The balance of forward and backward hippocampal sequences shifts across behavioral states.

Abstract

Place cell firing patterns in the rat hippocampus are often organized as sequences. Sequences falling within cycles of the theta (6-10 Hz) local field potential (LFP) oscillation represent segments of ongoing behavioral trajectories. Sequences expressed during sharp wave ripple (SWR) complexes represent spatial trajectories through the environment, in both the same direction as actual trajectories (forward sequences) and in an ordering opposite that of behavior (backward sequences). Although hippocampal sequences could fulfill unique functional roles depending on the direction of the sequence and the animal's state when the sequence occurs, quantitative comparisons of sequence direction across behavioral and physiological states within the same experiment, employing consistent methodology, are lacking. Here, we used cross-correlation and Bayesian decoding to measure the direction of hippocampal sequences in rats during active behavior, awake rest and slow-wave sleep. During pretask sleep, few sequences were detected in either direction. Sequences within theta cycles during active behavior were overwhelmingly forward. Sequences during quiescent moments of behavior were both forward and backward, in equal proportion. During postbehavior sleep, sequences were again expressed in both directions, but significantly more forward than backward sequences were detected. The shift in the balance of sequence direction could reflect changing functional demands on the hippocampal network across behavioral and physiological states.