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A Single Session of Robot-Controlled Proprioceptive Training Modulates Functional Connectivity of Sensory Motor Networks and Improves Reaching Accuracy in Chronic Stroke.

ABSTRACT: BACKGROUND:Passive robot-generated arm movements in conjunction with proprioceptive decision making and feedback modulate functional connectivity (FC) in sensory motor networks and improve sensorimotor adaptation in normal individuals. This proof-of-principle study investigates whether these effects can be observed in stroke patients. METHODS:A total of 10 chronic stroke patients with a range of stable motor and sensory deficits (Fugl-Meyer Arm score [FMA] 0-65, Nottingham Sensory Assessment [NSA] 10-40) underwent resting-state functional magnetic resonance imaging before and after a single session of robot-controlled proprioceptive training with feedback. Changes in FC were identified in each patient using independent component analysis as well as a seed region-based approach. FC changes were related to impairment and changes in task performance were assessed. RESULTS:A single training session improved average arm reaching accuracy in 6 and proprioception in 8 patients. Two networks showing training-associated FC change were identified. Network C1 was present in all patients and network C2 only in patients with FM scores >7. Relatively larger C1 volume in the ipsilesional hemisphere was associated with less impairment ( r = 0.83 for NSA, r = 0.73 for FMA). This association was driven by specific regions in the contralesional hemisphere and their functional connections (supramarginal gyrus with FM scores r = 0.82, S1 with NSA scores r = 0.70, and cerebellum with NSA score r = -0.82). CONCLUSION:A single session of robot-controlled proprioceptive training with feedback improved movement accuracy and induced FC changes in sensory motor networks of chronic stroke patients. FC changes are related to functional impairment and comprise bilateral sensory and motor network nodes.

SUBMITTER: Vahdat S

PROVIDER: S-EPMC6389407 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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A Single Session of Robot-Controlled Proprioceptive Training Modulates Functional Connectivity of Sensory Motor Networks and Improves Reaching Accuracy in Chronic Stroke.

Vahdat Shahabeddin S Darainy Mohammed M Thiel Alexander A Ostry David J DJ

Neurorehabilitation and neural repair 20181229 1

<h4>Background</h4>Passive robot-generated arm movements in conjunction with proprioceptive decision making and feedback modulate functional connectivity (FC) in sensory motor networks and improve sensorimotor adaptation in normal individuals. This proof-of-principle study investigates whether these effects can be observed in stroke patients.<h4>Methods</h4>A total of 10 chronic stroke patients with a range of stable motor and sensory deficits (Fugl-Meyer Arm score [FMA] 0-65, Nottingham Sensory ...[more]

PMID: 30595082

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Project description:This study examined the trainability of the proprioceptive sense and explored the relationship between proprioception and motor learning. With vision blocked, human learners had to perform goal-directed wrist movements relying solely on proprioceptive/haptic cues to reach several haptically specified targets. One group received additional somatosensory movement error feedback in form of vibro-tactile cues applied to the skin of the forearm. We used a haptic robotic device for the wrist and implemented a 3-day training regimen that required learners to make spatially precise goal-directed wrist reaching movements without vision. We assessed whether training improved the acuity of the wrist joint position sense. In addition, we checked if sensory learning generalized to the motor domain and improved spatial precision of wrist tracking movements that were not trained. The main findings of the study are: First, proprioceptive acuity of the wrist joint position sense improved after training for the group that received the combined proprioceptive/haptic and vibro-tactile feedback (VTF). Second, training had no impact on the spatial accuracy of the untrained tracking task. However, learners who had received VTF significantly reduced their reliance on haptic guidance feedback when performing the untrained motor task. That is, concurrent VTF was highly salient movement feedback and obviated the need for haptic feedback. Third, VTF can be also provided by the limb not involved in the task. Learners who received VTF to the contralateral limb equally benefitted. In conclusion, somatosensory training can significantly enhance proprioceptive acuity within days when learning is coupled with vibro-tactile sensory cues that provide feedback about movement errors. The observable sensory improvements in proprioception facilitates motor learning and such learning may generalize to the sensorimotor control of the untrained motor tasks. The implications of these findings for neurorehabilitation are discussed.

Project description:BackgroundNeurological injuries such as stroke often differentially impair hand motor and somatosensory function, as well as the interplay between the two, which leads to limitations in performing activities of daily living. However, it is challenging to identify which specific aspects of sensorimotor function are impaired based on conventional clinical assessments that are often insensitive and subjective. In this work we propose and validate a set of robot-assisted assessments aiming at disentangling hand proprioceptive from motor impairments, and capturing their interrelation (sensorimotor impairments).MethodsA battery of five complementary assessment tasks was implemented on a one degree-of-freedom end-effector robotic platform acting on the index finger metacarpophalangeal joint. Specifically, proprioceptive impairments were assessed using a position matching paradigm. Fast target reaching, range of motion and maximum fingertip force tasks characterized motor function deficits. Finally, sensorimotor impairments were assessed using a dexterous trajectory following task. Clinical feasibility (duration), reliability (intra-class correlation coefficient ICC, smallest real difference SRD) and validity (Kruskal-Wallis test, Spearman correlations [Formula: see text] with Fugl-Meyer Upper Limb Motor Assessment, kinesthetic Up-Down Test, Box & Block Test) of robotic tasks were evaluated with 36 sub-acute stroke subjects and 31 age-matched neurologically intact controls.ResultsEighty-three percent of stroke survivors with varied impairment severity (mild to severe) could complete all robotic tasks (duration: <15 min per tested hand). Further, the study demonstrated good to excellent reliability of the robotic tasks in the stroke population (ICC>0.7, SRD<30%), as well as discriminant validity, as indicated by significant differences (p-value<0.001) between stroke and control subjects. Concurrent validity was shown through moderate to strong correlations ([Formula: see text]=0.4-0.8) between robotic outcome measures and clinical scales. Finally, robotic tasks targeting different deficits (motor, sensory) were not strongly correlated with each other ([Formula: see text]0.32, p-value>0.1), thereby presenting complementary information about a patient's impairment profile.ConclusionsThe proposed robot-assisted assessments provide a clinically feasible, reliable, and valid approach to distinctly characterize impairments in hand proprioceptive and motor function, along with the interaction between the two. This opens new avenues to help unravel the contributions of unique aspects of sensorimotor function in post-stroke recovery, as well as to contribute to future developments towards personalized, assessment-driven therapies.

Project description:ObjectiveProprioceptive training is any intervention aiming to improve proprioceptive function with the ultimate goal to enhance motor function and performance. It has been promoted as an approach to enhance athletic performance and as a tool for sensorimotor rehabilitation. Numerous studies sought to provide evidence on the effectiveness of the approach. However, many different training regimes claiming to train proprioception report a variety of sensorimotor measures that are not directly comparable. This, in turn, makes it difficult to assess effectiveness across approaches. It is the objective of this study to systematically review recent empirical evidence to gain an understanding of which outcome measures are most sensitive, which populations may benefit most from proprioceptive training, and what are the effects on proprioceptive and motor systems.MethodsFour major databases were searched. The following inclusion criteria were applied: (1) A quantified pre- and post-treatment measure of proprioceptive function. (2) An intervention or training program believed to influence or enhance proprioceptive function. (3) Contained at least one form of treatment or outcome measure that is indicative of somatosensory function and not confounded by information from other sensory modalities. 4) The study reported of at least one quantified measure of motor performance.ResultsOf the 3,297 articles identified by the database search, 70 studies met the inclusion criteria and were included for further review. Across studies, proprioceptive training led to comparable gains in both proprioceptive (+46%) and motor performance (+45%). The majority of studies (50/70) applied active movement interventions. Interventions applying somatosensory stimulation were most successful in clinical populations. Joint position sense error (JPSE) was the most commonly used proprioceptive measure and presents a reliable and feasible measure for clinical use.ConclusionProprioceptive training can lead to significant improvements in proprioceptive and motor function across a range healthy and clinical populations. Regimens requiring active movement of the trainee tended to be most successful in improving sensorimotor performance. Conclusive evidence on how long training gains are retained is still lacking. There is no solid evidence about the underlying long-term neuroplastic changes associated proprioceptive training.

Project description:ObjectiveNumerous reports advocate that training of the proprioceptive sense is a viable behavioral therapy for improving impaired motor function. However, there is little agreement of what constitutes proprioceptive training and how effective it is. We therefore conducted a comprehensive, systematic review of the available literature in order to provide clarity to the notion of training the proprioceptive system.MethodsFour major scientific databases were searched. The following criteria were subsequently applied: (1) A quantified pre- and post-treatment measure of proprioceptive function. (2) An intervention or training program believed to influence or enhance proprioceptive function. (3) Contained at least one form of treatment or outcome measure that is indicative of somatosensory function. From a total of 1284 articles, 51 studies fulfilled all criteria and were selected for further review.ResultsOverall, proprioceptive training resulted in an average improvement of 52% across all outcome measures. Applying muscle vibration above 30 Hz for longer durations (i.e., min vs. s) induced outcome improvements of up to 60%. Joint position and target reaching training consistently enhanced joint position sense (up to 109%) showing an average improvement of 48%. Cortical stroke was the most studied disease entity but no clear evidence indicated that proprioceptive training is differentially beneficial across the reported diseases.ConclusionsThere is converging evidence that proprioceptive training can yield meaningful improvements in somatosensory and sensorimotor function. However, there is a clear need for further work. Those forms of training utilizing both passive and active movements with and without visual feedback tended to be most beneficial. There is also initial evidence suggesting that proprioceptive training induces cortical reorganization, reinforcing the notion that proprioceptive training is a viable method for improving sensorimotor function.

Project description:The study aimed to determine whether four weeks of motor imagery training (MIT) of goal-directed reaching (reaching to grasp task) would affect the cortical activity during motor imagery of reaching (MIR) and grasping (MIG) in the same way. We examined cortical activity regarding event-related potentials (ERPs) in healthy young participants. Our study also evaluated the subjective vividness of the imagery. Furthermore, we aimed to determine the relationship between the subjective assessment of motor imagery (MI) ability to reach and grasp and the cortical activity during those tasks before and after training to understand the underlying neuroplasticity mechanisms. Twenty-seven volunteers participated in MIT of goal-directed reaching and two measurement sessions before and after MIT. During the sessions 128-channel electroencephalography (EEG) was recorded during MIR and MIG. Also, participants assessed the vividness of the MI tasks using a visual analog scale (VAS). The vividness of imagination improved significantly (P < .05) after MIT. A repeated measures ANOVA showed that the task (MIR/MIG) and the location of electrodes had a significant effect on the ERP's amplitude (P < .05). The interaction between the task, location, and session (before/after MIT) also had a significant effect on the ERP's amplitude (P < .05). Finally, the location of electrodes and the interaction between location and session had a significant effect on the ERP's latency (P < .05). We found that MIT influenced the EEG signal associated with reaching differently than grasping. The effect was more pronounced for MIR than for MIG. Correlation analysis showed that changes in the assessed parameters due to MIT reduced the relationship between the subjective evaluation of imagining and the EEG signal. This finding means that the subjective evaluation of imagining cannot be a simple, functional insight into the bioelectrical activity of the cerebral cortex expressed by the ERPs in mental training. The changes we noted in ERPs after MIT may benefit the use of non-invasive EEG in the brain-computer interface (BCI) context.Trial registration: NCT04048083.

Project description:Detecting and evaluating errors in action execution is essential for learning. Through complex interactions of the inverse and the forward model, the human motor system can predict and subsequently adjust ongoing or subsequent actions. Inputs to such a prediction are efferent and afferent signals from various sources. The aim of the current study was to examine the impact of visual as well as a combination of efferent and proprioceptive input signals to error prediction in a complex motor task. Predicting motor errors has been shown to be correlated with a neural signal known as the error-related negativity (Ne/ERN). Here, we tested how the Ne/ERN amplitude was modulated by the availability of different sensory signals in a semi-virtual throwing task where the action outcome (hit or miss of the target) was temporally delayed relative to movement execution allowing participants to form predictions about the outcome prior to the availability of knowledge of results. 19 participants practiced the task and electroencephalogram was recorded in two test conditions. In the Visual condition, participants received only visual input by passively observing the throwing movement. In the EffProp condition, participants actively executed the task while visual information about the real and the virtual effector was occluded. Hence, only efferent and proprioceptive signals were available. Results show a significant modulation of the Ne/ERN in the Visual condition while no effect could be observed in the EffProp condition. In addition, amplitudes of the feedback-related negativity in response to the actual outcome feedback were found to be inversely related to the Ne/ERN amplitudes. Our findings indicate that error prediction is modulated by the availability of input signals to the forward model. The observed amplitudes were found to be attenuated in comparison to previous studies, in which all efferent and sensory inputs were present. Furthermore, we assume that visual signals are weighted higher than proprioceptive signals, at least in goal-oriented tasks with visual targets.

Dataset Information

A Single Session of Robot-Controlled Proprioceptive Training Modulates Functional Connectivity of Sensory Motor Networks and Improves Reaching Accuracy in Chronic Stroke.

Publications

A Single Session of Robot-Controlled Proprioceptive Training Modulates Functional Connectivity of Sensory Motor Networks and Improves Reaching Accuracy in Chronic Stroke.

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