Alternating sequences of future and past behavior encoded within hippocampal theta oscillations

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Science  09 Oct 2020:
Vol. 370, Issue 6513, pp. 247-250
DOI: 10.1126/science.abb4151

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Representing the past and the future

Adaptive behavior requires the ability to analyze experience both prospectively and retrospectively. How can forward-ordered neural activity facilitate the storage or expression of reverse-ordered sequences? Wang et al. used multitetrode recordings from many individual hippocampal CA1 neurons in rats while simultaneously recording field potentials expressing theta oscillations. Spatial representation in the place cell network oscillated between forward and backward sweeps within each theta oscillation. Backward replay was associated with theta peaks, whereas forward replay was associated with theta troughs. Most cells fell into one category, but some corresponding to deep-layer neurons showed bimodular responses. Backward replay was driven by entorhinal inputs, whereas forward replay was evoked by CA3 inputs. These are important insights into the underlying basis of coding future and past experiences.

Science, this issue p. 247


Neural networks display the ability to transform forward-ordered activity patterns into reverse-ordered, retrospective sequences. The mechanisms underlying this transformation remain unknown. We discovered that, during active navigation, rat hippocampal CA1 place cell ensembles are inherently organized to produce independent forward- and reverse-ordered sequences within individual theta oscillations. This finding may provide a circuit-level basis for retrospective evaluation and storage during ongoing behavior. Theta phase procession arose in a minority of place cells, many of which displayed two preferred firing phases in theta oscillations and preferentially participated in reverse replay during subsequent rest. These findings reveal an unexpected aspect of theta-based hippocampal encoding and provide a biological mechanism to support the expression of reverse-ordered sequences.

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