Flexible theta sequence compression mediated via phase precessing interneurons

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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.

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Angus Chadwick

Gatsby Computational Neuroscience Unit, Sainsbury Wellcome Centre, University College London, London, United Kingdom

Competing interests
No competing interests declared.
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.

"This ORCID iD identifies the author of this article:" 0000-0001-6525-6814
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.

"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.

Copyright

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.