Nested sequences of hippocampal assemblies during behavior support subsequent sleep replay

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Science  09 Nov 2018:
Vol. 362, Issue 6415, pp. 675-679
DOI: 10.1126/science.aat2952

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Theta rhythm protects sleep replay

Hippocampal replay of place cell sequences during sleep is critical for memory consolidation in target cortical areas. How is the sequential organization of place cell assemblies maintained across different time scales? Drieu et al. compared periods when a rat either sat passively on a moving train or ran actively on a treadmill on the same train. During the passive movement, the slow behavioral sequence of place cells was still present, but the rapid generation of theta sequences was lost. Active running on the treadmill, however, maintained the theta rhythm. After passive transport, sequence replay during sleep was destroyed, whereas active running protected replay.

Science, this issue p. 675


Consolidation of spatial and episodic memories is thought to rely on replay of neuronal activity sequences during sleep. However, the network dynamics underlying the initial storage of memories during wakefulness have never been tested. Although slow, behavioral time scale sequences have been claimed to sustain sequential memory formation, fast (“theta”) time scale sequences, nested within slow sequences, could be instrumental. We found that in rats traveling passively on a model train, place cells formed behavioral time scale sequences but theta sequences were degraded, resulting in impaired subsequent sleep replay. In contrast, when the rats actively ran on a treadmill while being transported on the train, place cells generated clear theta sequences and accurate trajectory replay during sleep. Our results support the view that nested sequences underlie the initial formation of memory traces subsequently consolidated during sleep.

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