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

Jayasinghe, Shanie A. L.; Sarlegna, Fabrice R.; Scheidt, Robert A.; Sainburg, Robert L.

doi:10.1016/j.cophys.2020.10.005

Cited by 23 publications

(17 citation statements)

References 47 publications

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“…The role of proprioception in motor control has been well documented, notably for postural stability, motor coordination, and fine motor skills (Gandevia & Burke, 1992;Pearson, 2001;Scott, 2016). The role of proprioception with and without visual feedback has been well-illustrated by the consequences of proprioceptive loss on motor functions (Jayasinghe et al, 2021;Rothwell et al, 1982;Sarlegna et al, 2006Sarlegna et al, , 2010. Considering the critical role of proprioception in the perception and control of postures and movements and considering the body's widespread proprioceptors, a key question is "Is proprioception uniform across the body?…”

Section: Introductionmentioning

confidence: 99%

Joint Specificity and Lateralization of Upper Limb Proprioceptive Perception

et al. 2022

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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.

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Section: Introductionmentioning

confidence: 99%

Joint Specificity and Lateralization of Upper Limb Proprioceptive Perception

et al. 2022

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“…Handedness is a particular aspect of motor control referring to the preferential employment of a hand -the dominant one -to perform daily-life tasks. Asymmetries in the neural organization of cerebral hemispheres could explain inter-limb differences in the control of arm movements (Carson et al 1992;Flowers 1975;Jayasinghe et al 2021;Roy et al 1994;Roy and Elliott 1986;Sainburg 2002Sainburg , 2014Woytowicz et al 2018). A large body of literature suggests that the dominant arm/hemisphere is specialized for open-loop optimization-like processes, whilst the non-dominant arm/hemisphere is specialized for closed-loop control that stabilized arm postures against unexpected environmental conditions (Bagesteiro and Sainburg 2002;Sainburg 2002;Schaffer and Sainburg 2017;Sainburg 2011, 2014).…”

Section: Introductionmentioning

confidence: 99%

Muscle effort is best minimized by the right-dominant arm in the gravity field

Poirier

Lebigre

Mourey

et al. 2021

Preprint

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The central nervous system (CNS) is thought to develop motor strategies that minimize various hidden criteria, such as end-point variance or effort. A large body of literature suggests that the dominant arm is specialized for such open-loop optimization-like processes whilst the non-dominant arm is specialized for closed-loop control. Building on recent results suggesting that the brain plans arm movements that takes advantage of gravity effects to minimize muscle effort, the present study tests the hypothesized superiority of the dominant arm motor system for effort minimization. Thirty participants (22.5 ± 2.1 years old; all right-handed) performed vertical arm movements between two targets (40° amplitude), in two directions (upwards and downwards) with their two arms (dominant and non-dominant). We recorded the arm kinematics and the electromyographic activity of the anterior and posterior deltoid to compare two motor signatures of the gravity-related optimization process; i.e., directional asymmetries and negative epochs on phasic muscular activity. We found that these motor signatures were still present during movements performed with the non-dominant arm, indicating that the effort-minimization process also occurs for the non-dominant motor system. However, these markers were reduced compared with movements performed with the dominant arm. This difference was especially prominent during downward movements, where the optimization of gravity effects occurs early in the movement. Assuming that the dominant arm is optimal to minimize muscle effort, as suggested by previous studies, the present results support the hypothesized superiority of the dominant arm motor system for effort-minimization.

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“…They observed that damage to the left hemisphere led to deficits in trajectory control, whereas as damage to the right hemisphere led to deficits in final position control. More recently, studies on somatosensory deafferentation also revealed lateralized roles of proprioceptive feedback (Jayasinghe et al, 2020(Jayasinghe et al, , 2021, with the right arm failing to stabilize at the end-point of the reaching movement and the left arm showing poor corrections of the trajectory. However, other results have shown that the two arms can develop feedforward adaptation equally well in an experiment in which participants performed fast straight reaching movements, with similar force fields to our experiments (Reuter et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Different Control Strategies Drive Interlimb Differences in Performance and Adaptation during Reaching Movements in Novel Dynamics

Bulens

Cluff

Blondeau

et al. 2023

eNeuro

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Humans exhibit lateralization such that most individuals typically show a preference for using one arm over the other for a range of movement tasks. The computational aspects of movement control leading to these differences in skill are not yet understood. It has been hypothesized that the dominant and non-dominant arms differ in terms of the use of predictive or impedance control mechanisms. However, previous studies present confounding factors that prevented clear conclusions: either the performances were compared across two different groups, or in a design in which asymmetrical transfer between limbs could take place. To address these concerns, we studied a reach adaptation task during which healthy volunteers performed movements with their right and left arms in random order. We performed two experiments. Experiment 1 (18 participants) focused on adaptation to the presence of a perturbing force field and Experiment 2 (12 participants) focused on rapid adaptations in feedback responses. The randomization of the left and right arm led to simultaneous adaptation, allowing us to study lateralization in single individuals with symmetrical and minimal transfer between limbs. This design revealed that participants could adapt control of both arms, with both arms showing similar performance levels. The non-dominant arm initially presented a slightly worst performance but reached similar levels of performance in late trials. We also observed that the non-dominant arm showed a different control strategy compatible with robust control when adapting to the force field perturbation. EMG data showed that these differences in control were not caused by differences in co-contraction across the arms. Thus, instead of assuming differences in predictive or reactive control schemes, our data show that in the context of optimal control, both arms can adapt, and that the non-dominant arm uses a more robust, model-free strategy likely to compensate for less accurate internal representations of movement dynamics.Significance statementWe studied a reach adaptation task during which volunteers performed the task with their right and left arm randomly. The randomization of the arms allowed us to study lateralization in single individuals with symmetrical and minimal transfer between limbs. We observed similar performance levels after adaptation of both arms in the force applied to counter the perturbation. Moreover, the non-dominant arm showed a more robust control strategy when adapting to the force field perturbation, which enabled similar deviations despite faster movements. These interlimb differences were not caused by differences in co-contraction across the two arms. Our results suggest that both arms can adapt to the presence of a force field but the non-dominant arm uses a more robust, model-free strategy.

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

Cited by 23 publications

References 47 publications

Joint Specificity and Lateralization of Upper Limb Proprioceptive Perception

Joint Specificity and Lateralization of Upper Limb Proprioceptive Perception

Muscle effort is best minimized by the right-dominant arm in the gravity field

Different Control Strategies Drive Interlimb Differences in Performance and Adaptation during Reaching Movements in Novel Dynamics

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