Neuron
Volume 101, Issue 1, 2 January 2019, Pages 119-132.e4
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Article
Assembly Responses of Hippocampal CA1 Place Cells Predict Learned Behavior in Goal-Directed Spatial Tasks on the Radial Eight-Arm Maze

https://doi.org/10.1016/j.neuron.2018.11.015Get rights and content
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Highlights

  • Place cells gradually move their firing fields toward newly learned rewards

  • Task-contingent firing is influenced by goal novelty during reference memory update

  • In reference memory tasks, trajectory replay predicts future arm at decision point

  • In the pure working memory task, trajectory replay encodes previously visited arm

Summary

Hippocampus is needed for both spatial working and reference memories. Here, using a radial eight-arm maze, we examined how the combined demand on these memories influenced CA1 place cell assemblies while reference memories were partially updated. This was contrasted with control tasks requiring only working memory or the update of reference memory. Reference memory update led to the reward-directed place field shifts at newly rewarded arms and to the gradual strengthening of firing in passes between newly rewarded arms but not between those passes that included a familiar-rewarded arm. At the maze center, transient network synchronization periods preferentially replayed trajectories of the next chosen arm in reference memory tasks but the previously visited arm in the working memory task. Hence, reference memory demand was uniquely associated with a gradual, goal novelty-related reorganization of place cell assemblies and with trajectory replay that reflected the animal’s decision of which arm to visit next.

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Present address: Kirby Neurobiology Center, Harvard Medical School, Boston, MA 02115, USA

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Present address: Department of Biochemistry, Institute of Biology, Eötvös Loránd University, Budapest 1117, Hungary

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Present address: School of Psychology, Cardiff University, Cardiff CF10 3AT, UK

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