Flexible theta sequence compression mediated via phase precessing interneurons

  1. Angus Chadwick
  2. Mark CW van Rossum  Is a corresponding author
  3. Matthew F Nolan  Is a corresponding author
  1. Sainsbury Wellcome Centre, University College London, United Kingdom
  2. University of Edinburgh, United Kingdom

Abstract

Encoding of behavioral episodes as spike sequences during hippocampal theta oscillations provides a neural substrate for computations on events extended across time and space. However, the mechanisms underlying the numerous and diverse experimentally observed properties of theta sequences remain poorly understood. Here we account for theta sequences using a novel model constrained by the septo-hippocampal circuitry. We show that when spontaneously active interneurons integrate spatial signals and theta frequency pacemaker inputs, they generate phase precessing action potentials that can coordinate theta sequences in place cell populations. We reveal novel constraints on sequence generation, predict cellular properties and neural dynamics that characterize sequence compression, identify circuit organization principles for high capacity sequential representation, and show that theta sequences can be used as substrates for association of conditioned stimuli with recent and upcoming events. Our results suggest mechanisms for flexible sequence compression that are suited to associative learning across an animal's lifespan.

Article and author information

Author details

  1. Angus Chadwick

    Gatsby Computational Neuroscience Unit, Sainsbury Wellcome Centre, University College London, London, United Kingdom
    Competing interests
    No competing interests declared.
  2. Mark CW van Rossum

    Centre for Integrative Physiology, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    mvanross@inf.ed.ac.uk
    Competing interests
    Mark CW van Rossum, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6525-6814
  3. Matthew F Nolan

    Centre for Integrative Physiology, University of Edinburgh, Edinburgh, United Kingdom
    For correspondence
    mattnolan@ed.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1062-6501

Funding

Engineering and Physical Sciences Research Council (EP/F500385/1)

  • Angus Chadwick
  • Mark CW van Rossum

Biotechnology and Biological Sciences Research Council (BB/L010496/1)

  • Matthew F Nolan

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

Reviewing Editor

  1. Frances K Skinner, University Health Network, Canada

Publication history

  1. Received: August 9, 2016
  2. Accepted: December 7, 2016
  3. Accepted Manuscript published: December 8, 2016 (version 1)
  4. Version of Record published: January 19, 2017 (version 2)

Copyright

© 2016, Chadwick 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. Angus Chadwick
  2. Mark CW van Rossum
  3. Matthew F Nolan
(2016)
Flexible theta sequence compression mediated via phase precessing interneurons
eLife 5:e20349.
https://doi.org/10.7554/eLife.20349

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