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.

Gravitational force level is well-known to influence arm motor control. Specifically, hyper- or microgravity environments drastically change pointing accuracy and kinematics, particularly during initial exposure. These modifications are thought to partly reflect impairment in arm position sense. Here we investigated whether applying normogravitational constraints at joint level during microgravity episodes of parabolic flights could restore movement accuracy equivalent to that observed on Earth. Subjects with eyes closed performed arm reaching movements toward predefined sagittal angular positions in four environment conditions: normogravity, hypergravity, microgravity, and microgravity with elastic bands attached to the arm to mimic gravity-like torque at the shoulder joint. We found that subjects overshot and undershot the target orientations in hypergravity and microgravity, respectively, relative to a normogravity baseline. Strikingly, adding gravity-like torque prior to and during movements performed in microgravity allowed subjects to be as accurate as in normogravity. In the former condition, arm movement kinematics, as notably illustrated by the relative time to peak velocity, were also unchanged relative to normogravity, whereas significant modifications were found in hyper- and microgravity. Overall, these results suggest that arm motor planning and control are tuned with respect to gravitational information issued from joint torque, which presumably enhances arm position sense and activates internal models optimally adapted to the gravitoinertial environment.

Understanding the impact of weightlessness on human behavior during the forthcoming long-term space missions is of critical importance, especially when considering the efficiency of goal-directed movements in these unusual environments. Several studies provided a large set of evidence that gravity is taken into account during the planning stage of arm reaching movements to optimally anticipate its consequence upon the moving limbs. However, less is known about sensorimotor changes required to face weightless environments when individuals have to perform fast and accurate goal-directed actions with whole-body displacement. We thus aimed at characterizing kinematic features of whole-body reaching movements in microgravity, involving high spatiotemporal constraints of execution, to question whether and how humans are able to maintain the performance of a functional behavior in the standards of normogravity execution. Seven participants were asked to reach as fast and as accurately as possible visual targets while standing during microgravity episodes in parabolic flight. Small and large targets were presented either close or far from the participants (requiring, in the latter case, additional whole-body displacement). Results reported that participants successfully performed the reaching task with general temporal features of movement (e.g., movement speed) close to land observations. However, our analyses also demonstrated substantial kinematic changes related to the temporal structure of focal movement and the postural strategy to successfully perform -constrained- whole-body reaching movements in microgravity. These immediate reorganizations are likely achieved by rapidly taking into account the absence of gravity in motor preparation and execution (presumably from cues about body limbs unweighting). Specifically, when compared to normogravity, the arm deceleration phase substantially increased. Furthermore, greater whole-body forward displacements due to smaller trunk flexions occurred when reaching far targets in microgravity. Remarkably, these changes of focal kinematics and postural strategy appear close to those previously reported when participants performed the same task underwater with neutral buoyancy applied to body limbs. Overall, these novel findings reveal that humans are able to maintain the performance of functional goal-directed whole-body actions in weightlessness by successfully managing spatiotemporal constraints of execution in this unusual environment.

The present study aimed at investigating the consequences of a massive loss of somatosensory inputs on the perception of spatial orientation. The occurrence of possible compensatory processes for external (i.e., object) orientation perception and self-orientation perception was examined by manipulating visual and/or vestibular cues. To that aim, we compared perceptual responses of a deafferented patient (GL) with respect to age-matched Controls in two tasks involving gravity-related judgments. In the first task, subjects had to align a visual rod with the gravitational vertical (i.e., Subjective Visual Vertical: SVV) when facing a tilted visual frame in a classic Rod-and-Frame Test. In the second task, subjects had to report whether they felt tilted when facing different visuo-postural conditions which consisted in very slow pitch tilts of the body and/or visual surroundings away from vertical. Results showed that, much more than Controls, the deafferented patient was fully dependent on spatial cues issued from the visual frame when judging the SVV. On the other hand, the deafferented patient did not rely at all on visual cues for self-tilt detection. Moreover, the patient never reported any sensation of tilt up to 18 deg contrary to Controls, hence showing that she did not rely on vestibular (i.e., otoliths) signals for the detection of very slow body tilts either. Overall, this study demonstrates that a massive somatosensory deficit substantially impairs the perception of spatial orientation, and that the use of the remaining sensory inputs available to a deafferented patient differs regarding whether the judgment concerns external versus self-orientation.

Performing accurate actions such as goal-directed arm movements requires taking into account visual and body orientation cues to localize the target in space and produce appropriate reaching motor commands. We experimentally tilted the body and/or the visual scene to investigate how visual and body orientation cues are combined for the control of unseen arm movements. Subjects were asked to point toward a visual target using an upward movement during slow body and/or visual scene tilts. When the scene was tilted, final pointing errors varied as a function of the direction of the scene tilt (forward or backward). Actual forward body tilt resulted in systematic target undershoots, suggesting that the brain may have overcompensated for the biomechanical movement facilitation arising from body tilt. Combined body and visual scene tilts also affected final pointing errors according to the orientation of the visual scene. The data were further analysed using either a body-centered or a gravity-centered reference frame to encode visual scene orientation with simple additive models (i.e., ‘combined’ tilts equal to the sum of ‘single’ tilts). We found that the body-centered model could account only for some of the data regarding kinematic parameters and final errors. In contrast, the gravity-centered modeling in which the body and visual scene orientations were referred to vertical could explain all of these data. Therefore, our findings suggest that the brain uses gravity, thanks to its invariant properties, as a reference for the combination of visual and non-visual cues.

Astronauts' training is conventionally performed in a pool to reproduce weightlessness by exploiting buoyancy which is supposed to reduce the impact of gravity on the body. However, this training method has not been scientifically validated yet, and requires first to study the effects of underwater exposure on motor behavior. We examined the influence of neutral buoyancy on kinematic features of whole-body reaching underwater and compared them with those produced on land. Eight professional divers were asked to perform arm reaching movements toward visual targets while standing. Targets were presented either close or far from the subjects (requiring in the latter case an additional whole-body displacement). Reaching movements were performed on land or underwater in two different contexts of buoyancy. The divers either wore a diving suit only with neutral buoyancy applied to their center of mass or were additionally equipped with a submersible simulated space suit with neutral buoyancy applied to their body limbs. Results showed that underwater exposure impacted basic movement features, especially movement speed which was reduced. However, movement kinematics also differed according to the way buoyancy was exerted on the whole-body. When neutral buoyancy was applied to the center of mass only, some focal and postural components of whole-body reaching remained close to land observations, notably when considering the relative deceleration duration of arm elevation and concomitant forward trunk bending when reaching the far target. On the contrary, when neutral buoyancy was exerted on body segments, movement kinematics were close to those reported in weightlessness, as reflected by the arm deceleration phase and the whole-body forward displacement when reaching the far target. These results suggest that astronauts could benefit from the application of neutral buoyancy across the whole-body segments to optimize underwater training and acquire specific motor skills which will be used in space.