Dissociation between the experience-dependent development of hippocampal theta sequences and single-trial phase precession

Theta sequences are circuit-level activity patterns produced when groups of hippocampal place cells fire in sequences that reflect a compressed behavioral order of place fields within each theta cycle. The high temporal coordination between place cells exhibited in theta sequences is compatible with the induction of synaptic plasticity and has been proposed as one of the mechanisms underlying the encoding of episodic memory of recently acquired experience. Yet how theta sequences develop with experience has not been directly addressed. Here we simultaneously recorded large numbers of cells in the dorsal hippocampal CA1 area from rats exploring on a novel linear track. Althoughplacecell firingactivities accuratelyrepresentedtheanimal’scurrent location, distinct thetasequences wereabsent on the first lap but emerged immediately thereafter and remained stable once established. The absence of theta sequences on the first lap was not due to place field instability, decreased overall excitability of place cells, behavior variables, or the absence of individual neuronal phase precession. We observed strong single-lap phase precession in a significant percentage of place fields on the first lap and throughout the recording. Individual neuronal phase precession was stable from the first lap to subsequent laps but, across neurons, phase precession became more synchronized after experience, suggesting a novel mechanism for the generation of theta sequences. These results suggest that experience-independent temporal coding in individual neurons is combined with rapid plasticity of hippocampal neural networks during experience to acquire predictive representations of the immediate future.