Hippocampal sharp-wave ripples decrease during physical actions including consummatory behavior in immobile rodents

Abstract

Hippocampal sharp-wave ripples (SWRs) are intermittent, fast synchronous oscillations that play a pivotal role in memory formation. It has been well-established that SWRs occur during “consummatory behaviors”, e.g., eating or drinking a reward for correct action. However, most of typical behavioral experiments using freely moving rodents have not rigorously distinguished between the act of eating/drinking (regardless of consummation or consumption) from stopping locomotion (immobility). Therefore, in this study, we investigated the occurrence of SWRs during a reward-seeking action and subsequent consummatory reward licking in constantly immobile rats (male and female) maintained under head fixation and body covering. Immobile rats performed a pedal hold-release action that was rewarded with water every other time (false and true consummation). Unexpectedly, the SWRs remarkably decreased during reward licking as well as pedal release action. Untrained rats also showed a similar SWR decrease during water licking. Conversely, SWRs gradually increased during the pedal hold period, which was enhanced by reward expectation. A cluster of hippocampal neurons responded to cue/pedal release and reward, as previously shown. Some other clusters exhibited spike activity changes similar to the SWR occurrence, i.e., decreasing during the pedal release action and reward licking, and enhanced by reward expectation during pedal hold period. These task event-responsive neurons and SWR-like neurons displayed stronger spiking synchrony with SWRs than task-unrelated neurons. These findings suggest that the hippocampus generates SWRs, which may associate action with outcome, in “relative immobility” (action pauses) rather than specific consummation or consumption.

Significance Statement To clarify the characteristics of hippocampal sharp-wave ripples (SWRs), we analyzed the SWRs occurring during operant task performance in immobile rats under both head fixation and body covering. First, we found that SWRs decreased when they licked and drank water, conflicting with the theory that SWRs occur in consummatory behavior. Second, hippocampal neurons showed different task-related activities, particularly those that resembled SWR occurrences or conveyed specific signals on task events. Third, these task-related neurons displayed strong synchronous discharges during SWRs in task-engaged periods. These findings may explain the neuronal mechanisms underlying the association between an action and its outcome.