Minimizing command timing volatility is a key factor in skilled actions

Abstract

AbstractVariability between movements prevents the best athletes from making a perfect shot every time. While fluctuations in the amplitude of neural sensory inputs and motor outputs are thought to be primarily responsible, they only account for a fraction of the observed variability. Here, we propose that a significant portion of the variability is due to imprecisely timed motor commands. This command timing volatility theory best explained the three peaks observed in the force variability’s time-series in discrete reaching movements and during periodic force control. Furthermore, we show how the timing volatility in the non-dominant arm’s muscles is larger than in the dominant arm, then develop a variability index that estimates the arm’s timing volatility via its variability during circle tracing. The difference in the variability index between the left and right hands accurately predicts the Edinburgh Quotient, suggesting a relationship between handedness and the command timing volatility of the left- and right-hands. Lastly, we constructed a simulation of reaching movements made by an arm controlled by muscles whose command timing was made incrementally more volatile. As timing volatility increased, aiming became less precise and movements jerkier. Such impairments during reaching are reported in patients with different neuronal diseases that damage any brain regions critical to motor timing, suggesting that essential aspects of these symptoms may be caused by excessive timing volatility. Our theory provides a unifying computational perspective of movement variability in healthy and diseased individuals that is essential to understanding the control of movements.