Hippocampal sharp wave-ripple dynamics in NREM sleep encode motivation for future physical activity.

Physical activity is an integral part of every mammal’s daily life, and as a driver of Darwinian fitness, required coordinated evolution of the body and brain. The human population is currently in its most historically sedentary state, creating a global health crisis - necessitating improved understanding of exercise motivation. The decision to engage in physical activity can be driven by survival needs (e.g., escaping danger) or by the motivation for the rewarding nature of physical activity itself (e.g., running exercise). Rodents exhibit innate and learned motivation for voluntary wheel running exercise, and over time run for longer durations and distances, reflecting increased incentive salience and motivation for this consummatory behavior. Daily motivation for running is highly variable, which necessitates dynamic coordination of neural and somatic physiology (e.g., action planning and associated metabolic demand) to ensure the ability to carry out the planned activity. Hippocampal sharp wave-ripples (SWRs) evolved both cognitive (e.g., action planning) and metabolic (e.g., blood glucose regulation) functions, suggesting a role in such body-brain coordination. Here we monitored hippocampal CA1 local field potential activity and running levels in adult mice, while manipulating the incentive salience of running. During non-REM (NREM) sleep, the duration of SWRs before (but not after) running positively correlated with future time spent running, while in contrast, the rate of SWR occurrence both before and after exhibited a positive correlation. Because SWR durations reflect information content and rates reflect both information and metabolic signaling, our results suggest multiplexing of SWR dynamics as a mechanism supporting both cognitive and metabolic aspects of exercise. We hypothesize that SWRs coordinate body-brain interactions to a greater extent than previously known.