Hippocampal replay reflects specific past experiences rather than a plan for subsequent choice

Anna K Gillespie; Daniela A Astudillo Maya; Eric L Denovellis; Daniel F Liu; David B Kastner; Michael E Coulter; Demetris K Roumis; Uri T Eden; Loren M Frank

doi:10.1016/j.neuron.2021.07.029

Hippocampal replay reflects specific past experiences rather than a plan for subsequent choice

Neuron. 2021 Oct 6;109(19):3149-3163.e6. doi: 10.1016/j.neuron.2021.07.029. Epub 2021 Aug 26.

Authors

Anna K Gillespie¹, Daniela A Astudillo Maya², Eric L Denovellis³, Daniel F Liu², David B Kastner², Michael E Coulter², Demetris K Roumis³, Uri T Eden⁴, Loren M Frank⁵

Affiliations

¹ Departments of Physiology and Psychiatry, University of California, San Francisco, San Francisco, CA 94158, USA; Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address: anna.gillespie@ucsf.edu.
² Departments of Physiology and Psychiatry, University of California, San Francisco, San Francisco, CA 94158, USA; Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA.
³ Departments of Physiology and Psychiatry, University of California, San Francisco, San Francisco, CA 94158, USA; Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA 94158, USA.
⁴ Department of Mathematics and Statistics, Boston University, Boston, MA 02215, USA.
⁵ Departments of Physiology and Psychiatry, University of California, San Francisco, San Francisco, CA 94158, USA; Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Howard Hughes Medical Institute, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address: loren@phy.ucsf.edu.

Abstract

Executing memory-guided behavior requires storage of information about experience and later recall of that information to inform choices. Awake hippocampal replay, when hippocampal neural ensembles briefly reactivate a representation related to prior experience, has been proposed to critically contribute to these memory-related processes. However, it remains unclear whether awake replay contributes to memory function by promoting the storage of past experiences, facilitating planning based on evaluation of those experiences, or both. We designed a dynamic spatial task that promotes replay before a memory-based choice and assessed how the content of replay related to past and future behavior. We found that replay content was decoupled from subsequent choice and instead was enriched for representations of previously rewarded locations and places that had not been visited recently, indicating a role in memory storage rather than in directly guiding subsequent behavior.

Keywords: consolidation; decoding; hippocampus; learning; memory; navigation; planning; replay; sharp wave ripples.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Algorithms
Animals
Choice Behavior / physiology*
Conditioning, Operant
Electrodes, Implanted
Goals
Hippocampus / physiology*
Linear Models
Male
Maze Learning
Memory / physiology*
Rats
Rats, Long-Evans
Space Perception / physiology*

Abstract

Publication types

MeSH terms

Grants and funding