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      Haptic Error Modulation Outperforms Visual Error Amplification When Learning a Modified Gait Pattern

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          Abstract

          Robotic algorithms that augment movement errors have been proposed as promising training strategies to enhance motor learning and neurorehabilitation. However, most research effort has focused on rehabilitation of upper limbs, probably because large movement errors are especially dangerous during gait training, as they might result in stumbling and falling. Furthermore, systematic large movement errors might limit the participants’ motivation during training. In this study, we investigated the effect of training with novel error modulating strategies, which guarantee a safe training environment, on motivation and learning of a modified asymmetric gait pattern. Thirty healthy young participants walked in the exoskeletal robotic system Lokomat while performing a foot target-tracking task, which required an increased hip and knee flexion in the dominant leg. Learning the asymmetric gait pattern with three different strategies was evaluated: (i) No disturbance: no robot disturbance/guidance was applied, (ii) haptic error amplification: unsafe and discouraging large errors were limited with haptic guidance, while haptic error amplification enhanced awareness of small errors relevant for learning, and (iii) visual error amplification: visually observed errors were amplified in a virtual reality environment. We also evaluated whether increasing the movement variability during training by adding randomly varying haptic disturbances on top of the other training strategies further enhances learning. We analyzed participants’ motor performance and self-reported intrinsic motivation before, during and after training. We found that training with the novel haptic error amplification strategy did not hamper motor adaptation and enhanced transfer of the practiced asymmetric gait pattern to free walking. Training with visual error amplification, on the other hand, increased errors during training and hampered motor learning. Participants who trained with visual error amplification also reported a reduced perceived competence. Adding haptic disturbance increased the movement variability during training, but did not have a significant effect on motor adaptation, probably because training with haptic disturbance on top of visual and haptic error amplification decreased the participants’ feelings of competence. The proposed novel haptic error modulating controller that amplifies small task-relevant errors while limiting large errors outperformed visual error augmentation and might provide a promising framework to improve robotic gait training outcomes in neurological patients.

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          Most cited references 73

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          Review of control strategies for robotic movement training after neurologic injury

          There is increasing interest in using robotic devices to assist in movement training following neurologic injuries such as stroke and spinal cord injury. This paper reviews control strategies for robotic therapy devices. Several categories of strategies have been proposed, including, assistive, challenge-based, haptic simulation, and coaching. The greatest amount of work has been done on developing assistive strategies, and thus the majority of this review summarizes techniques for implementing assistive strategies, including impedance-, counterbalance-, and EMG- based controllers, as well as adaptive controllers that modify control parameters based on ongoing participant performance. Clinical evidence regarding the relative effectiveness of different types of robotic therapy controllers is limited, but there is initial evidence that some control strategies are more effective than others. It is also now apparent there may be mechanisms by which some robotic control approaches might actually decrease the recovery possible with comparable, non-robotic forms of training. In future research, there is a need for head-to-head comparison of control algorithms in randomized, controlled clinical trials, and for improved models of human motor recovery to provide a more rational framework for designing robotic therapy control strategies.
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            Motor learning elicited by voluntary drive.

            Motor training consisting of voluntary movements leads to performance improvements and results in characteristic reorganizational changes in the motor cortex. It has been proposed that repetition of passively elicited movements could also lead to improvements in motor performance. In this study, we compared behavioural gains, changes in functional MRI (fMRI) activation in the contralateral primary motor cortex (cM1) and in motor cortex excitability measured with transcranial magnetic stimulation (TMS) after a 30 min training period of either voluntarily (active) or passively (passive) induced wrist movements, when alertness and kinematic aspects of training were controlled. During active training, subjects were instructed to perform voluntary wrist flexion-extension movements of a specified duration (target window 174-186 ms) in an articulated splint. Passive training consisted of wrist flexion- extension movements elicited by a torque motor, of the same amplitude and duration range as in the active task. fMRI activation and TMS parameters of motor cortex excitability were measured before and after each training type. Motor performance, measured as the number of movements that hit the target window duration, was significantly better after active than after passive training. Both active and passive movements performed during fMRI measurements activated cM1. Active training led to more prominent increases in (i) fMRI activation of cM1; (ii) recruitment curves (TMS); and (iii) intracortical facilitation (TMS) than passive training. Therefore, a short period of active motor training is more effective than passive motor training in eliciting performance improvements and cortical reorganization. This result is consistent with the concept of a pivotal role for voluntary drive in motor learning and neurorehabilitation.
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              Temporal structure of motor variability is dynamically regulated and predicts motor learning ability.

              Individual differences in motor learning ability are widely acknowledged, yet little is known about the factors that underlie them. Here we explore whether movement-to-movement variability in motor output, a ubiquitous if often unwanted characteristic of motor performance, predicts motor learning ability. Surprisingly, we found that higher levels of task-relevant motor variability predicted faster learning both across individuals and across tasks in two different paradigms, one relying on reward-based learning to shape specific arm movement trajectories and the other relying on error-based learning to adapt movements in novel physical environments. We proceeded to show that training can reshape the temporal structure of motor variability, aligning it with the trained task to improve learning. These results provide experimental support for the importance of action exploration, a key idea from reinforcement learning theory, showing that motor variability facilitates motor learning in humans and that our nervous systems actively regulate it to improve learning.
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                Author and article information

                Contributors
                Journal
                Front Neurosci
                Front Neurosci
                Front. Neurosci.
                Frontiers in Neuroscience
                Frontiers Media S.A.
                1662-4548
                1662-453X
                19 February 2019
                2019
                : 13
                Affiliations
                1Gerontechnology and Rehabilitation Group, ARTORG Center for Biomedical Engineering Research, University of Bern , Bern, Switzerland
                2Sensory-Motor Systems (SMS) Lab, Institute of Robotics and Intelligent Systems (IRIS), Department of Health Sciences and Technology (D-HEST), ETH Zürich , Zurich, Switzerland
                3Reharobotics Group, Spinal Cord Injury Center, Balgrist University Hospital, Medical Faculty, University of Zurich , Zurich, Switzerland
                4Hocoma AG , Volketswil, Switzerland
                Author notes

                Edited by: Mauro Murgia, University of Trieste, Italy

                Reviewed by: Herbert Heuer, Leibniz Research Centre for Working Environment and Human Factors (IfADo), Germany; Reinoud J. Bootsma, Aix-Marseille Université, France

                This article was submitted to Perception Science, a section of the journal Frontiers in Neuroscience

                Article
                10.3389/fnins.2019.00061
                6390202
                Copyright © 2019 Marchal-Crespo, Tsangaridis, Obwegeser, Maggioni and Riener.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                Page count
                Figures: 9, Tables: 4, Equations: 8, References: 86, Pages: 24, Words: 0
                Funding
                Funded by: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung 10.13039/501100001711
                Award ID: PMPDP2_151319
                Categories
                Neuroscience
                Original Research

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