Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms

  1. Colin T Kyle
  2. Jared D Stokes
  3. Jennifer S Lieberman
  4. Abdul S Hassan
  5. Arne D Ekstrom  Is a corresponding author
  1. University of California, Davis, United States

Abstract

The rodent hippocampus represents different spatial environments distinctly via changes in the pattern of "place cell" firing. It remains unclear, though, how spatial remapping in rodents relates more generally to human memory. Here participants retrieved four virtual reality environments with repeating or novel landmarks and configurations during high-resolution functional magnetic resonance imaging (fMRI). Both neural decoding performance and neural pattern similarity measures revealed environment-specific hippocampal neural codes. Conversely, an interfering spatial environment did not elicit neural codes specific to that environment, with neural activity patterns instead resembling those of competing environments, an effect linked to lower retrieval performance. We find that orthogonalized neural patterns accompany successful disambiguation of spatial environments while erroneous reinstatement of competing patterns characterized interference errors. These results provide the first evidence for environment-specific neural codes in the human hippocampus, suggesting that pattern separation/completion mechanisms play an important role in how we successfully retrieve memories.

Article and author information

Author details

  1. Colin T Kyle

    Center for Neuroscience, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jared D Stokes

    Department of Psychology, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Jennifer S Lieberman

    Center for Neuroscience, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Abdul S Hassan

    Center for Neuroscience, University of California, Davis, Davis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Arne D Ekstrom

    Department of Psychology, University of California, Davis, Davis, United States
    For correspondence
    adekstrom@ucdavis.edu
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

Ethics

Human subjects: This study was approved by the Institutional Review Board at the University of California at Davis. Written informed consent was obtained from each participant before the experiment.

Version history

  1. Received: July 31, 2015
  2. Accepted: November 26, 2015
  3. Accepted Manuscript published: November 27, 2015 (version 1)
  4. Version of Record published: January 19, 2016 (version 2)

Copyright

© 2015, Kyle et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Colin T Kyle
  2. Jared D Stokes
  3. Jennifer S Lieberman
  4. Abdul S Hassan
  5. Arne D Ekstrom
(2015)
Successful retrieval of competing spatial environments in humans involves hippocampal pattern separation mechanisms
eLife 4:e10499.
https://doi.org/10.7554/eLife.10499

Share this article

https://doi.org/10.7554/eLife.10499

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