Cell
Volume 180, Issue 3, 6 February 2020, Pages 552-567.e25
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Article
Constant Sub-second Cycling between Representations of Possible Futures in the Hippocampus

https://doi.org/10.1016/j.cell.2020.01.014Get rights and content
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Highlights

  • Firing across hippocampal neurons can regularly “take turns” (cycle) every ∼125 ms

  • Cycle firing is seen at single-cell, cell-pair, and population levels

  • Cycle firing encodes hypothetical experience, including multiple possible futures

  • Cycle coding generalizes across representational correlates, implying common process

Summary

Cognitive faculties such as imagination, planning, and decision-making entail the ability to represent hypothetical experience. Crucially, animal behavior in natural settings implies that the brain can represent hypothetical future experience not only quickly but also constantly over time, as external events continually unfold. To determine how this is possible, we recorded neural activity in the hippocampus of rats navigating a maze with multiple spatial paths. We found neural activity encoding two possible future scenarios (two upcoming maze paths) in constant alternation at 8 Hz: one scenario per ∼125-ms cycle. Further, we found that the underlying dynamics of cycling (both inter- and intra-cycle dynamics) generalized across qualitatively different representational correlates (location and direction). Notably, cycling occurred across moving behaviors, including during running. These findings identify a general dynamic process capable of quickly and continually representing hypothetical experience, including that of multiple possible futures.

Keywords

imagination
planning
decision-making
hippocampus
synchrony
theta rhythm
place cells
CA1
CA2
CA3

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Present address: Center for Theoretical Neuroscience, Columbia University, New York, NY 10027, USA

5

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