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

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.

Reviewing Editor

  1. Howard Eichenbaum, Boston University, United States

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.

Version 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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  1. Wang Yingxue
  2. Zachary Roth
  3. Eva Pastalkova
(2016)
Synchronized excitability in a network enables generation of internal neuronal sequences
eLife 5:e20697.
https://doi.org/10.7554/eLife.20697

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https://doi.org/10.7554/eLife.20697