Metabolic mode estimated by breathing reflects long-term motor memory

Abstract

Respiration is a crucial metabolic process that converts macronutrients, carbohydrates and fats, and oxygen (O2) into energy and carbon dioxide (CO2) to support motor actions. In addition to the energy demands of movements, the brain is a significant energy consumer, accounting for approximately 20% of the bodys total energy expenditure and relying primarily on carbohydrates for neural activity and plasticity. However, it is not known whether O2-CO2 gas composition in breathing can serve as an indicator of neural activity and plasticity as they can for movement intensity. In the human reaching movement tasks, we evaluated time-constants of sensorimotor learning while recording O2-CO2 gas exchange. We computed the respiratory exchange ratio (RER), indicating which carbohydrate or fat is used preferentially, and found that the RER was unaffected by the execution and learning of reaching movements and that it was stable within individuals but varied across individuals. Interestingly, using computational modeling to identify short and long-time constants of sensorimotor learning, individual RER levels correlated with the magnitude of long-term, but not short-term memory. Furthermore, to experimentally manipulate the individual RER, we provided 200 kcal of glucose immediately before the task. Surprisingly, this simple intervention dramatically increased 24-hour retention by 21%. Together, the RER served as a remarkable proxy for long-term motor memory, and glucose intake shifted the physiological idling state for sensorimotor learning.