Spatio-Temporal Separation of Roll and Pitch Balance-Correcting Commands in Humans

Abstract

This study was designed to provide evidence for the hypothesis that human balance corrections in response to pitch perturbations are controlled by muscle action mainly about the ankle and knee joints, whereas balance corrections for roll perturbations are controlled predominantly by motion about the hip and lumbro-sacral joints. A dual-axis rotating support surface delivered unexpected random perturbations to the stance of 19 healthy young adults through eight different directions in the pitch and the roll planes and three delays between pitch and roll directions. Roll delays with respect to pitch were no delay, a short 50-ms delay of roll with respect to pitch movements, (chosen to correspond to the onset time of leg muscle stretch reflexes), and a long 150-ms delay between roll and pitch movements (chosen to shift the time when trunk roll velocity peaks to the time when trunk peak pitch velocity normally occurs). Delays of stimulus roll with respect to pitch resulted in delayed roll responses of the legs, trunk, arms, and head consistent with stimulus delay without any changes in roll velocity amplitude. Delayed roll perturbations induced only small changes in the pitch motion of the legs and trunk; however, major changes were seen in the time when roll motion of the trunk was arrested. Amplitudes and directional sensitivity of short-latency (SL) stretch reflexes in ankle muscles were not altered with increasing roll delay. Small changes to balance correcting responses in ankle muscles were observed. SL stretch reflexes in hip and trunk muscles were delayed, and balance-correcting responses in trunk muscles became split into two distinct responses with delayed roll. The first of these responses was small and had a directional responsiveness aligned more along the pitch plane. The main, larger, response occurred with an onset and time-to-peak consistent with the delay in trunk roll displacement and its directional responsiveness was roll oriented. The sum of the amplitudes of these two types of balance-correcting responses remained constant with roll delay. These results support the hypothesis that corrections of the body's pitch and roll motion are programmed separately by neural command signals and provide insights into possible triggering mechanisms. The evidence that lower leg muscle balance-correcting activity is hardly changed by delayed trunk roll also indicates that lower leg muscle activity is not predominant in correcting roll motion of the body. Lower leg and trunk muscle activity appears to have a dual action in balance corrections. In trunk muscles the main action is to correct for roll perturbations and the lesser action may be an anticipatory stabilizing reaction for pitch perturbations. Likewise, the small changes in lower leg muscle activity may result from a generalized stabilizing reaction to roll perturbations, but the main action is to correct for pitch perturbations.