Online corrective responses following target jump in altered gravitoinertial force field point to nested feedforward and feedback control.

Studies on goal-directed arm movements have shown a close link between feedforward and feedback control in protocols where both planning and online control processes faced a similar type of perturbation, either mechanical or visual. This particular context might have facilitated the use of an adapted internal model by feedforward and feedback control. Here, we considered this link in a context where, after feedforward control was adapted through proprioception-based processes, feedback control was tested under visual perturbation. We analyzed the response of the reaching hand to target displacements following adaptation to an altered force field induced by rotating participants at constant velocity. Reaching corrections were assessed through variables related to the accuracy (lateral and longitudinal end point errors) and kinematics (movement time, peak velocity) of the corrective movements. The electromyographic activity of different arm muscles (pectoralis, posterior deltoid, biceps brachii, and triceps brachii) was analyzed. Statistical analyses revealed that accuracy and kinematics of corrective movements were strikingly alike between normal and altered gravitoinertial force fields. However, pectoralis and biceps muscle activities recorded during corrective movements were significantly modified to counteract the effect of rotation-induced Coriolis and centrifugal forces on the arm. Remarkably, feedback control was functional from the very first time participants encountered a target jump in the altered force field. Overall, the present results demonstrate that feedforward control enables immediate functional feedback control even when applied to distinct sensorimotor processes.NEW & NOTEWORTHY We investigated the link between feedforward and feedback control when applying a double-step perturbation (visual target jump) during reaching movements performed in modified gravitoinertial environments. Altogether, kinematics and EMG analyses showed that movement corrections were highly effective in the different force fields, suggesting that, although feedforward and feedback control were driven by different sensory inputs, feedback control was remarkably functional from the very first time participants encountered a target jump in the altered force field.

Double-Step Paradigm in Microgravity: Preservation of Sensorimotor Flexibility in Altered Gravitational Force Field.

The way we can correct our ongoing movements to sudden and unforeseen perturbations is key to our ability to rapidly adjust our behavior to novel environmental demands. Referred to as sensorimotor flexibility, this ability can be assessed by the double-step paradigm in which participants must correct their ongoing arm movements to reach targets that unexpectedly change location (i.e., target jump). While this type of corrections has been demonstrated in normogravity in the extent of reasonable spatiotemporal constraints underpinning the target jumps, less is known about sensorimotor flexibility in altered gravitational force fields. We thus aimed to assess sensorimotor flexibility by comparing online arm pointing corrections observed during microgravity episodes of parabolic flights with normogravity standards. Seven participants were asked to point as fast and as accurately as possible toward one of two visual targets with their right index finger. The targets were aligned vertically in the mid-sagittal plane and were separated by 10 cm. In 20% of the trials, the initially illuminated lower target was switched off at movement onset while the upper target was concomitantly switched on prompting participants to change the trajectory of their ongoing movements. Results showed that, both in normogravity and microgravity, participants successfully performed the pointing task including when the target jumped unexpectedly (i.e., comparable success rate). Most importantly, no significant difference was found in target jump trials regarding arm kinematics between both gravitational environments, neither in terms of peak velocity, relative deceleration duration, peak acceleration or time to peak acceleration. Using inverse dynamics based on experimental and anthropometrical data, we demonstrated that the shoulder torques for accelerating and decelerating the vertical arm movements substantially differed between microgravity and normogravity. Our data therefore highlight the capacity of the central nervous system to perform very fast neuromuscular adjustments that are adapted to the gravitational constraints. We discuss our findings by considering the contribution of feedforward and feedback mechanisms in the online control of arm pointing movements.

The gravitational imprint on sensorimotor planning and control.

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.

Kinematic features of whole-body reaching movements underwater: Neutral buoyancy effects.

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.

Slow changing postural cues cancel visual field dependence on self-tilt detection.

Interindividual differences influence the multisensory integration process involved in spatial perception. Here, we assessed the effect of visual field dependence on self-tilt detection relative to upright, as a function of static vs. slow changing visual or postural cues. To that aim, we manipulated slow rotations (i.e., 0.05° s(-1)) of the body and/or the visual scene in pitch. Participants had to indicate whether they felt being tilted forward at successive angles. Results show that thresholds for self-tilt detection substantially differed between visual field dependent/independent subjects, when only the visual scene was rotated. This difference was no longer present when the body was actually rotated, whatever the visual scene condition (i.e., absent, static or rotated relative to the observer). These results suggest that the cancellation of visual field dependence by dynamic postural cues may rely on a multisensory reweighting process, where slow changing vestibular/somatosensory inputs may prevail over visual inputs.

How do visual and postural cues combine for self-tilt perception during slow pitch rotations?

Self-orientation perception relies on the integration of multiple sensory inputs which convey spatially-related visual and postural cues. In the present study, an experimental set-up was used to tilt the body and/or the visual scene to investigate how these postural and visual cues are integrated for self-tilt perception (the subjective sensation of being tilted). Participants were required to repeatedly rate a confidence level for self-tilt perception during slow (0.05°·s(-1)) body and/or visual scene pitch tilts up to 19° relative to vertical. Concurrently, subjects also had to perform arm reaching movements toward a body-fixed target at certain specific angles of tilt. While performance of a concurrent motor task did not influence the main perceptual task, self-tilt detection did vary according to the visuo-postural stimuli. Slow forward or backward tilts of the visual scene alone did not induce a marked sensation of self-tilt contrary to actual body tilt. However, combined body and visual scene tilt influenced self-tilt perception more strongly, although this effect was dependent on the direction of visual scene tilt: only a forward visual scene tilt combined with a forward body tilt facilitated self-tilt detection. In such a case, visual scene tilt did not seem to induce vection but rather may have produced a deviation of the perceived orientation of the longitudinal body axis in the forward direction, which may have lowered the self-tilt detection threshold during actual forward body tilt.

To pass or not to pass: more a question of body orientation than visual cues.

This study investigated the influence of pitch body tilt on judging the possibility of passing under high obstacles in the presence of an illusory horizontal self-motion. Seated subjects tilted at various body orientations were asked to estimate the possibility of passing under a projected bar (i.e., a parking barrier), while imagining a forward whole-body displacement normal to gravity. This task was performed under two visual conditions, providing either no visual surroundings or a translational horizontal optic flow that stopped just before the barrier appeared. The results showed a main overestimation of the possibility of passing under the bar in both cases and most importantly revealed a strong influence of body orientation despite the visual specification of horizontal self-motion by optic flow (i.e., both visual conditions yielded a comparable body tilt effect). Specifically, the subjective passability was proportionally deviated towards the body tilt by 46% of its magnitude when facing a horizontal optic flow and 43% without visual surroundings. This suggests that the egocentric attraction exerted by body tilt when referring the subjective passability to horizontal self-motion still persists even when anchoring horizontally related visual cues are displayed. These findings are discussed in terms of interaction between spatial references. The link between the reliability of available sensory inputs and the weight attributed to each reference is also addressed.

Influence of postural constraints on eye and head latency during voluntary rotations.

Redirecting gaze towards new targets often requires not only eye movements, but also synergistic rotations of the head, trunk and feet. This study investigates the influence of postural constraints on eye and head latency during voluntary refixations in the horizontal plane in 14 normal subjects. Three postural conditions were presented, (1) sitting in a chair using only eye and head movements, (2) standing without feet movements and (3) standing with feet movement. Head-eye reorientations towards eccentric un-predictable locations were performed towards ±45° and ±90° targets and back towards a central, spatially predictable target. Results showed that postural constraints affected eye latency but only when subjects knew the future location of the target (recentering "return" trials). Specifically, relatively longer eye latencies were observed when subjects had to turn their feet back towards the predictable central target. These findings suggest that the additional CNS processing required to reduce degrees of freedom during predictive motion introduces delays to the eye movement in order to efficiently assemble the components of a new motor synergy.

Effect of gravity-like torque on goal-directed arm movements in microgravity.

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.

Spatial localization investigated by continuous pointing during visual and gravitoinertial changes.

In order to accurately localize an object, human observers must integrate multiple sensory cues related to the environment and/or to the body. Such multisensory integration must be repeated over time, so that spatial localization is constantly updated according to environmental changes. In the present experimental study, we examined the multisensory integration processes underlying spatial updating by investigating how gradual modifications of gravitoinertial cues (i.e., somatosensory and vestibular cues) and visual cues affect target localization skills. These were assessed by using a continuous pointing task toward a body-fixed visual target. The "single" rotation of the gravitoinertial vector (produced by off-axis centrifugation) resulted in downward pointing errors, which likely were related to a combination of oculogravic and somatogravic illusions. The "single" downward pitch rotation of the visual background produced an elevation of the arm relative to the visual target, suggesting that the rotation of the visual background caused an illusory target elevation (induced-motion phenomenon). Strikingly, the errors observed during the "combined" rotation of the visual background and of the gravitoinertial vector appeared as a linear combination of the errors independently observed during "single" rotations. In other words, the centrifugation effect on target localization was reduced by the visual background rotation. The observed linear combination indicates that the weights of visual and gravitoinertial cues were similar and remained constant throughout the stimulation.

Postural configuration affects the perception of earth-based space during pitch tilt.

This study investigates the relative contribution of body parts in the elaboration of a whole-body egocentric attraction phenomenon previously observed during earth-based judgments. This was addressed through a particular earth-based task requiring estimating the possibility of passing under a projected line, imagining a forward horizontal displacement. Different postural configurations were tested, involving whole-body tilt, trunk tilt alone or head tilt alone. Two legs positions relative to the trunk were manipulated. Results showed systematic deviations of the subjective "passability" toward the tilt, linearly related to the tilt magnitude. For each postural configuration, the egocentric influence appeared to be highly dependent on the position of trunk and head axes, whereas the legs position appeared not relevant. When compared to the whole-body tilt condition, tilting the trunk alone consistently reduced the amount of the deviation toward the tilt, whereas tilting the head alone consistently increased it. Our results suggest that several specific effects from multiple body parts can account for the global deviation of the estimates observed during whole-body tilt. Most importantly, we support that the relative contribution of the body segments could mainly depend on a reweighting process, probably based on the reliability of sensory information available for a particular postural set.

Pitch body orientation influences the perception of self-motion direction induced by optic flow.

We studied the effect of static pitch body tilts on the perception of self-motion direction induced by a visual stimulus. Subjects were seated in front of a screen on which was projected a 3D cluster of moving dots visually simulating a forward motion of the observer with upward or downward directional biases (relative to a true earth horizontal direction). The subjects were tilted at various angles relative to gravity and were asked to estimate the direction of the perceived motion (nose-up, as during take-off or nose-down, as during landing). The data showed that body orientation proportionally affected the amount of error in the reported perceived direction (by 40% of body tilt magnitude in a range of +/-20 degrees) and these errors were systematically recorded in the direction of body tilt. As a consequence, a same visual stimulus was differently interpreted depending on body orientation. While the subjects were required to perform the task in a geocentric reference frame (i.e., relative to a gravity-related direction), they were obviously influenced by egocentric references. These results suggest that the perception of self-motion is not elaborated within an exclusive reference frame (either egocentric or geocentric) but rather results from the combined influence of both.

Judging beforehand the possibility of passing under obstacles without motion: the influence of egocentric and geocentric frames of reference.

Previous studies have shown that the perception of the earth-based visual horizon, also named Gravity Referenced Eye Level (GREL), is modified by body tilt around a trans-ocular axis. Here, we investigated whether estimates of the elevation of a luminous horizontal line presented on a screen in otherwise darkness and estimates of the possibility of passing under are identically related to body tilt in absence of motion. Results showed that subjects overestimated the elevation of the projected line, whatever their body orientation. In the same way, subjects also overestimated their capacity of passing under the line. Both estimates appeared as a linear function of body tilt, that is, forward body tilt yielded increased overestimations, and backward body tilt yielded decreased overestimations. More strikingly, the linear effect of body tilt upon these estimates is comparable to that previously observed for direct GREL judgements. Overall, these data strongly suggest that the perception of the elevation of a visible obstacle and the perception of the ability of passing under in otherwise darkness shared common processes which are intimately linked to the GREL perception. The effect of body tilt upon these perceptions may illustrate an egocentric influence upon the semi-geocentric frame of reference required to perform the task. Possible interactions between egocentric and geocentric frames of reference are discussed.

Influence of pitch tilts on the perception of gravity-referenced eye level in labyrinthine defective subjects.

We investigate the role of vestibular information in judging the gravity-referenced eye level (i.e., earth-referenced horizon or GREL) during sagittal body tilt whilst seated. Ten bilateral labyrinthine-defective subjects (LDS) and 10 age-matched controls set a luminous dot to their perception of GREL in darkness, with and without arm pointing. Although judgements were linearly influenced by the magnitude of whole-body tilt, results showed no significant difference between LDS and age-matched controls in the subjective GREL accuracy or in the intra-subject variability of judgement. However, LDS performance without arm pointing was related to the degree of vestibular compensation inferred from another postural study performed with the same patients. LDS did not utilize upper limb input during arm pointing movements as a source of graviceptive information to compensate for the vestibular loss. The data suggest that vestibular cues are not of prime importance in GREL estimates in static conditions. The absence of difference between controls and LDS GREL performance, and the correlation between the postural task and GREL accuracy, indicate that somatosensory input may convey as much graviceptive information required for GREL judgements as the vestibular system.

Vision of the hand prior to movement onset allows full motor adaptation to a multi-force environment.

In everyday life, because of unexpected mechanical perturbation applied to the hand or to the whole body, hand movements may become suddenly inaccurate. With prolonged exposure to the perturbation, trajectories slowly recover their normal accuracy, which is the mark of motor adaptation. However, full development of this adaptive process in complete darkness has been recently challenged in a multi-force environment. Here, we report on the effectiveness of static hand position information as specified through vision prior to movement onset on the adaptative changes, over trials, of pointing movements performed in a gravitoinertial force field. For this, subjects seated off-center on a platform rotating at constant velocity, were either confined to complete darkness (No Vision Session, NV) or provided with vision of the hand resting on the starting position prior to movement onset (Hand Vision Prior to Movement Session, HVPM). Overall, our results showed that adaptation to the centrifugal force was very rapid, and allowed subjects to demonstrate appropriate motor control as early as of the very first trials performed during the rotation period, even in the NV condition. They also showed that the integration by the Central Nervous System (CNS) of visual and proprioceptive information prior to the execution of a reaching movement allows subjects to reach full motor adaptation in a multi-force environment. Furthermore, our data confirm the existence of differentiated motor adaptive mechanisms for centrifugal and Coriolis forces. Adaptation to the former may fully develop on the basis of an a priori coding of the characteristics of the background force level even without visual information, while the latter needs visual cues about hand position prior to movement onset to take place.

Effects of external feedback about body tilt: Influence on the Subjective Proprioceptive Horizon.

The present study investigated a cognitive aspect upon spatial perception, namely the impact of a true or false verbal feedback (FB) about the magnitude of body tilt on Subjective Proprioceptive Horizon (SPH) estimates. Subjects were asked to set their extended arm normal to gravity for different pitch body tilts up to 9 degrees . True FB were provided at all body tilt angles, whereas false FB were provided only at 6 degrees backward and 6 degrees forward body tilts for half of the trials. Our data confirmed previous results about the egocentric influence of body tilt itself upon SPH: estimates were linearly lowered with forward tilts and elevated with backward tilts. In addition, results showed a significant effect of the nature of the external FB provided to the subjects. When subjects received a false FB inducing a 3 degrees forward bias relative to physical body tilt, they set their SPH consequently higher than when they received a false FB inducing a 3 degrees backward bias. These findings clearly indicated that false cognitive information about body tilt might significantly modify the judgement of a geocentric direction of space, such as the SPH. This may have deleterious repercussions in aeronautics when pilots have to localize external objects relative to earth-based directions in darkened environments.

Influence of whole-body pitch tilt and kinesthetic cues on the perceived gravity-referenced eye level.

We investigated the effects of whole body tilt and lifting the arm against gravity on perceptual estimates of the Gravity-Referenced Eye Level (GREL), which corresponds to the subjective earth-referenced horizon. The results showed that the perceived GREL was influenced by body tilt, that is, lowered with forward tilt and elevated with backward tilt of the body. GREL estimates obtained by arm movements without vision were more biased by whole-body tilt than purely visual estimates. Strikingly, visual GREL estimates became more dependent on whole-body tilt when the indication of level was obtained by arm lifting. These findings indicate that active motor involvement and/or the addition of kinesthetic information increases the body tilt-induced bias when making GREL judgements. The introduction of motor/kinaesthetic cues may induce a switch from a semi-geocentric to a more egocentric frame of reference. This result challenges the assumption that combining non-conflicting multiple sensory inputs and/or using intermodal information provided during action should improve perceptual performance.

Accuracy level of pointing movements performed during slow passive whole-body rotations.

Seated observers requested to detect low-velocity passive rotations show a high motion-detection threshold. However, when standing on a slowly rotating platform, their equilibrium is preserved, suggesting that cognitive sensing and sensorimotor reactions do not share the same central processes. The present experiments investigated the ability of observers seated on a slowly rotating chair in total darkness to indicate with their hand the position of briefly flashed targets (Experiment 1) and to indicate the subjective horizon with an outstretched arm (Experiment 2) or with a target driven by a joystick (Experiment 3). The overall hypothesis stated that egocentric coding of the position of a target should not be affected by sensing or not-sensing body rotation (Experiment 1), while geocentric positioning may (Experiments 2 and 3). Our data partially supported the hypothesis. Subjects pointed accurately to the memorized targets (Experiment 1), whereas misperception of body orientation was a source of inaccuracy for actions referred to a geocentric frame (Experiments 2 and 3). More interestingly, subjects' perceptions changed as a single, smooth, and monotonic function of tilt, independent of whether the perception of body orientation was present or not.

Effects of gymnastics expertise on the perception of body orientation in the pitch dimension.

The purpose of this study was to investigate how experts in motor skills requiring a fine postural control perceive their body orientation with few gravity based sensory cues. In Experiment 1, expert gymnasts and controls had to detect their body tilt when pitching at a velocity of 0.05 deg.s(-1), in two conditions of body restriction (strapped and body cast altering the somatosensory cues). Contrary to the experts, the controls exhibited a larger body tilt when totally restrained in the body cast. In Experiment 2, subjects had to estimate their Subjective Postural Vertical (SPV) starting from different angles of pitch tilt. The controls exhibited significant errors of SPV judgement whereas the experts were very precise. These results suggest that 1) somatosensory cues are more informative than otolithic cues for the perception of body orientation, and 2) the efficiency of otolithic and/or interoceptive inputs can be improved through a specific training to compensate for the lack of somatosensory cues.