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

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. [Display omitted] •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 Imagination, planning, and decision-making require the ability to generate representations of hypothetical experience. Kay et. al. find that neurons in the rat hippocampus can represent alternative hypothetical scenarios both regularly and quickly (every ∼125 ms). Further, the underlying activity has a temporal structure that is equivalent across different representational correlates (location and direction), implying a common process.