Article | Published:

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

Nature Neuroscience volume 18, pages 121128 (2015) | Download Citation

Abstract

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.

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Acknowledgements

We thank F. Quezada and B. Popeney for help with behavioral training, F. Quezada for help with spike sorting, N. Agarwal for help with electrophysiology, B. Willers for help with the analyses, P. Ravassard and A. Kees for help with surgeries, technical support and manuscript comments, D. Aharoni for help with hardware and the participants of the Kavli Institute for Theoretical Physics workshop on 'Neurophysics of Space, Time and Learning' for discussions. This work was supported by grants to M.R.M. from the US National Institutes of Health (5R01MH092925-02) and the W.M. Keck foundation. Results presented in this manuscript were uploaded on a preprint server BioRxiv in December 2013 at http://dx.doi.org/10.1101/001636.

Author information

Author notes

    • Zahra M Aghajan
    •  & Lavanya Acharya

    These authors contributed equally to this work.

Affiliations

  1. W.M. Keck Center for Neurophysics, Integrative Center for Learning and Memory, and Brain Research Institute, University of California at Los Angeles, Los Angeles, California, USA.

    • Zahra M Aghajan
    • , Lavanya Acharya
    • , Jason J Moore
    • , Jesse D Cushman
    • , Cliff Vuong
    •  & Mayank R Mehta
  2. Department of Physics and Astronomy, University of California at Los Angeles, Los Angeles, California, USA.

    • Zahra M Aghajan
    • , Jesse D Cushman
    • , Cliff Vuong
    •  & Mayank R Mehta
  3. Biomedical Engineering Interdepartmental Program, University of California at Los Angeles, Los Angeles, California, USA.

    • Lavanya Acharya
  4. Neuroscience Interdepartmental Program, University of California at Los Angeles, Los Angeles, California, USA.

    • Jason J Moore
    •  & Mayank R Mehta
  5. Department of Neurology, University of California at Los Angeles, Los Angeles, California, USA.

    • Mayank R Mehta
  6. Department of Neurobiology, University of California at Los Angeles, Los Angeles, California, USA.

    • Mayank R Mehta

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Contributions

L.A., J.D.C., Z.M.A. and M.R.M. designed the experiments. L.A., C.V. and J.D.C. performed the experiments. Z.M.A. and J.J.M. performed analyses with input from M.R.M. Z.M.A., L.A., J.J.M. and M.R.M. wrote the manuscript with input from other authors.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Mayank R Mehta.

Integrated supplementary information

Supplementary information

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  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–10

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    Supplementary Methods Checklist

Videos

  1. 1.

    RW Random Foraging: Spatial Selectivity.

    Animation of experimental data when a rat was performing the RW random foraging task during a representative session with spikes from a place cell overlaid over the rat's trajectory. The rat's position is represented by the moving grey shape. The light blue trace corresponds to the trajectory of the rat and the dark blue dots indicate where the spikes occurred. Note that the activity of the neuron is composed of motifs that occur in a restricted region of space.

  2. 2.

    VR Random-Pillar: No Spatial Selectivity.

    Animation of experimental data when a rat was performing the VR random-pillar task during a representative session with spikes from a putative pyramidal neuron overlaid over the rat's trajectory. The rat's position in virtual space is represented by the moving grey shape. The light brown trace corresponds to the trajectory of the rat and the dark brown dots indicate where the spikes occurred. Note that the activity of the neuron is composed of motifs that are distributed nearly randomly in space.

  3. 3.

    VR Systematic-Pillar: Place Code.

    Animation of experimental data when a rat was performing the VR systematic-pillar task during a representative session with recorded spikes from a putative pyramidal neuron overlaid over the rat's trajectory. The rat's position is represented by the moving grey shape. The light green trace corresponds to the trajectory of the rat and the dark green dots indicate where the spikes occurred. Note that the activity of the neuron is composed of motifs which occur in a restricted region of space on only on one of the three arms of the triangular path followed by the rat.

  4. 4.

    VR Systematic-Pillar: Disto-Code.

    Animation of experimental data when a rat was performing the VR systematic-pillar task during a representative session with spikes from a recorded putative pyramidal neuron overlaid over the rat's trajectory. The rat's position is represented by the moving grey shape. The light green trace corresponds to the trajectory of the rat and the dark green dots indicate where the spikes occurred. Note that the activity of the neuron is composed of motifs which occur in restricted regions of space at the same distance along all the three arms of the triangular path of the rat.

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DOI

https://doi.org/10.1038/nn.3884