The brain has evolved an internal model of gravity to cope with life in the Earth's gravitational environment. How this internal model benefits the implementation of skilled movement has remained unsolved. One prevailing theory has assumed that this internal model is used to compensate for gravity's mechanical effects on the body, such as to maintain invariant motor trajectories. Alternatively, gravity force could be used purposely and efficiently for the planning and execution of voluntary movements, thereby resulting in direction-depending kinematics. Here we experimentally interrogate these two hypotheses by measuring arm kinematics while varying movement direction in normal and zero-G gravity conditions. By comparing experimental results with model predictions, we show that the brain uses the internal model to implement control policies that take advantage of gravity to minimize movement effort.DOI: http://dx.doi.org/10.7554/eLife.16394.001

Recent kinematic results, combined with model simulations, have provided support for the hypothesis that the human brain shapes motor patterns that use gravity effects to minimize muscle effort. Because many different muscular activation patterns can give rise to the same trajectory, here, we specifically investigate gravity-related movement properties by analyzing muscular activation patterns during single-degree-of-freedom arm movements in various directions. Using a well-known decomposition method of tonic and phasic electromyographic activities, we demonstrate that phasic electromyograms (EMGs) present systematic negative phases. This negativity reveals the optimal motor plan’s neural signature, where the motor system harvests the mechanical effects of gravity to accelerate downward and decelerate upward movements, thereby saving muscle effort. We compare experimental findings in humans to monkeys, generalizing the Effort-optimization strategy across species.

We permanently deal with gravity force. Experimental evidences revealed that moving against gravity strongly differs from moving along the gravity vector. This directional asymmetry has been attributed to an optimal planning process that optimizes gravity force effects to minimize energy. Yet, only few studies have considered the case of vertical movements in the context of optimal control. What kind of cost is better suited to explain kinematic patterns in the vertical plane? Here, we aimed to understand further how the central nervous system (CNS) plans and controls vertical arm movements. Our reasoning was the following: if the CNS optimizes gravity mechanical effects on the moving limbs, kinematic patterns should change according to the direction and the magnitude of the gravity torque being encountered in the motion. Ten subjects carried out single-joint movements, i.e., rotation around the shoulder (whole arm), elbow (forearm), and wrist (hand) joints, in the vertical plane. Joint kinematics were analyzed and compared with various theoretical optimal model predictions (minimum absolute work-jerk, jerk, torque change, and variance). We found both direction-dependent and joint-dependent variations in several kinematic parameters. Notably, directional asymmetries decreased according to a proximodistal gradient. Numerical simulations revealed that our experimental findings could be attributed to an optimal motor planning (minimum absolute work-jerk) that integrates the direction and the magnitude of gravity torque and minimizes the absolute work of forces (energy-related cost) around each joint. Present results support the general idea that the CNS implements optimal solutions according to the dynamic context of the action.

The present study investigates how the CNS deals with the omnipresent force of gravity during arm motor planning. Previous studies have reported direction-dependent kinematic differences in the vertical plane; notably, acceleration duration was greater during a downward than an upward arm movement. Although the analysis of acceleration and deceleration phases has permitted to explore the integration of gravity force, further investigation is necessary to conclude whether feedforward or feedback control processes are at the origin of this incorporation. We considered that a more detailed analysis of the temporal features of vertical arm movements could provide additional information about gravity force integration into the motor planning. Eight subjects performed single joint vertical arm movements (45° rotation around the shoulder joint) in two opposite directions (upwards and downwards) and at three different speeds (slow, natural and fast). We calculated different parameters of hand acceleration profiles: movement duration (MD), duration to peak acceleration (D PA), duration from peak acceleration to peak velocity (D PA-PV), duration from peak velocity to peak deceleration (D PV-PD), duration from peak deceleration to the movement end (D PD-End), acceleration duration (AD), deceleration duration (DD), peak acceleration (PA), peak velocity (PV), and peak deceleration (PD). While movement durations and amplitudes were similar for upward and downward movements, the temporal structure of acceleration profiles differed between the two directions. More specifically, subjects performed upward movements faster than downward movements; these direction-dependent asymmetries appeared early in the movement (i.e., before PA) and lasted until the moment of PD. Additionally, PA and PV were greater for upward than downward movements. Movement speed also changed the temporal structure of acceleration profiles. The effect of speed and direction on the form of acceleration profiles is consistent with the premise that the CNS optimises motor commands with respect to both gravitational and inertial constraints.

After an exposure to weightlessness, the central nervous system operates under new dynamic and sensory contexts. To find optimal solutions for rapid adaptation, cosmonauts have to decide whether parameters from the world or their body have changed and to estimate their properties. Here, we investigated sensorimotor adaptation after a spaceflight of 10 days. Five cosmonauts performed forward point-to-point arm movements in the sagittal plane 40 days before and 24 and 72 h after the spaceflight. We found that, whereas the shape of hand velocity profiles remained unaffected after the spaceflight, hand path curvature significantly increased 1 day after landing and returned to the preflight level on the third day. Control experiments, carried out by 10 subjects under normal gravity conditions, showed that loading the arm with varying loads (from 0.3 to 1.350 kg) did not affect path curvature. Therefore, changes in path curvature after spaceflight cannot be the outcome of a control process based on the subjective feeling that arm inertia was increased. By performing optimal control simulations, we found that arm kinematics after exposure to microgravity corresponded to a planning process that overestimated the gravity level and optimized movements in a hypergravity environment (∼1.4 g). With time and practice, the sensorimotor system was recalibrated to Earth's gravity conditions, and cosmonauts progressively generated accurate estimations of the body state, gravity level, and sensory consequences of the motor commands (72 h). These observations provide novel insights into how the central nervous system evaluates body (inertia) and environmental (gravity) states during sensorimotor adaptation of point-to-point arm movements after an exposure to weightlessness.

The central nervous system (CNS) develops motor strategies that minimize various hidden criteria, such as end-point variance or effort. A large body of literature suggests that the dominant arm is specialized for such open-loop optimization-like processes, whilst the non-dominant arm is specialized for closed-loop postural control. Building on recent results suggesting that the brain plans arm movements that take advantage of gravity effects to minimize muscle effort, the present study tests the hypothesized superiority of the dominant arm motor system for effort minimization. Thirty participants (22.5 ± 2.1 years old; all right-handed) performed vertical arm movements between two targets (40° amplitude), in two directions (upwards and downwards) with their two arms (dominant and non-dominant). We recorded the arm kinematics and electromyographic activities of the anterior and posterior deltoid to compare two motor signatures of the gravity-related optimization process; i.e., directional asymmetries and negative epochs on phasic muscular activity. We found that these motor signatures were still present during movements performed with the non-dominant arm, indicating that the effort-minimization process also occurs for the non-dominant motor system. However, these markers were reduced compared with movements performed with the dominant arm. This difference was especially prominent during downward movements, where the optimization of gravity effects occurs early in the movement. Assuming that the dominant arm is optimal to minimize muscle effort, as demonstrated by previous studies, the present results support the hypothesized superiority of the dominant arm motor system for effort-minimization.

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Humans excel at learning complex tasks, and elite performers such as musicians or athletes develop motor skills that defy biomechanical constraints. All actions require the movement of massive bodies. Of particular interest in the process of sensorimotor learning and control is the impact of gravitational forces on the body. Indeed, efficient control and accurate internal representations of the body configuration in space depend on our ability to feel and anticipate the action of gravity. Here we review studies on perception and sensorimotor control in both normal and altered gravity. Behavioral and modeling studies together suggested that the nervous system develops efficient strategies to take advantage of gravitational forces across a wide variety of tasks. However, when the body was exposed to altered gravity, the rate and amount of adaptation exhibited substantial variation from one experiment to another and sometimes led to partial adjustment only. Overall, these results support the hypothesis that the brain uses a multimodal and flexible representation of the effect of gravity on our body and movements. Future work is necessary to better characterize the nature of this internal representation and the extent to which it can adapt to novel contexts.