Neuronal sequences during theta rely on behavior-dependent spatial maps

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Abstract

Navigation through space involves learning and representing relationships between past, current and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations provided by neuronal sequences start behind the animal's true location and then sweep forward. However, the exact relationship between theta phase, represented position and true location remains unclear and even paradoxical. Here, we formalize previous notions of 'spatial' or 'temporal' theta sweeps that have appeared in the literature. We analyze single-cell and population variables in unit recordings from rat CA1 place cells and compare them to model simulations based on each of these schemes. We show that neither spatial nor temporal sweeps quantitatively accounts for how all relevant variables change with running speed. To reconcile these schemes with our observations, we introduce 'behavior-dependent' sweeps, in which theta sweep length and place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. These behavior-dependent spatial maps provide a structured heterogeneity that is essential for understanding the hippocampal code.

Data availability

No new data was generated for this study. All analysis code has been made available at https://github.com/sencheng/models-and-analysis-of-theta-phase-coding

The following previously published data sets were used

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Eloy Parra-Barrero

Ruhr University Bochum, Bochum, Germany

Competing interests
The authors declare that no competing interests exist.
Kamran Diba

Department of Anesthesiology, University of Michigan, Ann Arbor, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5128-4478
Sen Cheng

Ruhr University Bochum, Bochum, Germany

For correspondence
sen.cheng@rub.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-6719-8029

Funding

German Research Foundation (419037518 - FOR 2812,P2)

Sen Cheng

German Federal Ministry of Education and Research (01GQ1506)

Sen Cheng

National Institute of Mental Health (NIMH R01MH109170)

Kamran Diba

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.