Constant Sub-second Cycling between Representations of Possible Futures in the Hippocampus

Kenneth Kay; Jason E Chung; Marielena Sosa; Jonathan S Schor; Mattias P Karlsson; Margaret C Larkin; Daniel F Liu; Loren M Frank

doi:10.1016/j.cell.2020.01.014

Constant Sub-second Cycling between Representations of Possible Futures in the Hippocampus

Cell. 2020 Feb 6;180(3):552-567.e25. doi: 10.1016/j.cell.2020.01.014. Epub 2020 Jan 30.

Authors

Kenneth Kay¹, Jason E Chung², Marielena Sosa², Jonathan S Schor³, Mattias P Karlsson², Margaret C Larkin², Daniel F Liu², Loren M Frank⁴

Affiliations

¹ Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Physiology, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address: kk3291@columbia.edu.
² Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Physiology, University of California, San Francisco, San Francisco, CA 94158, USA.
³ Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA.
⁴ Kavli Institute for Fundamental Neuroscience, University of California, San Francisco, San Francisco, CA 94158, USA; Department of Physiology, 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

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

Publication types

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

MeSH terms

Action Potentials / physiology
Animals
Behavior, Animal / physiology*
Cognition / physiology*
Decision Making / physiology*
Hippocampus / physiology*
Locomotion / physiology
Male
Maze Learning / physiology
Nerve Net / physiology
Neurons / physiology
Rats
Rats, Long-Evans
Theta Rhythm / physiology

Abstract

Publication types

MeSH terms

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