1. Neuroscience
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Synchronized excitability in a network enables generation of internal neuronal sequences

  1. Wang Yingxue
  2. Zachary Roth
  3. Eva Pastalkova  Is a corresponding author
  1. Janelia Farm Research Campus, Howard Hughes Medical Institute, United States
Research Article
  • Cited 14
  • Views 2,837
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Cite this article as: eLife 2016;5:e20697 doi: 10.7554/eLife.20697

Abstract

Hippocampal place field sequences are supported by sensory cues and network internal mechanisms. In contrast, sharp-wave (SPW) sequences, theta sequences and episode-field sequences are internally generated. The relationship of these sequences to memory is unclear. SPW sequences have been shown to support learning and have been assumed to also support episodic memory. Conversely, we demonstrate these SPW sequences were present even after episodic memory in trained rats was impaired and after other internal sequences - episode-field and theta sequences - were eliminated. SPW sequences did not support memory despite continuing to 'replay' all task-related sequences - place-field and episode-field sequences. Sequence replay occurred selectively during a synchronous increase of population excitability -- SPWs. Similarly, theta sequences depended on the presence of repeated synchronized waves of excitability - theta oscillations. Thus, we suggest that either intermittent or rhythmic synchronized changes of excitability trigger sequential firing of neurons, which in turn supports learning and/or memory.

Article and author information

Author details

  1. Wang Yingxue

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Zachary Roth

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Eva Pastalkova

    Janelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    pastak@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.

Funding

Howard Hughes Medical Institute

  • Wang Yingxue
  • Zachary Roth

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

Ethics

Animal experimentation: All of the animals were handled according to approved institutional animal care and use committee (IACUC) of Janelia Research Campus, HHMI: protocols 10-59 and #13-96.

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

Publication history

  1. Received: August 17, 2016
  2. Accepted: September 13, 2016
  3. Accepted Manuscript published: September 28, 2016 (version 1)
  4. Version of Record published: November 1, 2016 (version 2)
  5. Version of Record updated: January 26, 2017 (version 3)
  6. Version of Record updated: April 21, 2017 (version 4)

Copyright

© 2016, Yingxue 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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    Representations related to past experiences play a critical role in memory and decision-making processes. The rat hippocampus expresses these types of representations during sharp-wave ripple (SWR) events, and previous work identified a minority of SWRs that contain ‘replay’ of spatial trajectories at ∼20x the movement speed of the animal. Efforts to understand replay typically make multiple assumptions about which events to examine and what sorts of representations constitute replay. We therefore lack a clear understanding of both the prevalence and the range of representational dynamics associated with replay. Here, we develop a state space model that uses a combination of movement dynamics of different speeds to capture the spatial content and time evolution of replay during SWRs. Using this model, we find that the large majority of replay events contain spatially coherent, interpretable content. Furthermore, many events progress at real-world, rather than accelerated, movement speeds, consistent with actual experiences.