Anticipatory coadaptation of ankle stiffness and sensorimotor gain for standing balance

External perturbation forces may compromise standing balance. The nervous system can intervene only after a delay greater than 100 ms, during which the body falls freely. With ageing, sensorimotor delays are prolonged, posing a critical threat to balance. We study a generic model of stabilisation with neural delays to understand how the organism should adapt to challenging balance conditions. The model suggests that ankle stiffness should be increased in anticipation of perturbations, for example by muscle co-contraction, so as to slow down body fall during the neural response delay. Increased ankle muscle co-contraction is indeed observed in young adults when standing in challenging balance conditions, and in older relative to young adults during normal stance. In parallel, the analysis of the model shows that increases in either stiffness or neural delay must be coordinated with decreases in spinal sensorimotor gains, otherwise the feedback itself becomes destabilizing. Accordingly, a decrease in spinal feedback is observed in challenging conditions, and with age-related increases in neural delay. These observations have been previously interpreted as indicating an increased reliance on cortical rather than spinal control of balance, despite the fact that cortical responses have a longer latency. Our analysis challenges this interpretation by showing that these observations are consistent with a functional coadaptation of spinal feedback gains to functional changes in stiffness and neural delay.Author summary: Being able to stand still can be difficult when faced with an unexpected push. It takes the nervous system more than a tenth of a second to respond to such a perturbation, and during this delay the body falls under the influence of its own weight. By co-contracting their ankle muscles in anticipation of a perturbation, subjects can increase their ankle stiffness, which slows down their fall during the neural delay. Young subjects indeed adopt this strategy when they need to remain particularly still (for example when they stand in front of a cliff). Older subjects adopt this strategy even during normal standing. We present a model of standing balance that shows that this postural strategy provides partial compensation for the increase in neural delays with ageing. According to our model, increasing ankle stiffness only improves balance if it is accompanied by a decrease in sensorimotor gain. This provides a novel and functional interpretation for the decrease in spinal feedback observed during ageing, and observed in young subjects when they stand in challenging balance conditions.