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

• Published in: Neuron (Cambridge, Mass.) Vol. 109; no. 19; pp. 3149 - 3163.e6
• Main Authors: Gillespie, Anna K., Astudillo Maya, Daniela A., Denovellis, Eric L., Liu, Daniel F., Kastner, David B., Coulter, Michael E., Roumis, Demetris K., Eden, Uri T., Frank, Loren M.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 06.10.2021
• Subjects: Algorithms; Animals; Choice Behavior - physiology; Conditioning, Operant; consolidation; decoding; Electrodes, Implanted; Goals; hippocampus; Hippocampus - physiology; learning; Linear Models; Male; Maze Learning; memory; Memory - physiology; navigation; planning; Rats; Rats, Long-Evans; replay; sharp wave ripples; Space Perception - physiology; planning; navigation; memory; hippocampus; sharp wave ripples; learning; replay; consolidation; decoding
• ISSN: 0896-6273; 1097-4199; 1097-4199
• DOI: 10.1016/j.neuron.2021.07.029

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. [Display omitted] •Replay does not reliably represent the upcoming path of the subject•Replay tends to represent previous goals and non-recently visited locations•Replay is poorly suited to guiding immediately subsequent behavior•Replay is better suited to storing and updating representations of past experience Gillespie et al. find that hippocampal replay does not reliably relate to immediately subsequent choice in a spatial memory task. Instead, replay preferentially represents previous goals and places that have not been visited recently, suggesting a role in storing and updating memories rather than in directly guiding upcoming behavior.