and internal movement-related information from other sensory information, and to study their contributions to place cell firing.…”

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How vision and movement combine in the hippocampal place code

Chen¹,

King

Burgess

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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How do external environmental and internal movement-related information combine to tell us where we are? We examined the neural representation of environmental location provided by hippocampal place cells while mice navigated a virtual reality environment in which both types of information could be manipulated. Extracellular recordings were made from region CA1 of head-fixed mice navigating a virtual linear track and running in a similar real environment. Despite the absence of vestibular motion signals, normal place cell firing and theta rhythmicity were found. Visual information alone was sufficient for localized firing in 25% of place cells and to maintain a local field potential theta rhythm (but with significantly reduced power). Additional movement-related information was required for normally localized firing by the remaining 75% of place cells. Trials in which movement and visual information were put into conflict showed that they combined nonlinearly to control firing location, and that the relative influence of movement versus visual information varied widely across place cells. However, within this heterogeneity, the behavior of fully half of the place cells conformed to a model of path integration in which the presence of visual cues at the start of each run together with subsequent movement-related updating of position was sufficient to maintain normal fields. Hippocampal place cells fire when the animal visits a specific area in a familiar environment (1), providing a population representation of self-location (2-4). However, it is still unclear what information determines their firing location ("place field"). Existing models suggest that movement-related information updates the representation of self-location from moment-to-moment (i.e., performing "path integration"), whereas environmental information provides initial localization and allows the accumulating error inherent in path integration to be corrected sporadically (5-13). Previous experimental work addressing this question has found it difficult to dissociate the different types of information available in the real world. Both external sensory cues (3, 14-16) and internal self-motion information (17-19) can influence place cell firing, but these have usually been tightly coupled in previous experiments.To date, a range of computational models predicting place fields has been proposed based on the assumption that either environmental sensory information (20-22) or a self-motion metric is fundamental (7, 23). However, there is no agreement on which is more important and how these signals combine to generate spatially localized place cell firing and its temporal organization with respect to the theta rhythm (24). Recent studies showed that mice could navigate in a virtual environment (VE) and a small sample of place cells has been recorded in mice running on a virtual linear track (25)(26)(27). VE affords the opportunity to isolate the visual environment and internal movement-related information from other sensory information, and to study t...

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Rats are able to navigate in virtual environments

Cited by 173 publications

References 19 publications

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Impaired spatial selectivity and intact phase precession in two-dimensional virtual reality

Grid cells: The position code, neural network models of activity, and the problem of learning

How vision and movement combine in the hippocampal place code

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