Abstract

Although the hippocampus plays a critical role in spatial and episodic memories, the mechanisms underlying memory formation, stabilization, and recall for adaptive behavior remain relatively unknown. During exploration, within single cycles of the ongoing theta rhythm that dominates hippocampal local field potentials, place cells form precisely ordered sequences of activity. These neural sequences result from the integration of both external inputs conveying sensory-motor information, and intrinsic network dynamics possibly related to memory processes. Their endogenous replay during subsequent sleep is critical for memory consolidation. The present review discusses possible mechanisms and functions of hippocampal theta sequences during exploration. We present several lines of evidence suggesting that these neural sequences play a key role in information processing and support the formation of initial memory traces, and discuss potential functional distinctions between neural sequences emerging during theta vs. awake sharp-wave ripples.

Highlights

  • The ability of brain circuits to generate precise sequences of neuronal activity may underlie certain forms of sensory-motor processing and learning (Skaggs et al, 1996; Riehle et al, 1997; Stopfer et al, 1997; Petersen et al, 2001)

  • This indicates that theta sequences play a causal role in establishing initial memory traces, which can later be reinstated during sleep for memory consolidation

  • The above discussion suggests a functional dissociation between theta sequences and awake replay, where theta sequences would store initial memory traces about ongoing experiences as well as recall previously formed memories and enhance them to include goal-directed information, while awake replay would play an instrumental role in learning goal locations and planning upcoming trajectories

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Summary

INTRODUCTION

The ability of brain circuits to generate precise sequences of neuronal activity may underlie certain forms of sensory-motor processing and learning (Skaggs et al, 1996; Riehle et al, 1997; Stopfer et al, 1997; Petersen et al, 2001). Hippocampal Sequences During Exploration place cells fire in sequence, reflecting the ongoing trajectory at the behavioral timescale Embedded in these slow sequences, time-compressed sequences emerge in each cycle of the ongoing theta rhythm (O’Keefe and Recce, 1993; Skaggs et al, 1996), a strong and regular ∼8 Hz oscillation of the hippocampal local field potential (LFP; Jouvet, 1969; Vanderwolf, 1969). Fast time-compressed trajectories are represented by neuronal sequences that occur during brief pauses and prolonged immobility (Foster and Wilson, 2006; Diba and Buzsáki, 2007), when theta oscillations are absent Instead, these replay events occur during sharp-wave ripple complexes (O’Keefe, 1976; Buzsáki et al, 1983, 1992), a transient LFP pattern associating fast (∼200 Hz) oscillations in stratum pyramidale and a large deflection in stratum radiatum. We discuss possible functional distinctions between neural sequences emerging during theta and awake sharp-wave ripples

EMERGENCE OF THETA SEQUENCES
Theta During Locomotion
Theta Phase Precession
Mechanisms of Phase Precession
Mechanisms of Theta Sequences
Theta-Gamma Neural Code
Theta Sequences and Trajectory
Theta Sequences and Memory
Awake Replay During Sharp-Wave
Functional Dissociation Between Theta
CONCLUSION

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