Minimal impact of chronic proprioceptive loss on implicit sensorimotor adaptation and perceived movement outcome.

Implicit sensorimotor adaptation keeps our movements well calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual realignment model, implicit adaptation ceases when the perceived movement outcome-a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision-is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who experience deafferentation (i.e., individuals with impaired proprioception and touch). We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived movement outcomes throughout the experiment. Surprisingly, both implicit adaptation and perceived movement outcome were minimally impacted by chronic deafferentation, posing a challenge to the perceptual realignment model of implicit adaptation.NEW & NOTEWORTHY We tested six individuals with chronic somatosensory deafferentation on a novel task that isolates implicit sensorimotor adaptation and probes perceived movement outcome. Strikingly, both implicit motor adaptation and perceptual movement outcome were not significantly impacted by chronic deafferentation, posing a challenge for theoretical models of adaptation that involve proprioception.

Role of proprioception in corrective visually-guided movements: larger movement errors in both arms of a deafferented individual compared to control participants.

Proprioception plays an important role in both feedforward and feedback processes underlying movement control. This has been shown with individuals who suffered a profound proprioceptive loss and use vision to partially compensate for the sensory loss. The purpose of this study was to specifically examine the role of proprioception in feedback motor responses to visual perturbations by examining voluntary arm movements in an individual with a rare case of selective peripheral deafferentation (GL). We compared her left and right hand movements with those of age-matched female control participants (70.0 years ± 0.2 SEM) during a reaching task. Participants were asked to move their unseen hand, represented by a cursor on the screen, quickly and accurately to reach a visual target. A visual perturbation could be pseudorandomly applied, at movement onset, to either the target position (target jump) or the cursor position (cursor jump). Results showed that despite the continuous visual feedback that was provided, GL produced larger errors in final position accuracy compared to control participants, with her left nondominant hand being more erroneous after a cursor jump. We also found that the proprioceptively-deafferented individual produced less spatially efficient movements than the control group. Overall, these results provide evidence of a heavier reliance on proprioceptive feedback for movements of the nondominant hand relative to the dominant hand, supporting the view of a lateralization of the feedback processes underlying motor control.

Dissociation between dreams and wakefulness: Insights from body and action representations of rare individuals with massive somatosensory deafferentation.

The realism of body and actions in dreams is thought to be induced by simulations based on internal representations used during wakefulness. As somatosensory signals contribute to the updating of body and action representations, these are impaired when somatosensory signals are lacking. Here, we tested the hypothesis that individuals with somatosensory deafferentation have impaired body and actions in their dreams, as in wakefulness. We questioned three individuals with a severe, acquired sensory neuropathy on their dreams. While deafferented participants were impaired in daily life, they could dream of themselves as able-bodied, with some sensations (touch, proprioception) and actions (such as running or jumping) which had not been experienced in physical life since deafferentation. We speculate that simulation in dreams could be based on former, "healthy" body and action representations. Our findings are consistent with the idea that distinct body and action representations may be used during dreams and wakefulness.

Anticipation and compensation for somatosensory deficits in object handling: evidence from a patient with large fiber sensory neuropathy.

The purpose of this study was to determine the contributions of feedforward and feedback processes on grip force regulation and object orientation during functional manipulation tasks. One patient with massive somatosensory loss resulting from large fiber sensory neuropathy and 10 control participants were recruited. Three experiments were conducted: 1) perturbation to static holding; 2) discrete vertical movement; and 3) functional grasp and place. The availability of visual feedback was also manipulated to assess the nature of compensatory mechanisms. Results from experiment 1 indicated that both the deafferented patient and controls used anticipatory grip force adjustments before self-induced perturbation to static holding. The patient exhibited increased grip response time, but the magnitude of grip force adjustments remained correlated with perturbation forces in the self-induced and external perturbation conditions. In experiment 2, the patient applied peak grip force substantially in advance of maximum load force. Unlike controls, the patient's ability to regulate object orientation was impaired without visual feedback. In experiment 3, the duration of unloading, transport, and release phases were longer for the patient, with increased deviation of object orientation at phase transitions. These findings show that the deafferented patient uses distinct modes of anticipatory control according to task constraints and that responses to perturbations are mediated by alternative afferent information. The loss of somatosensory feedback thus appears to impair control of object orientation, whereas variation in the temporal organization of functional tasks may reflect strategies to mitigate object instability associated with changes in movement dynamics.NEW & NOTEWORTHY This study evaluates the effects of sensory neuropathy on the scaling and timing of grip force adjustments across different object handling tasks (i.e., holding, vertical movement, grasping, and placement). In particular, these results illustrate how novel anticipatory and online control processes emerge to compensate for the loss of somatosensory feedback. In addition, we provide new evidence on the role of somatosensory feedback for regulating object orientation during functional prehensile movement.

Opposing force fields induce direction-specific sensorimotor adaptation but a non-specific perceptual shift consistent with a contraction of peripersonal space representation.

Most of our daily interactions with objects occur in the space immediately surrounding the body, i.e. the peripersonal space. The peripersonal space is characterized by multisensory processing of objects which are coded in terms of potential actions, specifying for instance whether objects are within reach or not. Our recent work suggested a link between exposure to a new force field, which changed the effector dynamics, and the representation of peripersonal space. To better understand the interplay between the plasticity of the motor system and peripersonal space representation, the present study examined whether changing the direction of the force field specifically modified the perception of action boundaries. Participants seated at the centre of an experimental platform estimated visual targets' reachability before and after adapting upper-limb reaching movements to the Coriolis force generated by either clockwise or counter clockwise rotation of the platform (120°/s). Opposite spatial after-effects were observed, showing that force-field adaptation depends on the direction of the rotation. In contrast, perceived action boundaries shifted leftward following exposure to the new force field, regardless of the direction of the rotation. Overall, these findings support the idea that abrupt exposure to a new force field results in a direction-specific updating of the central sensorimotor representations underlying the control of arm movements. Abrupt exposure to a new force field also results in a nonspecific shift in the perception of action boundaries, which is consistent with a contraction of the peripersonal space. Such effect, which does not appear to be related to state anxiety, could be related to the protective role of the peripersonal space in response to the uncertainty of the sensorimotor system induced by the abrupt modification of the environment.

Individual movement features during prism adaptation correlate with after-effects and interlimb transfer.

The human nervous system displays such plasticity that we can adapt our motor behavior to various changes in environmental or body properties. However, how sensorimotor adaptation generalizes to new situations and new effectors, and which factors influence the underlying mechanisms, remains unclear. Here we tested the general hypothesis that differences across participants can be exploited to uncover what drives interlimb transfer. Twenty healthy adults adapted to prismatic glasses while reaching to visual targets with their dominant arm. Classic adaptation and generalization across movement directions were observed but transfer to the non-dominant arm was not significant and inter-individual differences were substantial. Interlimb transfer resulted for some participants in a directional shift of non-dominant arm movements that was consistent with an encoding of visuomotor adaptation in extrinsic coordinates. For some other participants, transfer was consistent with an intrinsic coordinate system. Simple and multiple regression analyses showed that a few kinematic parameters such as peak acceleration (or peak velocity) and variability of movement direction were correlated with interlimb transfer. Low peak acceleration and low variability were related to extrinsic transfer, while high peak acceleration and high variability were related to intrinsic transfer. Motor variability was also positively correlated with the magnitude of the after-effect systematically observed on the dominant arm. Overall, these findings on unconstrained movements support the idea that individual movement features could be linked to the sensorimotor adaptation and its generalization. The study also suggests that distinct movement characteristics may be related to different coordinate frames of action representations in the nervous system.

Case Studies in Neuroscience: The central and somatosensory contributions to finger interdependence and coordination: lessons from a study of a "deafferented person".

We tested finger force interdependence and multifinger force-stabilizing synergies in a patient with large-fiber peripheral neuropathy ("deafferented person"). The subject performed a range of tasks involving accurate force production with one finger and with four fingers. In one-finger tasks, nontask fingers showed unintentional force production (enslaving) with an atypical pattern: very large indices for the lateral (index and little) fingers and relatively small indices for the central (middle and ring) fingers. Indices of multifinger synergies stabilizing total force and of anticipatory synergy adjustments in preparation to quick force pulses were similar to those in age-matched control females. During constant force production, removing visual feedback led to a slow force drift to lower values (by ~25% over 15 s). The results support the idea of a neural origin of enslaving and suggest that the patterns observed in the deafferented person were reorganized based on everyday manipulation tasks. The lack of significant changes in the synergy index shows that synergic control can be organized in the absence of somatosensory feedback. We discuss the control of the hand in deafferented persons within the α-model of the equilibrium-point hypothesis and suggest that force drift results from an unintentional drift of the control variables to muscles toward zero values. NEW & NOTEWORTHY We demonstrate atypical patterns of finger enslaving and unchanged force-stabilizing synergies in a person with large-fiber peripheral neuropathy. The results speak strongly in favor of central origin of enslaving and its reorganization based on everyday manipulation tasks. The data show that synergic control can be implemented in the absence of somatosensory feedback. We discuss the control of the hand in deafferented persons within the α-model of the equilibrium-point hypothesis.

Loss of haptic feedback impairs control of hand posture: a study in chronically deafferented individuals when grasping and lifting objects.

Previous work has highlighted the role of haptic feedback for manual dexterity, in particular for the control of precision grip forces between the index finger and thumb. It is unclear how fine motor skills involving more than just two digits might be affected, especially given that loss of sensation from the hand affects many neurological patients, and impacts on everyday actions. To assess the functional consequences of haptic deficits on multi-digit grasp of objects, we studied the ability of three rare individuals with permanent large-fibre sensory loss involving the entire upper limb. All three reported difficulties in everyday manual actions (ABILHAND questionnaire). Their performance in a reach-grasp-lift task was compared to that of healthy controls. Twenty objects of varying shape, mass, opacity and compliance were used. In the reach-to-grasp phase, we found slower movement, larger grip aperture and less dynamic modulation of grip aperture in deafferented participants compared to controls. Hand posture during the lift phase also differed; deafferented participants often adopted hand postures that may have facilitated visual guidance, and/or reduced control complexity. For example, they would extend fingers that were not in contact with the object, or fold these fingers into the palm of the hand. Variability in hand postures was increased in deafferented participants, particularly for smaller objects. Our findings provide new insights into how the complex control required for whole hand actions is compromised by loss of haptic feedback, whose contribution is, thus, highlighted.

Proprioceptive loss and the perception, control and learning of arm movements in humans: evidence from sensory neuronopathy.

It is uncertain how vision and proprioception contribute to adaptation of voluntary arm movements. In normal participants, adaptation to imposed forces is possible with or without vision, suggesting that proprioception is sufficient; in participants with proprioceptive loss (PL), adaptation is possible with visual feedback, suggesting that proprioception is unnecessary. In experiment 1 adaptation to, and retention of, perturbing forces were evaluated in three chronically deafferented participants. They made rapid reaching movements to move a cursor toward a visual target, and a planar robot arm applied orthogonal velocity-dependent forces. Trial-by-trial error correction was observed in all participants. Such adaptation has been characterized with a dual-rate model: a fast process that learns quickly, but retains poorly and a slow process that learns slowly and retains well. Experiment 2 showed that the PL participants had large individual differences in learning and retention rates compared to normal controls. Experiment 3 tested participants' perception of applied forces. With visual feedback, the PL participants could report the perturbation's direction as well as controls; without visual feedback, thresholds were elevated. Experiment 4 showed, in healthy participants, that force direction could be estimated from head motion, at levels close to the no-vision threshold for the PL participants. Our results show that proprioceptive loss influences perception, motor control and adaptation but that proprioception from the moving limb is not essential for adaptation to, or detection of, force fields. The differences in learning and retention seen between the three deafferented participants suggest that they achieve these tasks in idiosyncratic ways after proprioceptive loss, possibly integrating visual and vestibular information with individual cognitive strategies.

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 subject's 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.

Minimal impact of proprioceptive loss on implicit sensorimotor adaptation and perceived movement outcome.

Implicit sensorimotor adaptation keeps our movements well-calibrated amid changes in the body and environment. We have recently postulated that implicit adaptation is driven by a perceptual error: the difference between the desired and perceived movement outcome. According to this perceptual re-alignment model, implicit adaptation ceases when the perceived movement outcome - a multimodal percept determined by a prior belief conveying the intended action, the motor command, and feedback from proprioception and vision - is aligned with the desired movement outcome. Here, we examined the role of proprioception in implicit motor adaptation and perceived movement outcome by examining individuals who lack proprioception. We used a modified visuomotor rotation task designed to isolate implicit adaptation and probe perceived outcome throughout the experiment. Surprisingly, implicit adaptation and perceived outcome were minimally impacted by deafferentation, posing a challenge to the perceptual re-alignment model of implicit adaptation.

Does visual experience influence arm proprioception and its lateralization? Evidence from passive matching performance in congenitally-blind and sighted adults.

In humans, body segments' position and movement can be estimated from multiple senses such as vision and proprioception. It has been suggested that vision and proprioception can influence each other and that upper-limb proprioception is asymmetrical, with proprioception of the non-dominant arm being more accurate and/or precise than proprioception of the dominant arm. However, the mechanisms underlying the lateralization of proprioceptive perception are not yet understood. Here we tested the hypothesis that early visual experience influences the lateralization of arm proprioceptive perception by comparing 8 congenitally-blind and 8 matched, sighted right-handed adults. Their proprioceptive perception was assessed at the elbow and wrist joints of both arms using an ipsilateral passive matching task. Results support and extend the view that proprioceptive precision is better at the non-dominant arm for blindfolded sighted individuals. While this finding was rather systematic across sighted individuals, proprioceptive precision of congenitally-blind individuals was not lateralized as systematically, suggesting that lack of visual experience during ontogenesis influences the lateralization of arm proprioception.

Gradual exposure to Coriolis force induces sensorimotor adaptation with no change in peripersonal space.

The space immediately surrounding the body is crucial for the organization of voluntary motor actions and seems to be functionally represented in the brain according to motor capacities. However, despite extensive research, little is known about how the representation of peripersonal space is adjusted to new action capacities. Abrupt exposure to a new force field has been shown to cause the representation of peripersonal space to shrink, possibly reflecting a conservative spatial strategy triggered by consciously-perceived motor errors. The present study assessed whether the representation of peripersonal space is influenced by gradual exposure of reaching movements to a new force field, produced by a stepwise acceleration of a rotating platform. We hypothesized that such gradual exposure would induce progressive sensorimotor adaptation to motor errors, albeit too small to be consciously perceived. In contrast, we hypothesized that reachability judgments, used as a proxy of peripersonal space representation, would not be significantly affected. Results showed that gradual exposure to Coriolis force produced a systematic after-effect on reaching movements but no significant change in reachability judgments. We speculate that the conscious experience of large motor errors may influence the updating of the representation of peripersonal space.

Joint Specificity and Lateralization of Upper Limb Proprioceptive Perception.

Proprioception is the sense of position and movement of body segments. The widespread distribution of proprioceptors in human anatomy raises questions about proprioceptive uniformity across different body parts. For the upper limbs, previous research, using mostly active and/or contralateral matching tasks, has suggested better proprioception of the non-preferred arm, and at the elbow rather than the wrist. Here we assessed proprioceptive perception through an ipsilateral passive matching task by comparing the elbow and wrist joints of the preferred and non-preferred arms. We hypothesized that upper limb proprioception would be better at the elbow of the non-preferred arm. We found signed errors to be less variable at the non-preferred elbow than at the preferred elbow and both wrists. Signed errors at the elbow were also more stable than at the wrist. Across individuals, signed errors at the preferred and non-preferred elbows were correlated. Also, variable signed errors at the preferred wrist, non-preferred wrist, and preferred elbow were correlated. These correlations suggest that an individual with relatively consistent matching errors at one joint may have relatively consistent matching errors at another joint. Our findings also support the view that proprioceptive perception varies across upper limb joints, meaning that a single joint assessment is insufficient to provide a general assessment of an individual's proprioception.

A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination.

Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.

Somatosensory deafferentation reveals lateralized roles of proprioception in feedback and adaptive feedforward control of movement and posture.

Proprioception provides crucial information necessary for determining limb position and movement, and plausibly also for updating internal models that might underlie the control of movement and posture. Seminal studies of upper-limb movements in individuals living with chronic, large fiber deafferentation have provided evidence for the role of proprioceptive information in the hypothetical formation and maintenance of internal models to produce accurate motor commands. Vision also contributes to sensorimotor functions but cannot fully compensate for proprioceptive deficits. More recent work has shown that posture and movement control processes are lateralized in the brain, and that proprioception plays a fundamental role in coordinating the contributions of these processes to the control of goal-directed actions. In fact, the behavior of each limb in a deafferented individual resembles the action of a controller in isolation. Proprioception, thus, provides state estimates necessary for the nervous system to efficiently coordinate multiple motor control processes.

Interlimb Transfer of Reach Adaptation Does Not Require an Intact Corpus Callosum: Evidence from Patients with Callosal Lesions and Agenesis.

Generalization of sensorimotor adaptation across limbs, known as interlimb transfer, is a well-demonstrated phenomenon in humans, yet the underlying neural mechanisms remain unclear. Theoretical models suggest that interlimb transfer is mediated by interhemispheric transfer of information via the corpus callosum. We thus hypothesized that lesions of the corpus callosum, especially to its midbody connecting motor, supplementary motor, and premotor areas of the two cerebral hemispheres, would impair interlimb transfer of sensorimotor adaptation. To test this hypothesis, we recruited three patients: two rare stroke patients with recent, extensive callosal lesions including the midbody and one patient with complete agenesis. A prismatic adaptation paradigm involving unconstrained arm reaching movements was designed to assess interlimb transfer from the prism-exposed dominant arm (DA) to the unexposed non-dominant arm (NDA) for each participant. Baseline results showed that spatial performance of each patient did not significantly differ from controls, for both limbs. Further, each patient adapted to the prismatic perturbation, with no significant difference in error reduction compared with controls. Crucially, interlimb transfer was found in each patient. The absolute magnitude of each patient's transfer did not significantly differ from controls. These findings show that sensorimotor adaptation can transfer across limbs despite extensive lesions or complete absence of the corpus callosum. Therefore, callosal pathways connecting homologous motor, premotor, and supplementary motor areas are not necessary for interlimb transfer of prismatic reach adaptation. Such interlimb transfer could be mediated by transcallosal splenium pathways (connecting parietal, temporal and visual areas), ipsilateral cortico-spinal pathways or subcortical structures such as the cerebellum.

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.

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.

The roles of vision and proprioception in the planning of reaching movements.

While vision and proprioception can both provide information about arm configuration prior to movement, substantial evidence suggests that each modality is used for different stages of the planning process. In this chapter, we provide support for the idea that vision is mainly used to define the trajectory and the kinematics of reaching movements. Proprioception appears to be critical in the transformation of this plan into the motor commands sent to the arm muscles.