Functional electrical stimulation (FES) is capable of activating muscles that are under-recruited in neurological diseases, such as stroke. Therefore, FES provides a promising technology for assisting upper-limb motor functions in rehabilitation following stroke. However, the full benefits of FES may be limited due to lack of a systematic approach to formulate the pattern of stimulation. Our preliminary work demonstrated that it is feasible to use muscle synergy to guide the generation of FES patterns.In this paper, we present a methodology of formulating FES patterns based on muscle synergies of a normal subject using a programmable multi-channel FES device. The effectiveness of the synergy-based FES was tested in two sets of experiments. In experiment one, the instantaneous effects of FES to improve movement kinematics were tested in three patients post ischemic stroke. Patients performed frontal reaching and lateral reaching tasks, which involved coordinated movements in the elbow and shoulder joints. The FES pattern was adjusted in amplitude and time profile for each subject in each task. In experiment two, a 5-day session of intervention using synergy-based FES was delivered to another three patients, in which patients performed task-oriented training in the same reaching movements in one-hour-per-day dose. The outcome of the short-term intervention was measured by changes in Fugl–Meyer scores and movement kinematics. Results on instantaneous effects showed that FES assistance was effective to increase the peak hand velocity in both or one of the tasks. In short-term intervention, evaluations prior to and post intervention showed improvements in both Fugl–Meyer scores and movement kinematics. The muscle synergy of patients also tended to evolve towards that of the normal subject. These results provide promising evidence of benefits using synergy-based FES for upper-limb rehabilitation following stroke. This is the first step towards a clinical protocol of applying FES as therapeutic intervention in stroke rehabilitation.
Muscle activation during movement is commonly disrupted due to neural injuries from stroke. A major challenge for stroke rehabilitation is to re-establish the normal ways of muscle activation through a general restoration of motor control, otherwise impairments may be compensated by the motor system through a substitution strategy of task control . In post-stroke intervention, new technologies such as neuromuscular electrical stimulation (NMES) or functional electrical stimulation (FES) offer advantages for non-invasively targeting specific groups of muscles – to restore the pattern of muscle activation. Nevertheless, their effectiveness is limited by lack of a systematic methodology to optimize the stimulation pattern, to implement the optimal strategy in clinical settings, and to design a protocol of training towards the goal of restoring motor functions. This pioneer study addresses these issues in clinical application with a non-invasive FES technology.
Sign in to Continue Reading
M. F. Levin, J. A. Kleim, and S. L. Wolf, “What do motor ‘recovery’ and ‘compensation’ mean in patients following stroke?” Neurorehabilitation Neural Repair, vol. 23, no. 4, pp. 313–319, 2008.
G. Alon, A. F. Levitt, and P. A. McCarthy, “Functional electrical stimulation (FES) may modify the poor prognosis of stroke survivors with severe motor loss of the upper extremity: A preliminary study,” Amer. J. Phys. Med. Rehabil., vol. 87, no. 8, pp. 627–636, 2008.
W. Rong, “A neuromuscular electrical stimulation (NMES) and robot hybrid system for multi-joint coordinated upper limb rehabilitation after stroke,” J. Neuroeng. Rehabil., vol. 14, no. 1, p. 34, Dec. 2017.
J. J. Daly, “Recovery of coordinated gait: Randomized controlled stroke trial of functional electrical stimulation (FES) versus no FES, with weight-supported treadmill and over-ground training,” Neurorehabilitation Neural Repair, vol. 25, no. 7, pp. 588–596, Sep. 2011.
R. Nataraj, M. L. Audu, R. F. Kirsch, and R. J. Triolo, “Comprehensive joint feedback control for standing by functional neuromuscular stimulation—A simulation study,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 18, no. 6, pp. 646–657, Dec. 2010.
R. Nataraj, M. L. Audu, and R. J. Triolo, “Restoring standing capabilities with feedback control of functional neuromuscular stimulation following spinal cord injury,” Med. Eng. Phys., vol. 42, pp. 13–25, Apr. 2017.
H. Rouhani, M. Same, K. Masani, Y. Q. Li, and M. R. Popovic, “PID controller design for FES applied to ankle muscles in neuroprosthesis for standing balance,” Frontiers Neurosci., vol. 11, p. 347, Jun. 2017.
V. K. Mushahwar, P. L. Jacobs, R. A. Normann, R. J. Triolo, and N. Kleitman, “New functional electrical stimulation approaches to standing and walking,” J. Neural Eng., vol. 4, no. 3, pp. S181–S197, Sep. 2007.
B. J. Holinski, “Intraspinal microstimulation produces over-ground walking in anesthetized cats,” J. Neural Eng., vol. 13, no. 5, p. 056016, Oct. 2016.
M. B. Popovic, D. B. Popovic, T. Sinkjær, A. Stefanovic, and L. Schwirtlich, “Restitution of reaching and grasping promoted by functional electrical therapy,” Artif. Organs, vol. 26, no. 3, pp. 271–275, Mar. 2002.
A. B. Ajiboye, “Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: A proof-of-concept demonstration,” Lancet Lond. Engl., vol. 389, no. 10081, pp. 1821–1830, May 2017.
J. H. Grill and P. H. Peckham, “Functional neuromuscular stimulation for combined control of elbow extension and hand grasp in C5 and C6 quadriplegics,” IEEE Trans. Rehabil. Eng., vol. 6, no. 2, pp. 190–199, Jun. 1998.
M. R. Popovic, T. A. Thrasher, M. E. Adams, V. Takes, V. Zivanovic, and M. I. Tonack, “Functional electrical therapy: Retraining grasping in spinal cord injury,” Spinal Cord, vol. 44, no. 3, pp. 143–151, Mar. 2006.
C. Ethier, E. R. Oby, M. J. Bauman, and L. E. Miller, “Restoration of grasp following paralysis through brain-controlled stimulation of muscles,” Nature, vol. 485, no. 7398, pp. 368–371, May 2012.
G. Alon, “Use of neuromuscular electrical stimulation in neureorehabilitation: A challenge to all,” J. Rehabil. Res. Develop., vol. 40, no. 6, pp. 9–12, Dec. 2003.
G. Alon, A. F. Levitt, and P. A. McCarthy, “Functional electrical stimulation enhancement of upper extremity functional recovery during stroke rehabilitation: A pilot study,” Neurorehabilitation Neural Repair, vol. 21, no. 3, pp. 207–215, Jun. 2007.
C. Church, C. Price, A. D. Pandyan, S. Huntley, R. Curless, and H. Rodgers, “Randomized controlled trial to evaluate the effect of surface neuromuscular electrical stimulation to the shoulder after acute stroke,” Stroke, vol. 37, no. 12, pp. 2995–3001, Dec. 2006.
J. H. Cauraugh and S. B. Kim, “Chronic stroke motor recovery: Duration of active neuromuscular stimulation,” J. Neurolog. Sci., vol. 215, nos. 1–2, pp. 13–19, Nov. 2003.
S. Ferrante, T. Schauer, G. Ferrigno, J. Raisch, and F. Molteni, “The effect of using variable frequency trains during functional electrical stimulation cycling,” Neuromodulation, Technol. Neural Interface, vol. 11, no. 3, pp. 216–226, Jul. 2008.
R. W. Fields, “Electromyographically triggered electric muscle stimulation for chronic hemiplegia,” Arch. Phys. Med. Rehabil., vol. 68, no. 7, pp. 407–414, Jul. 1987.
G. H. Kraft, S. S. Fitts, and M. C. Hammond, “Techniques to improve function of the arm and hand in chronic hemiplegia,” Arch. Phys. Med. Rehabil., vol. 73, no. 3, pp. 220–227, Mar. 1992.
G. van Overeem Hansen, “EMG-controlled functional electrical stimulation of the paretic hand,” Scand. J. Rehabil. Med., vol. 11, no. 4, pp. 189–193, 1979.
J. H. Cauraugh, S. B. Kim, and A. Duley, “Coupled bilateral movements and active neuromuscular stimulation: Intralimb transfer evidence during bimanual aiming,” Neurosci. Lett., vol. 382, nos. 1–2, pp. 39–44, Jul. 2005.
J. S. Knutson, D. D. Gunzler, R. D. Wilson, and J. Chae, “Contralaterally controlled functional electrical stimulation improves hand dexterity in chronic hemiparesis: A randomized trial,” Stroke, vol. 47, no. 10, pp. 2596–2602, Oct. 2016.
D. A. E. Bolton, J. H. Cauraugh, and H. A. Hausenblas, “Electromyogram-triggered neuromuscular stimulation and stroke motor recovery of arm/hand functions: A meta-analysis,” J. Neurol. Sci., vol. 223, no. 2, pp. 121–127, Aug. 2004.
M. K.-L. Chan, R. K.-Y. Tong, and K. Y.-W. Chung, “Bilateral upper limb training with functional electric stimulation in patients with chronic stroke,” Neurorehabilitation Neural Repair, vol. 23, no. 4, pp. 357–365, May 2009.
J. B. Manigandan, G. S. Ganesh, M. Pattnaik, and P. Mohanty, “Effect of electrical stimulation to long head of biceps in reducing gleno humeral subluxation after stroke,” Neuro Rehabil., vol. 34, no. 2, pp. 245–252, 2014.
S. Li, C. Zhuang, C. M. Niu, Y. Bao, Q. Xie, and N. Lan, “Evaluation of functional correlation of task-specific muscle synergies with motor performance in patients poststroke,” Frontiers Neurol., vol. 8, p. 337, Jul. 2017.
A. d’Avella, P. Saltiel, and E. Bizzi, “Combinations of muscle synergies in the construction of a natural motor behavior,” Nature Neurosci., vol. 6, no. 3, pp. 300–308, Mar. 2003.
V. C. K. Cheung, “Muscle synergy patterns as physiological markers of motor cortical damage,” Proc. Nat. Acad. Sci. USA, vol. 109, no. 36, pp. 14652–14656, Sep. 2012.
D. J. Clark, L. H. Ting, F. E. Zajac, R. R. Neptune, and S. A. Kautz, “Merging of healthy motor modules predicts reduced locomotor performance and muscle coordination complexity post-stroke,” J. Neurophysiol., vol. 103, no. 2, pp. 844–857, Feb. 2010.
E. Ambrosini, “Neuro-mechanics of recumbent leg cycling in post-acute stroke patients,” Ann. Biomed. Eng., vol. 44, pp. 3238–3251, Jun. 2016.
C. Zhuang, J. C. Marquez, H. E. Qu, X. He, and N. Lan, “A neuromuscular electrical stimulation strategy based on muscle synergy for stroke rehabilitation,” in Proc. IEEE 7th Int./EMBS Conf. Neural Eng. (NER), vol. 15, Apr. 2015, pp. 816–819.
R. S. Razavian, B. Ghannadi, N. Mehrabi, M. Charlet, and J. McPhee, “Feedback control of functional electrical stimulation for 2-D arm reaching movements,” IEEE Trans. Neural Syst. Rehabil. Eng., vol. 26, no. 10, pp. 2033–2043, Oct. 2018.
C. M. Niu, C. Zhuang, Y. Bao, S. Li, N. Lan, and Q. Xie, “Synergy-based NMES intervention accelerated rehabilitation of post-stroke hemiparesis,” in Proc. Assoc. Acad. Physiatrists Annu. Conf., Las Vegas, NV, USA, 2017.
H. Qu, “Development of network-based multichannel neuromuscular electrical stimulation system for stroke rehabilitation,” J. Rehabil. Res. Develop., vol. 52, no. 3, pp. 263–278, 2016.
C. M. Niu, “Effectiveness of short-term training with a synergy-based FES paradigm on motor function recovery post stroke,” in Proc. 12th Int. Soc. Phys. Rehabil. Med. World Congr., Paris, France, 2018.
T. Wang, “Customization of synergy-based FES for post-stroke rehabilitation of upper-limb motor functions,” in Proc. IEEE 40th Annu. Int. Conf. Eng. Med. Biol. Soc. (EMBS), Jul. 2018, 3541–3544.
L. L. Baker, D. R. McNeal, L. A. Benton, B. R. Bowman, and R. L. Waters, Ed., Neuromuscular Electrical Stimulation a Practical Guide, 4th ed. Downey, CA, USA: Los Amigos Research & Education Institute, 2000.
A. d’Avella, A. Portone, L. Fernandez, and F. Lacquaniti, “Control of fast-reaching movements by muscle synergy combinations.,” J. Neurosci., vol. 26, no. 30, pp. 7791–7810, Jul. 2006.
R. D. Wilson, “Upper-limb recovery after stroke: A randomized controlled trial comparing EMG-triggered, cyclic, and sensory electrical stimulation,” Neurorehabilitation Neural Repair, vol. 30, no. 10, pp. 978–987, Nov. 2016.
A. J. Levine, “Identification of a cellular node for motor control pathways,” Nature Neurosci., vol. 17, no. 4, pp. 586–593, Apr. 2014.
S. B. Frost, S. Barbay, K. M. Friel, E. J. Plautz, and R. J. Nudo, “Reorganization of remote cortical regions after ischemic brain injury: A potential substrate for stroke recovery,” J. Neurophysiol., vol. 89, no. 6, pp. 3205–3214, Jun. 2003.
P. Langhorne, J. Bernhardt, and G. Kwakkel, “Stroke rehabilitation,” Lancet, vol. 377, no. 9778, pp. 1693–1702, May 2011.
M. D. Ellis, B. G. Holubar, A. M. Acosta, R. F. Beer, and J. P. A. Dewald, “Modifiability of abnormal isometric elbow and shoulder joint torque coupling after stroke,” Muscle Nerve, vol. 32, pp. 170–178, Aug. 2005.
J. P. A. Dewald, P. S. Pope, J. D. Given, T. S. Buchanan, and W. Z. Rymer, “Abnormal muscle coactivation patterns during isometric torque generation at the elbow and shoulder in hemiparetic subjects,” Brain, vol. 118, no. 2, pp. 495–510, 1995.
D. G. Kamper, A. N. McKenna-Cole, L. E. Kahn, and D. J. Reinkensmeyer, “Alterations in reaching after stroke and their relation to movement direction and impairment severity,” Arch. Phys. Med. Rehabil., vol. 83, no. 5, pp. 702–707, May 2002.
C. L. Massie, S. Fritz, and M. P. Malcolm, “Elbow extension predicts motor impairment and performance after stroke,” Rehabil. Res. Pract., vol. 2011, pp. 1–7, 2011.
V. C. K. Cheung, L. Piron, M. Agostini, S. Silvoni, A. Turolla, and E. Bizzi, “Stability of muscle synergies for voluntary actions after cortical stroke in humans,” Proc. Nat. Acad. Sci. USA, vol. 106, no. 46, pp. 19563–19568, Nov. 2009.
J. Roh, W. Z. Rymer, and R. F. Beer, “Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans,” J. Neurophysiol., vol. 107, no. 8, pp. 2123–2142, Apr. 2012.
J. Roh, W. Z. Rymer, and R. F. Beer, “Evidence for altered upper extremity muscle synergies in chronic stroke survivors with mild and moderate impairment,” Frontiers Hum. Neurosci., vol. 9, p. 6, Feb. 2015.
J. Roh, W. Z. Rymer, E. J. Perreault, S. B. Yoo, and R. F. Beer, “Alterations in upper limb muscle synergy structure in chronic stroke survivors,” J. Neurophysiol., vol. 109, no. 3, pp. 768–781, Feb. 2013.
W. H. Backes, W. H. Mess, V. van Kranen-Mastenbroek, and J. P. H. Reulen, “Somatosensory cortex responses to median nerve stimulation: fMRI effects of current amplitude and selective attention,” Clin. Neurophysiol., vol. 111, no. 10, pp. 1738–1744, Oct. 2000.
G. Francisco, “Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute stroke survivors: A randomized pilot study,” Arch. Phys. Med. Rehabil., vol. 79, no. 5, pp. 570–575, May 1998.
S. K. Sabut, C. Sikdar, R. Kumar, and M. Mahadevappa, “Functional electrical stimulation of dorsiflexor muscle: Effects on dorsiflexor strength, plantarflexor spasticity, and motor recovery in stroke patients,” Neurorehabilitation, vol. 29, no. 4, pp. 393–400, 2011.
Y.-H. Wang, F. Meng, Y. Zhang, M.-Y. Xu, and S.-W. Yue, “Full-movement neuromuscular electrical stimulation improves plantar flexor spasticity and ankle active dorsiflexion in stroke patients: A randomized controlled study,” Clin. Rehabil., vol. 30, no. 6, pp. 577–586, Jun. 2016.
W. H. Chang and Y.-H. Kim, “Robot-assisted therapy in stroke rehabilitation,” J. Stroke, vol. 15, no. 3, p. 174, 2013.
H. G. Wu, Y. R. Miyamoto, L. N. G. Castro, B. P. Ölveczky, and M. A. Smith, “Temporal structure of motor variability is dynamically regulated and predicts motor learning ability,” Nature Neurosci., vol. 17, no. 2, pp. 312–321, Jan. 2014.
J. Frère and F. Hug, “Between-subject variability of muscle synergies during a complex motor skill,” Frontiers Comput. Neurosci., vol. 6, p. 99, Dec. 2012.
S. Muceli, A. T. Boye, A. d’Avella, and D. Farina, “Identifying representative synergy matrices for describing muscular activation patterns during multidirectional reaching in the horizontal plane,” J. Neurophysiol., vol. 103, no. 3, pp. 1532–1542, Mar. 2010.
J. F. Soechting and F. Lacquaniti, “Invariant characteristics of a pointing movement in man,” J. Neurosci., vol. 1, no. 7, pp. 710–720, Jul. 1981.
B. Cesqui, A. d’Avella, A. Portone, and F. Lacquaniti, “Catching a ball at the right time and place: Individual factors matter,” PLoS ONE, vol. 7, no. 2, p. e31770, Feb. 2012.
via Synergy-Based FES for Post-Stroke Rehabilitation of Upper-Limb Motor Functions – IEEE Journals & Magazine
It is evident that the dominant therapy of functional electrical stimulation (FES) for stroke rehabilitation suffers from heavy dependency on therapists experience and lack of feedback from patients status, which decrease the patients’ voluntary participation, reducing the rehabilitation efficacy. This paper proposes a closed loop FES system using surface electromyography (sEMG) bias feedback from bilateral arms for enhancing upper-limb stroke rehabilitation. This wireless portable system consists of sEMG data acquisition and FES modules, the former is used to measure and analyze the subject’s bilateral arm motion intention and neuromuscular states in terms of their sEMG, the latter of multi-channel FES output is controlled via the sEMG bias of the bilateral arms. The system has been evaluated with experiments proving that the system can achieve 39.9 dB signal-to-noise ratio (SNR) in the lab environment, outperforming existing similar systems. The results also show that voluntary and active participation can be effectively employed to achieve different FES intensity for FES-assisted hand motions, demonstrating the potential for active stroke rehabilitation.
via sEMG Bias-driven Functional Electrical Stimulation System for Upper-Limb Stroke Rehabilitation – IEEE Journals & Magazine
Reaching and grasping are two of the most affected functions after stroke. Hybrid rehabilitation systems combining Functional Electrical Stimulation with Robotic devices have been proposed in the literature to improve rehabilitation outcomes. In this work, we present the combined use of a hybrid robotic system with an EEG-based Brain-Machine Interface to detect the user’s movement intentions to trigger the assistance. The platform has been tested in a single session with a stroke patient. The results show how the patient could successfully interact with the BMI and command the assistance of the hybrid system with low latencies. Also, the Feedback Error Learning controller implemented in this system could adjust the required FES intensity to perform the task.
Stroke is a leading cause of adult disability around the world. A large number of stroke survivors are left with a unilateral arm or leg paralysis. After completing conventional rehabilitation therapy, a significant number of stroke survivors are left with limited reaching and grasping capabilities .
Source: Combining a hybrid robotic system with a bain-machine interface for the rehabilitation of reaching movements: A case study with a stroke patient – IEEE Xplore Document
The torque generation capability of muscles often reduces during a functional electrical stimulation (FES) session due to the rapid onset of muscle fatigue. Hybrid rehabilitation systems that use FES and electric motor assist may overcome this issue.
The primary control challenge in such a system is how to allocate control inputs between electric motor and FES during muscle fatigue and muscle recovery. One strategy is to switch between FES and the electric motor by using an estimate of the muscle fatigue. This would allow the system to switch from using FES to using the electric motor when the muscle torque output has significantly decreased, then switch back to FES once the muscles have sufficiently recovered.
This paper uses a second order sliding mode controller cascaded with a feedback linearization controller for a switched, FES and electric motor, system. The second order sliding mode is achieved through the use of a variable-gain super-twisting algorithm. A Lyapunov stability analysis was used to prove asymptotic stability of the switched control system. Simulations of the developed controller on a hybrid knee extension model illustrate that prolonged knee movements can be elicited through the switched system.
Source: IEEE Xplore Abstract (Abstract) – Switching control of functional electrical stimulation and motor assist for muscle fatigue compensat…