Hippocampal replay of experience at real-world speeds

Author:

Denovellis Eric L123ORCID,Gillespie Anna K23ORCID,Coulter Michael E23,Sosa Marielena4ORCID,Chung Jason E5,Eden Uri T6,Frank Loren M123ORCID

Affiliation:

1. Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, United States

2. Departments of Physiology and Psychiatry, University of California, San Francisco, San Francisco, United States

3. Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, United States

4. Department of Neurobiology, Stanford University School of Medicine, Stanford, United States

5. Department of Neurological Surgery, University of California, San Francisco, San Francisco, United States

6. Department of Mathematics and Statistics, Boston University, Boston, United States

Abstract

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.

Funder

Simons Foundation

Howard Hughes Medical Institute

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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