Uncovering temporal structure in hippocampal output patterns

  1. Kourosh Maboudi
  2. Etienne Ackermann
  3. Laurel Watkins de Jong
  4. Brad Pfeiffer
  5. David Foster
  6. Kamran Diba  Is a corresponding author
  7. Caleb Kemere  Is a corresponding author
  1. University of Michigan, United States
  2. Rice University, United States
  3. University of Texas Southwestern, United States
  4. University of California, Berkeley, United States

Abstract

Place cell activity of hippocampal pyramidal cells has been described as the cognitive substrate of spatial memory. Replay is observed during hippocampal sharp-wave-ripple-associated population burst events (PBEs) and is critical for consolidation and recall-guided behaviors. PBE activity has historically been analyzed as a phenomenon subordinate to the place code. Here, we use hidden Markov models to study PBEs observed in rats during exploration of both linear mazes and open fields. We demonstrate that estimated models are consistent with a spatial map of the environment, and can even decode animals' positions during behavior. Moreover, we demonstrate the model can be used to identify hippocampal replay without recourse to the place code, using only PBE model congruence. These results suggest that downstream regions may rely on PBEs to provide a substrate for memory. Additionally, by forming models independent of animal behavior, we lay the groundwork for studies of non-spatial memory.

Data availability

We analyzed data from neural recording experiments. Data for Figures 1-5 has been previously reported in [1]. These data and also data for Figure 8 are available from Kamran Diba on request. Data for Figure 6 was previously reported in [2] and is available from Brad Pfeiffer and David Foster on request. Data for Figure 7 was previously reported in [3] is available from the CRCNS.org archive ('hc-6'). [1] Diba and Buzsaki, Nature Neuroscience, 2007 [2] Pfeiffer and Foster, Science, 2015 [3] Karlsson and Frank, Nature Neuroscience, 2009.All analysis code and sample recording epochs for Figures 1-7 are available on https://github.com/kemerelab/UncoveringTemporalStructureHippocampus. These make use of our broader open-source Python analysis software https://github.com/nelpy.

The following previously published data sets were used

Article and author information

Author details

  1. Kourosh Maboudi

    Department of Anesthesiology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Etienne Ackermann

    Department of Electrical and Computer Engineering, Rice University, Houston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Laurel Watkins de Jong

    Department of Anesthesiology, University of Michigan, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Brad Pfeiffer

    Department of Neuroscience, University of Texas Southwestern, Dallas, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. David Foster

    Department of Psychology, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Kamran Diba

    Department of Anesthesiology, University of Michigan, Ann Arbor, United States
    For correspondence
    kdiba@umich.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5128-4478
  7. Caleb Kemere

    Department of Electrical and Computer Engineering, Rice University, Houston, United States
    For correspondence
    caleb.kemere@rice.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2054-0234

Funding

National Science Foundation (IOS-1550994)

  • Etienne Ackermann
  • Caleb Kemere

Human Frontier Science Program (RGY0088)

  • Etienne Ackermann
  • Caleb Kemere

Ken Kennedy Institute (ERIT)

  • Caleb Kemere

National Institute of Mental Health (R01MH109170)

  • Kourosh Maboudi
  • Kamran Diba

National Institute of Mental Health (R01MH085823)

  • Brad Pfeiffer
  • David Foster

Alfred P. Sloan Foundation

  • Brad Pfeiffer
  • David Foster

Brain and Behavior Research Foundation (NARSAD Young Investigator Grant)

  • Brad Pfeiffer
  • David Foster

McKnight Endowment Fund for Neuroscience

  • David Foster

National Science Foundation (CBET-1351692)

  • Etienne Ackermann

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: As reported previously, all procedures were approved by the Johns Hopkins University, Rutgers University, and University of California, San Francisco Animal Care and Use Committees and followed US National Institutes of Health animal use guidelines (protocol 90-042).

Reviewing Editor

  1. Laura Colgin, The University of Texas at Austin, Center for Learning and Memory, United States

Publication history

  1. Received: December 20, 2017
  2. Accepted: May 14, 2018
  3. Accepted Manuscript published: June 5, 2018 (version 1)
  4. Version of Record published: June 21, 2018 (version 2)

Copyright

© 2018, Maboudi 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. Kourosh Maboudi
  2. Etienne Ackermann
  3. Laurel Watkins de Jong
  4. Brad Pfeiffer
  5. David Foster
  6. Kamran Diba
  7. Caleb Kemere
(2018)
Uncovering temporal structure in hippocampal output patterns
eLife 7:e34467.
https://doi.org/10.7554/eLife.34467

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