Hippocampal sharp-wave ripples decrease during physical actions including consummatory behavior in immobile rodents
Hippocampal sharp-wave ripples (SWRs) are intermittent, fast synchronous oscillations that play a pivotal role in memory formation. It is well known 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 eating/drinking itself (regardless of whether it means consummation or consumption) from stopping locomotion (immobility). In this study, therefore, we examined the occurrence of SWRs during a reward-seeking action and subsequent consummatory reward licking in constantly immobile rats under head fixation and body restriction. The immobile rats performed a pedal hold-release action that was rewarded with water every other time for their correct action (false and true consummation). Unexpectedly, the SWRs remarkably decreased during reward licking as well as pedal release action. Unlearned rats also showed a similar SWR decrease during water licking. On the other hand, the SWRs increased gradually during pedal hold period, which was enhanced by reward expectation. A cluster of hippocampal neurons responded to Cue/pedal release and reward as known previously. 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 the SWRs than task-unrelated neurons. These findings suggest that the hippocampus generates the SWRs, which may associate action with outcome, in animals "relative immobility" (action pauses) rather than specific consummation or consumption.

Significance StatementTo clarify the nature of sharp-wave ripples (SWRs) in the hippocampus, we analyzed the SWRs occurring during operant task performance by immobile rats under head-fixation and body restriction. First, we found the SWRs decreased when they licked and drank water, which conflicts with the theory that the SWRs occur in consummatory behavior. Second, hippocampal neurons showed different task-related activities, particularly those that resemble the SWR occurrence and those that conveyed specific signals on task events. Third, these task-related neurons displayed strong synchronous discharges during the SWRs in task-engaged periods. These findings may explain the neuronal mechanism underlying the association between an action and its outcome.