Speed-dependent optimization of gravity effects for motor control

Abstract

Several sensorimotor control studies have provided evidence supporting that the central nervous system optimizes gravity effects to minimize muscle effort. Recently, this hypothesis has been supported by the consistent observation of direction-specific negative epochs in the phasic electromyographic signal of antigravity muscles during vertical arm movements. This suggests that gravity torque is harvested to produce some of the arm motion. However, further investigation is needed to more finely understand how the CNS integrates gravity effects into muscle commands. Here, we aimed to analyze the phasic muscular activity across varying movement speeds during horizontal and vertical arm movements. We quantified the amount of negativity during acceleration and deceleration phases for all movement directions during fast, natural, and slow movements. We found that the negativity was more important during the acceleration phase of downward movements and during the deceleration phase of upward movements, resulting in diminished phasic activity compared to horizontal movements. Concomitantly, we found direction-specific effects of movement speed on phasic EMG activity of gravity muscles. This resulted in altered EMG to kinematics relationships in vertical movements compared to horizontal ones. These results support the Effort-minimization hypothesis and confirm that the negativity of phasic EMG is an important aspect of the motor command. Furthermore, the present results reveal that the CNS finely tunes this feature across a range of movement speeds and directions.

Evidence for flexible motor costs in vertical arm movements: reduced gravity-related effort minimization under high accuracy constraints

“…Because the tonic electromyogram (EMG)—i.e., the muscle activity that is hypothesized to compensate for gravity torque—is subtracted from the full EMG signal to obtain phasic EMG (Flanders and Herrmann, 1992; Buneo et al, 1994; Flanders et al, 1994), negative phasic EMGs mean that muscular activity is not sufficient to compensate gravity torque and thus that gravity torque participates in the arm’s motion (Gaveau et al, 2021). The existence of these negative phases has been experimentally observed in the deceleration phase of upward movements and in the acceleration phase of downward movements, thereby supporting the model’s predictions (Gaveau et al, 2021; Poirier et al, 2022, 2023b, 2023a). Consequently, directional asymmetries and negatives epochs on phasic EMG are thought to represent the hallmark of the gravity-related effort-optimization process.…”

“…It was recently shown that phasic EMG activity of antigravity muscles consistently exhibits negative epochs during vertical arm movements (Gaveau et al, 2021; Poirier et al, 2022; 2023a; 2023b) when the arm’s acceleration sign is coherent to gravity’s – i.e., in the acceleration phase of downward movements and in the deceleration phase of upward movements). Model simulations demonstrated that the negativity of antigravity muscles reflects an optimal motor strategy where gravity force is harvested to save muscle force.…”

“…This negativity reflects the fact that the current EMG activity is inferior than the activity necessary to compensate gravity torque, thereby demonstrating the harnessing of gravity's effects by the CNS. These negative epochs are now thought to represent a marker of the gravity-related motor optimization (Gaveau et al, 2021;Poirier et al, 2022Poirier et al, , 2023bPoirier et al, , 2023a.…”

“…Gravity-related motor planning (see Gaveau et al, 2016, 2021) could represent a useful paradigm to address this question. Multiple studies investigating vertical arm reaching movements consistently reported direction-dependent arm kinematics: the time to peak acceleration and time to peak velocity were shorter for upward than for downward movements (Papaxanthis et al, 2005; Gentili et al, 2007; Le Seac’h and McIntyre, 2007; Gaveau and Papaxanthis, 2011; Gaveau et al, 2014; Yamamoto and Kushiro, 2014; Gaveau et al, 2016, 2021; Yamamoto et al, 2016, 2019; Hondzinski et al, 2016; Poirier et al, 2023b, 2023a, 2020, 2022). Optimal control simulations have explained these directional differences - and their progressive disappearance during microgravity exposure (Gaveau et al, 2016) - as the signature of a gravity-related optimization process that minimizes muscle effort.…”

“…Some results suggest that the gravity-related effort optimization process may be influenced by task’s demands (speed instructions notably; (Gaveau and Papaxanthis, 2011; Poirier et al, 2023a). However, no study has hitherto specifically investigated this hypothesis.…”