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

© 2018 The Author(s) 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

Le transfert d'adaptation entre les membres : facteurs prédictifs et processus

L’adaptation motrice renvoie à la capacité de notre système nerveux à produire continuellement des mouvements précis et ce malgré le fait que notre environnement ainsi que notre corps puissent être soumis à des modifications. Le transfert d’adaptation entre les membres découle de notre habilité à généraliser ce que l’on a appris, par exemple, avec un bras au bras opposé. Le transfert entre les membres est un objet d’étude complexe. Les conditions amenant au transfert sont largement débattues dans la littérature car les résultats d’une étude à l’autre peuvent être contradictoires. Ce travail de thèse s’inscrit dans une tentative d’apporter une explication concernant l’hétérogénéité des performances et les divergences observées dans les différentes études portant sur le transfert entre les membres. Les deux premières expériences avaient pour but d’identifier si des conditions paradigmatiques ou idiosyncratiques pouvaient influencer les performances du transfert au bras opposé. L’objectif de la troisième expérience était d’étudier l’influence des processus sous-jacents à l’adaptation sur le transfert entre les membres d’après le modèle de Smith et collaborateurs (2006). Nos résultats nous ont permis d’éclaircir certains aspects du transfert concernant les facteurs prédictifs et les processus mis en jeu. Nos deux premières études suggèrent que les différences individuelles sont une source d’information pertinente pour expliquer certains comportements tels que le transfert entre les membres. Notre troisième étude nous a permis de caractériser les processus qui, durant l’adaptation, prédisposent au transfert.Motor adaptation refers to the capacity of our nervous system to produce accurate movements while the properties of our body and our environment continuously change. Interlimb transfer is a process that directly stems from motor adaptation. It occurs when knowledge gained through training with one arm change the performance of the opposite arm movements. Interlimb transfer of adaptation is an intricate process. Numerous studies have investigated the patterns of transfer and conflicted results have been found. The attempt of my PhD project was to identify which factors and processes favor interlimb transfer of adaptation and thence may explain the discrepancies found in the literature. The first two experiments aimed at investigated whether paradigmatic or idiosyncratic features would influence the performance in interlimb transfer. The third experiment provided some insights on the processes allowing interlimb transfer by using the dual-rate model of adaptation put forth by Smith et al. (2006). Our results show that inter-individual differences may be a key factor to consider when studying interlimb transfer of adaptation. Also, the study of the different sub-processes of adaptation seems helpful to understand how interlimb transfer works and how it can be related to other behaviors such as the expression of motor memory

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

International audienceThe 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

Generalization of force-field adaptation in proprioceptively-deafferented subjects

International audienceHumans have the remarkable ability to adapt their motor behaviour to changes in body properties and/or environmental conditions, based on sensory feedback such as vision and proprioception. The role of proprioception has been highlighted for the adaptation to new upper-limb dynamics, which is known to generalize to the opposite, non-adapted limb in healthy individuals. Such interlimb transfer seems to depend on sensory feedback, and the present study assessed whether the chronic loss of proprioception precludes interlimb transfer of dynamic adaptation by testing two well-characterized proprioceptively-deafferented subjects. These had to reach toward visual targets with vision of the limb. For both deafferented subjects, we observed adaptation of the dominant arm to Coriolis forces and aftereffects on non-dominant arm movements in different movement directions, thus indicating interlimb transfer. Overall, our findings show that motor learning can generalize across limbs and movement directions despite the loss of proprioceptive afferents. (C) 2016 Elsevier Ireland Ltd. All rights reserved

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

International audienceHumans 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 post- rotation 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