Fabrice R. Sarlegna

Galvanic vestibular stimulation in humans produces online arm movement deviations when reaching towards memorized visual targets.

Using galvanic vestibular stimulation (GVS), we tested whether a change in vestibular input at the onset of goal-directed arm movements induces deviations in arm trajectory. Eight head-fixed standing subjects were instructed to reach for memorized visual targets in complete darkness. In half of the trials, randomly-selected, a 3 mA bipolar binaural galvanic stimulation of randomly alternating polarity was triggered by the movement onset. Results revealed significant GVS-induced directional shifts of reaching movements towards the anode side. The earliest significant deviations of hand path occurred 240 ms after stimulation onset. The likely goal of these online deviations of arm trajectory was to compensate for a vestibular-evoked apparent change in the spatial relationship between the target and the hand.

Force-field adaptation without proprioception: Can vision be used to model limb dynamics?

Because our environment and our body can change from time to time, the efficiency of human motor behavior relies on the updating of the neural processes transforming intentions into actions. Adaptation to the context critically depends on sensory feedback such as vision, touch or hearing. Although proprioception is not commonly listed as one of the main senses, its role is determinant for the coordination of daily gestures like goal-directed arm movements. In particular, previous work suggests that proprioceptive information is critical to update the internal representation of limb dynamic properties. Here, we examined the motor behavior of a deafferented patient, deprived of proprioception below the nose, to assess adaptation to new dynamic conditions in the absence of limb proprioception. The patient, and age-matched control participants, reached toward visual targets in a new force field created by a rotating platform. Full vision of the limb and workspace was available throughout the experiment. Although her impairment was obvious in baseline reaching performance, the proprioceptively deafferented patient clearly adapted to the new force conditions. In fact, her time course of adaptation was similar to that observed in controls. Moreover, when tested in the normal force field after adaptation to the new force field, the patient exhibited after-effects similar to those of controls. These findings show that motor adaptation to a modified force field is possible without proprioception and that vision can compensate for the permanent loss of proprioception to update the central representation of limb dynamics.

On-line versus off-line vestibular-evoked control of goal-directed arm movements.

The present study tested whether vestibular input can be processed on-line to control goal-directed arm movements towards memorized visual targets when the whole body is passively rotated during movement execution. Subjects succeeded in compensating for current body rotation by regulating ongoing arm movements. This performance was compared to the accuracy with which subjects reached for the target when the rotation occurred before the movement. Subjects were less accurate in updating the internal representation of visual space through vestibular signals than in monitoring on-line body orientation to control arm movement. These results demonstrate that vestibular signals contribute to motor control of voluntary arm movements and suggest that the processes underlying on-line regulation of goal-directed movements are different from those underlying navigation-like behaviors.

Delayed Visual Feedback Affects Both Manual Tracking and Grip Force Control When Transporting a Handheld Object

When we manipulate an object, grip force is adjusted in anticipation of the mechanical consequences of hand motion (i.e., load force) to prevent the object from slipping. This predictive behavior is assumed to rely on an internal representation of the object dynamic properties, which would be elaborated via visual information before the object is grasped and via somatosensory feedback once the object is grasped. Here we examined this view by investigating the effect of delayed visual feedback during dextrous object manipulation. Adult participants manually tracked a sinusoidal target by oscillating a handheld object whose current position was displayed as a cursor on a screen along with the visual target. A delay was introduced between actual object displacement and cursor motion. This delay was linearly increased (from 0 to 300 ms) and decreased within 2-min trials. As previously reported, delayed visual feedback altered performance in manual tracking. Importantly, although the physical properties of the object remained unchanged, delayed visual feedback altered the timing of grip force relative to load force by about 50 ms. Additional experiments showed that this effect was not due to task complexity nor to manual tracking. A model inspired by the behavior of mass-spring systems suggests that delayed visual feedback may have biased the representation of object dynamics. Overall, our findings support the idea that visual feedback of object motion can influence the predictive control of grip force even when the object is grasped.

The influence of visual target information on the online control of movements

The continuously changing properties of our environment require constant monitoring of our actions and updating of our motor commands based on the task goals. Such updating relies upon our predictions about the sensory consequences of our movement commands, as well as sensory feedback received during movement execution. Here we focus on how visual information about target location is used to update and guide ongoing actions so that the task goal is successfully achieved. We review several studies that have manipulated vision of the target in a variety of ways, ranging from complete removal of visual target information to changes in visual target properties after movement onset to examine how such changes are accounted for during motor execution. We also examined the specific role of a critical neural structure, the parietal cortex, and argue that a fundamental challenge for the future is to understand how visual information about target location is integrated with other streams of information, during movement execution, to estimate the state of the body and the environment in order to ensure optimal motor performance.

Visual guidance of arm reaching: Online adjustments of movement direction are impaired by amplitude control

Most reaching arm movements have amplitude and direction constraints. Here we investigated the interdependence of these movement parameters in terms of visual control. To do so, we asked human adults to look and reach toward targets such that, in a first experiment, both movement amplitude and direction had to be controlled. Randomly, hand visual feedback was shifted near arm movement onset to influence movement direction, movement amplitude or both. Because the visual shifts occurred during ocular saccades, they were not consciously perceived. The rapid reaching movements (mean duration = 334 ms) were slightly influenced by the visual shifts (approximately 15% and 8% of visual adjustment for movement direction and amplitude, respectively). Moreover, directional adjustments varied according to amplitude adjustments (and vice-versa). We thus examined, in a second experiment, the effect of relaxing the requirement to control movement amplitude. Asking participants to control only movement direction led to substantial directional adjustments (49%) based on shifted hand visual feedback. Overall, these findings indicate that the control of movement amplitude constrains the online adjustments of movement direction and that the mechanisms controlling movement amplitude and direction are not independent.

Influence of feedback modality on sensorimotor adaptation: contribution of visual, kinesthetic, and verbal cues.

In 4 studies, the authors tested the contributions of visual, kinesthetic, and verbal knowledge of results to the adaptive control of reaching movements toward visual targets. The same apparatus was used in all experiments, but the procedures differed in the sensory modality of the feedback that participants (N s = 5, 5, 6, and 6, respectively, in Experiments 1, 2, 3, and 4) received about their performances. Using biased visual, proprioceptive, or verbal feedback, the authors introduced a 5° shift in the visuomanual relationship. Results showed no significant difference in the final amount of adaptation to the mismatch: On average, participants adapted to 79% of the perturbation. That finding is consistent with the view that adaptation is a multisensory, highly flexible process whose efficiency does not depend on the sensory channel conveying the error signal.

To transfer or not to transfer? Kinematics and laterality quotient predict interlimb transfer of motor learning

Humans can remarkably adapt their motor behavior to novel environmental conditions, yet it remains unclear which factors enable us to transfer what we have learned with one limb to the other. Here we tested the hypothesis that interlimb transfer of sensorimotor adaptation is determined by environmental conditions but also by individual characteristics. We specifically examined the adaptation of unconstrained reaching movements to a novel Coriolis, velocity-dependent force field. Right-handed subjects sat at the center of a rotating platform and performed forward reaching movements with the upper limb toward flashed visual targets in prerotation, per-rotation (i.e., adaptation), and postrotation tests. Here only the dominant arm was used during adaptation and interlimb transfer was assessed by comparing performance of the nondominant arm before and after dominant-arm adaptation. Vision and no-vision conditions did not significantly influence interlimb transfer of trajectory adaptation, which on average was significant but limited. We uncovered a substantial heterogeneity of interlimb transfer across subjects and found that interlimb transfer can be qualitatively and quantitatively predicted for each healthy young individual. A classifier showed that in our study, interlimb transfer could be predicted based on the subjects task performance, most notably motor variability during learning, and his or her laterality quotient. Positive correlations suggested that variability of motor performance and lateralization of arm movement control facilitate interlimb transfer. We further show that these individual characteristics can predict the presence and the magnitude of interlimb transfer of left-handers. Overall, this study suggests that individual characteristics shape the way the nervous system can generalize motor learning.

Do Visual and Vestibular Inputs Compensate for Somatosensory Loss in the Perception of Spatial Orientation? Insights from a Deafferented Patient

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° 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 vs. self-orientation.

Combined influence of visual scene and body tilt on arm pointing movements: gravity matters!

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.