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Rhythmic Action Synchronizes Memory Replay During Reinforcement Learning


Our cognitive abilities - learning from the past, sensing the current environment, planning into the future, executing an action, and infusing value into an experience - all rely on precisely timed and widespread electrical communications across neural networks. The brain’s hippocampal formation receives multimodal input, forges episodic associations, and predicts future state. Oscillating electrical bursts originating from the hippocampus, termed ‘sharp-wave ripples’ (SWR), often contain patterns of previously expressed neural spike sequences, and are necessary for certain forms of learning and memory. The discharge of SWR-replay resonates in remote parts of the brain and displays specific characteristics depending on a subject’s state of awareness and sensory context. In the sleep state, when motoric repertoire is limited, waves of breathing synchronize neural activity in several regions of the brain, including SWRs of the hippocampus. During active sensation of the awake state, cyclic licking dynamically entrains taste-reward networks in subcortical and cortical areas throughout learning. However, the neural correlates linking oromotor movements in the active learning state to the memory system of the hippocampal formation have not yet been established. Given the recurrence of SWR-replay during rhythmic ingestion of reinforcement learning and the hierarchical coupling of orofacial behaviors, we hypothesized that repeated licking could provide the oscillatory framework to synchronize memory reactivation during active learning. We approach this question with new technology development to track licking events at a reward port (P-event) during behavior on a spatial alternation task. Additionally, we developed a modular brain implant to simultaneously record from hippocampal area CA1 and medial entorhinal cortex (MEC) - interconnected brain regions that are crucial to episodic memory processing. Along with the co-modulation of individual neurons by licking and SWRs, we provide the first evidence that SWRs detected in dorsal CA1 synchronize with the phase of P-event cycle during learning. Furthermore, we confirmed that SWRs occurring during licking bouts contain neural reactivation of active navigation and trigger enhanced ripple-frequency power in downstream MEC. These results connect movement with memory and may assist in addressing abnormal ingestion behaviors that negatively affect mental or physical health

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