Effects of a robot-aided somatosensory training on proprioception and motor function in stroke survivors.

BACKGROUND: Proprioceptive deficits after stroke are associated with poor upper limb function, slower motor recovery, and decreased self-care ability. Improving proprioception should enhance motor control in stroke survivors, but current evidence is inconclusive. Thus, this study examined whether a robot-aided somatosensory-based training requiring increasingly accurate active wrist movements improves proprioceptive acuity as well as motor performance in chronic stroke. METHODS: Twelve adults with chronic stroke completed a 2-day training (age range: 42-74 years; median time-after-stroke: 12 months; median Fugl-Meyer UE: 65). Retention was assessed at Day 5. Grasping the handle of a wrist-robotic exoskeleton, participants trained to roll a virtual ball to a target through continuous wrist adduction/abduction movements. During training vision was occluded, but participants received real-time, vibro-tactile feedback on their forearm about ball position and speed. Primary outcome was the just-noticeable-difference (JND) wrist position sense threshold as a measure of proprioceptive acuity. Secondary outcomes were spatial error in an untrained wrist tracing task and somatosensory-evoked potentials (SEP) as a neural correlate of proprioceptive function. Ten neurologically-intact adults were recruited to serve as non-stroke controls for matched age, gender and hand dominance (age range: 44 to 79 years; 6 women, 4 men). RESULTS: Participants significantly reduced JND thresholds at posttest and retention (Stroke group: pretest: mean: 1.77° [SD: 0.54°] to posttest mean: 1.38° [0.34°]; Control group: 1.50° [0.46°] to posttest mean: 1.45° [SD: 0.54°]; F[2,37] = 4.54, p = 0.017, ηp2 = 0.20) in both groups. A higher pretest JND threshold was associated with a higher threshold reduction at posttest and retention (r = - 0.86, - 0.90, p ≤ 0.001) among the stroke participants. Error in the untrained tracing task was reduced by 22 % at posttest, yielding an effect size of w = 0.13. Stroke participants exhibited significantly reduced P27-N30 peak-to-peak SEP amplitude at pretest (U = 11, p = 0.03) compared to the non-stroke group. SEP measures did not change systematically with training. CONCLUSIONS: This study provides proof-of-concept that non-visual, proprioceptive training can induce fast, measurable improvements in proprioceptive function in chronic stroke survivors. There is encouraging but inconclusive evidence that such somatosensory learning transfers to untrained motor tasks. Trial registration Clinicaltrials.gov; Registration ID: NCT02565407; Date of registration: 01/10/2015; URL: https://clinicaltrials.gov/ct2/show/NCT02565407 .

Audio-Motor Training Enhances Auditory and Proprioceptive Functions in the Blind Adult.

Several reports indicate that spatial perception in blind individuals can be impaired as the lack of visual experience severely affects the development of multisensory spatial correspondences. Despite the growing interest in the development of technological devices to support blind people in their daily lives, very few studies have assessed the benefit of interventions that help to refine sensorimotor perception. In the present study, we directly investigated the impact of a short audio-motor training on auditory and proprioceptive spatial perception in blind individuals. Our findings indicate that auditory and proprioceptive spatial capabilities can be enhanced through interventions designed to foster sensorimotor perception in the form of audio-motor correspondences, demonstrating the importance of the early introduction of sensorimotor training in therapeutic intervention for blind individuals.

Audio motor training improves mobility and spatial cognition in visually impaired children.

Since it has been demonstrated that spatial cognition can be affected in visually impaired children, training strategies that exploit the plasticity of the human brain should be early adopted. Here we developed and tested a new training protocol based on the reinforcement of audio-motor associations and thus supporting spatial development in visually impaired children. The study involved forty-four visually impaired children aged 6-17 years old assigned to an experimental (ABBI training) or a control (classical training) rehabilitation conditions. The experimental training group followed an intensive but entertaining rehabilitation for twelve weeks during which they performed ad-hoc developed audio-spatial exercises with the Audio Bracelet for Blind Interaction (ABBI). A battery of spatial tests administered before and after the training indicated that children significantly improved in almost all the spatial aspects considered, while the control group didn't show any improvement. These results confirm that perceptual development in the case of blindness can be enhanced with naturally associated auditory feedbacks to body movements. Therefore the early introduction of a tailored audio-motor training could potentially prevent spatial developmental delays in visually impaired children.

Audio Feedback Associated With Body Movement Enhances Audio and Somatosensory Spatial Representation.

In the last years, the positive impact of sensorimotor rehabilitation training on spatial abilities has been taken into account, e.g., providing evidence that combined multimodal compared to unimodal feedback improves responsiveness to spatial stimuli. To date, it still remains unclear to which extent spatial learning is influenced by training conditions. Here we investigated the effects of active and passive audio-motor training on spatial perception in the auditory and proprioceptive domains on 36 healthy young adults. First, to investigate the role of voluntary movements on spatial perception, we compared the effects of active vs. passive multimodal training on auditory and proprioceptive spatial localization. Second, to investigate the effectiveness of unimodal training conditions on spatial perception, we compared the impact of only proprioceptive or only auditory sensory feedback on spatial localization. Finally, to understand whether the positive effects of multimodal and unimodal trainings generalize to the untrained part, both dominant and non-dominant arms were tested. Results indicate that passive multimodal training (guided movement) is more beneficial than active multimodal training (active exploration) and only in passive condition the improvement is generalized also on the untrained hand. Moreover, we found that combined audio-motor training provides the strongest benefit because it significantly affects both auditory and somatosensory localization, while the effect of a single feedback modality is limited to a single domain, indicating a cross-modal influence of the two domains. Therefore, the use of multimodal feedback is more efficient in improving spatial perception. These results indicate that combined sensorimotor signals are effective in recalibrating auditory and proprioceptive spatial perception and that the beneficial effect is mainly due to the combination of auditory and proprioceptive spatial cues.

Consolidation of human somatosensory memory during motor learning.

Sensorimotor learning is a bidirectional process associated with concurrent neuroplastic changes in the motor and somatosensory system. While motor memory consolidation and retention have been extensively studied during skill acquisition, little is known about the formation and consolidation of somatosensory memory associated with motor learning. Using a robotic exoskeleton, we tracked markers of somatosensory and motor learning while healthy participants trained to make goal-directed wrist reaching movements over five days and evaluated retention for up to 10 days after practice. Markers of somatosensory learning were changes in wrist position sense bias (systematic error) and precision (random error). The main results are as follows: First, somatosensory (proprioceptive) memory consolidation shows signs of cost savings with repeated sensorimotor training - the same feature is known for motor memory formation. Moreover, somatosensory learning generalized to untrained workspace. Second, somatosensory learning over days can be characterized as an early improvement in sensory precision and a later improvement in sensory bias. Third, the time course of learning gains in position sense acuity coincided with improvements in spatial movement accuracy. Finally, the gains of somatosensory learning were retained for several days. Improvements in position sense bias were still visible up to 3 days after the end of practice for the trained workspace positions, but decayed faster in the untrained workspace. Improvements in position sense precision were retained for up to 10 days and were workspace independent. The findings are consistent with the view that an internal model of somatosensory joint space is formed during motor learning.

Biofeedback Signals for Robotic Rehabilitation: Assessment of Wrist Muscle Activation Patterns in Healthy Humans.

Electrophysiological recordings from human muscles can serve as control signals for robotic rehabilitation devices. Given that many diseases affecting the human sensorimotor system are associated with abnormal patterns of muscle activation, such biofeedback can optimize human-robot interaction and ultimately enhance motor recovery. To understand how mechanical constraints and forces imposed by a robot affect muscle synergies, we mapped the muscle activity of seven major arm muscles in healthy individuals performing goal-directed discrete wrist movements constrained by a wrist robot. We tested six movement directions and four force conditions typically experienced during robotic rehabilitation. We analyzed electromyographic (EMG) signals using a space-by-time decomposition and we identified a set of spatial and temporal modules that compactly described the EMG activity and were robust across subjects. For each trial, coefficients expressing the strength of each combination of modules and representing the underlying muscle recruitment, allowed for a highly reliable decoding of all experimental conditions. The decomposition provides compact representations of the observable muscle activation constrained by a robotic device. Results indicate that a low-dimensional control scheme incorporating EMG biofeedback could be an effective add-on for robotic rehabilitative protocols seeking to improve impaired motor function in humans.

Robot-Assisted Proprioceptive Training with Added Vibro-Tactile Feedback Enhances Somatosensory and Motor Performance.

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.