EMG patterns during assisted walking in the exoskeleton

Frontiers in Human Neuroscience

Volumn 8, Issue JUNE, 2014, Pages

  Sylos Labini, Francesca ^a,b   La Scaleia, Valentina ^a,b   d'Avella, Andrea ^a   Pisotta, Iolanda ^a   Tamburella, Federica ^a   Scivoletto, Giorgio ^a   Molinari, Marco ^a   Wang, Shiqian ^c   Wang, Letian ^d   van Asseldonk, Edwin ^d   van der Kooij, Herman ^c,d   Hoellinger, Thomas ^e   Cheron, Guy ^e   Thorsteinsson, Freygardur ^f   Ilzkovitz, Michel ^g   Gancet, Jeremi ^g   Hauffe, Ralf ^h   Zanov, Frank ^h   Lacquaniti, Francesco ^a,b   Ivanenko, Yuri P ^a  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c Delft University of Technology   (Netherlands)

^d UNIVERSITY OF TWENTE   (Netherlands)

^e UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^f Research and Development   (Iceland)

^g ESEC Galaxia   (Belgium)

^h ANT Neuro   (Germany)

Author keywords

Assisted gait; EMG patterns; Neuroprosthetic technology; Robotic exoskeleton; Spinal cord injury

Indexed keywords

ADULT; ARM MUSCLE; ARTICLE; ASSISTED WALKING; CASE REPORT; CONTROLLED STUDY; DELTOID MUSCLE; ELECTROMYOGRAM; EXTENSOR CARPI ULNARIS; FEMALE; GAIT; GAIT ORTHOSIS; GAIT SPEED; GASTROCNEMIUS MUSCLE; HAMSTRING; HUMAN; KINEMATICS; LOCOMOTION; MALE; MAN MACHINE INTERACTION; MUSCLE CONTRACTION; RECTUS FEMORIS MUSCLE; ROBOTIC EXOSKELETON; SELF SELECTED WALKING; SEMITENDINOUS MUSCLE; SLOW WALKING; SOLEUS MUSCLE; SPINAL CORD INJURY; SWING PHASE; TIBIALIS ANTERIOR MUSCLE; UNASSISTED WALKING; VASTUS MEDIALIS MUSCLE; WALKING; WAVEFORM; YOUNG ADULT;

EID: 84902590669     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00423     Document Type: Article

References (52)

1. Aoyagi, D., Ichinose, W. E., Harkema, S. J., Reinkensmeyer, D. J., and Bobrow, J. E. (2007). A robot and control algorithm that can synchronously assist in naturalistic motion during body-weight-supported gait training following neurologic injury. IEEE Trans. Neural Syst. Rehabil. Eng. 15, 387-400. doi: 10.1109/TNSRE.2007.903922
2. Batschelet, E. (1981). Circular Statistics in Biology. New York, NY: Academic Press.
3. Berens, P. (2009). CircStat: a MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1-21.
4. Beres-Jones, J. A., and Harkema, S. J. (2004). The human spinal cord interprets velocity-dependent afferent input during stepping. Brain 127, 2232-2246. doi: 10.1093/brain/awh252
5. Cai, L. L., Courtine, G., Fong, A. J., Burdick, J. W., Roy, R. R., and Edgerton, V. R. (2006). Plasticity of functional connectivity in the adult spinal cord. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1635-1646. doi: 10.1098/rstb. 2006.1884
6. Cappellini, G., Ivanenko, Y. P., Dominici, N., Poppele, R. E., and Lacquaniti, F. (2010). Motor patterns during walking on a slippery walkway. J. Neurophysiol. 103, 746-760. doi: 10.1152/jn.00499.2009
7. Cheron, G., Bengoetxea, A., Pozzo, T., Bourgeois, M., and Draye, J. P. (1997). Evidence of a preprogrammed deactivation of the hamstring muscles for triggering rapid changes of posture in humans. Electroencephalogr. Clin. Neurophysiol. 105, 58-71. doi: 10.1016/S0924-980X(96)96544-3
8. Cheron, G., Duvinage, M., De Saedeleer, C., Castermans, T., Bengoetxea, A., Petieau, M., et al. (2012). From spinal central pattern generators to cortical network: integrated BCI for walking rehabilitation. Neural Plast. 2012:375148. doi: 10.1155/2012/375148
9. Courtine, G., Papaxanthis, C., and Schieppati, M. (2006). Coordinated modulation of locomotor muscle synergies constructs straight-ahead and curvilinear walking in humans. Exp. Brain Res. 170, 320-335. doi: 10.1007/s00221-005-0215-7
10. del-Ama, A. J., Moreno, J. C., Gil-Agudo, A., de-los-Reyes, A., and Pons, J. L. (2012). Online assessment of human-robot interaction for hybrid control of walking. Sensors 12, 215-225. doi: 10.3390/s120100215
11. Dietz, V., Grillner, S., Trepp, A., Hubli, M., and Bolliger, M. (2009). Changes in spinal reflex and locomotor activity after a complete spinal cord injury: a common mechanism? Brain 132, 2196-2205. doi: 10.1093/brain/awp124
12. Duysens, J., De Groote, F., and Jonkers, I. (2013). The flexion synergy, mother of all synergies and father of new models of gait. Front. Comput. Neurosci. 7:14. doi: 10.3389/fncom.2013.00014
13. Duysens, J., van Wezel, B. M., van de Crommert, H. W., Faist, M., and Kooloos, J. G. (1998). The role of afferent feedback in the control of hamstrings activity during human gait. Eur. J. Morphol. 36, 293-299. doi: 10.1076/ejom.36.4.0293
14. Fitzsimmons, N. A., Lebedev, M. A., Peikon, I. D., and Nicolelis, M. A. L. (2009). Extracting kinematic parameters for monkey bipedal walking from cortical neuronal ensemble activity. Front. Integr. Neurosci. 3:3. doi: 10.3389/neuro.07.003.2009
15. Goldberg, E. J., and Neptune, R. R. (2007). Compensatory strategies during normal walking in response to muscle weakness and increased hip joint stiffness. Gait Posture 25, 360-367. doi: 10.1016/j.gaitpost.2006.04.009
16. Gordon, K. E., Kinnaird, C. R., and Ferris, D. P. (2013). Locomotor adaptation to a soleus EMG-controlled antagonistic exoskeleton. J. Neurophysiol. 109, 1804-1814. doi: 10.1152/jn.01128.2011
17. Grasso, R., Bianchi, L., and Lacquaniti, F. (1998). Motor patterns for human gait: backward versus forward locomotion. J. Neurophysiol. 80, 1868-1885.
18. Grasso, R., Ivanenko, Y. P., Zago, M., Molinari, M., Scivoletto, G., Castellano, V., et al. (2004). Distributed plasticity of locomotor pattern generators in spinal cord injured patients. Brain 127, 1019-1034. doi: 10.1093/ brain/awh115
19. Guertin, P. A. (2014). Preclinical evidence supporting the clinical development of central pattern generator-modulating therapies for chronic spinal cord-injured patients. Front. Hum. Neurosci. 8:272. doi: 10.3389/fnhum.2014.00272
20. Hidler, J. M., and Wall, A. E. (2005). Alterations in muscle activation patterns during robotic-assisted walking. Clin. Biomech. 20, 184-193. doi: 10.1016/j.clinbiomech.2004.09.016
21. Hsu, J. D., Michael, J., and Fisk, J. (2008). AAOS Atlas of Orthoses and Assistive Devices. Philadelphia, PA: MOSBY Elsevier.
22. Huang, S., and Ferris, D. P. (2012). Muscle activation patterns during walking from transtibial amputees recorded within the residual limb-prosthetic interface. J. Neuroeng. Rehabil. 9:55. doi: 10.1186/1743-0003-9-55
23. Israel, J. F., Campbell, D. D., Kahn, J. H., and Hornby, T. G. (2006). Metabolic costs and muscle activity patterns during robotic-and therapist-assisted tread-mill walking in individuals with incomplete spinal cord injury. Phys. Ther. 86, 1466-1478. doi: 10.2522/ptj.20050266
24. Ivanenko, Y. P., Cappellini, G., Solopova, I. A., Grishin, A. A., Maclellan, M. J., Poppele, R. E., et al. (2013). Plasticity and modular control of locomotor patterns in neurological disorders with motor deficits. Front. Comput. Neurosci. 7:123. doi: 10.3389/fncom.2013.00123
25. Ivanenko, Y. P., Dominici, N., Daprati, E., Nico, D., Cappellini, G., and Lacquaniti, F. (2011). Locomotor body scheme. Hum. Mov. Sci. 30, 341-351. doi: 10.1016/j.humov.2010.04.001
26. Ivanenko, Y. P., Grasso, R., and Lacquaniti, F. (2000). Influence of leg muscle vibration on human walking. J. Neurophysiol. 84, 1737-1747.
27. Ivanenko, Y. P., Grasso, R., Macellari, V., and Lacquaniti, F. (2002). Control of foot trajectory in human locomotion: role of ground contact forces in simulated reduced gravity. J. Neurophysiol. 87, 3070-3089.
28. Ivanenko, Y. P., Poppele, R. E., and Lacquaniti, F. (2006). Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different Speeds. J. Neurophysiol. 95, 602-618. doi: 10.1152/jn.00767.2005
29. Jasiewicz, J. M., Allum, J. H. J., Middleton, J. W., Barriskill, A., Condie, P., Purcell, B., et al. (2006). Gait event detection using linear accelerometers or angular velocity transducers in able-bodied and spinal-cord injured individuals. Gait Posture 24, 502-509. doi: 10.1016/j.gaitpost.2005.12.017
30. Kendall, F. P., McCreary, E. K., Provance, P. G., Rodgers, M. M., and Romani, W. A. (2005). Muscles: Testing and Function, with Posture and Pain. 5th Edn. Baltimore, MD: Lippincott Williams & Wilkins.
31. Lam, T., Wirz, M., Lünenburger, L., and Dietz, V. (2008). Swing phase resistance enhances flexor muscle activity during treadmill locomotion in incomplete spinal cord injury. Neurorehabil. Neural Repair 22, 438-446. doi: 10.1177/1545968308315595
32. Lünenburger, L., Colombo, G., and Riener, R. (2007). Biofeedback for robotic gait rehabilitation. J. Neuroeng. Rehabil. 4:1. doi: 10.1186/1743-0003-4-1
33. Maegele, M., Müller, S., Wernig, A., Edgerton, V. R., and Harkema, S. J. (2002). Recruitment of spinal motor pools during voluntary movements versus stepping after human spinal cord injury. J. Neurotrauma 19, 1217-1229. doi: 10.1089/08977150260338010
34. Malcolm, P., Derave, W., Galle, S., and De Clercq, D. (2013). A simple exoskeleton that assists plantarflexion can reduce the metabolic cost of human walking. PLoS ONE 8:e56137. doi: 10.1371/journal.pone.0056137
35. McGowan, C. P., Neptune, R. R., Clark, D. J., and Kautz, S. A. (2010). Modular control of human walking: adaptations to altered mechanical demands. J. Biomech. 43, 412-419. doi: 10.1016/j.jbiomech.2009.10.009
36. Molinari, M. (2009). Plasticity properties of CPG circuits in humans: impact on gait recovery. Brain Res. Bull. 78, 22-25. doi: 10.1016/j.brainresbull.2008.02.030
37. Moreno, J. C., Barroso, F., Farina, D., Gizzi, L., Santos, C., Molinari, M., et al. (2013). Effects of robotic guidance on the coordination of locomotion. J. Neuroeng. Rehabil. 10:79. doi: 10.1186/1743-0003-10-79
38. Nielsen, J. B., and Sinkjaer, T. (2002). Afferent feedback in the control of human gait. J. Electromyogr. Kinesiol. 12, 213-217. doi: 10.1016/S1050-6411(02)00023-8
39. Noble, J. W., and Prentice, S. D. (2006). Adaptation to unilateral change in lower limb mechanical properties during human walking. Exp. Brain Res. 169, 482-495. doi: 10.1007/s00221-005-0162-3
40. Perry, J. (1992). Gait Analysis: Normal and Pathological Function. Thorofare, NJ: SLACK Incorporated.
41. Roy, R. R., Harkema, S. J., and Edgerton, V. R. (2012). Basic concepts of activity-based interventions for improved recovery of motor function after spinal cord injury. Arch. Phys. Med. Rehabil. 93, 1487-1497. doi: 10.1016/j.apmr.2012.04.034
42. Sale, P., Franceschini, M., Waldner, A., and Hesse, S. (2012). Use of the robot assisted gait therapy in rehabilitation of patients with stroke and spinal cord injury. Eur. J. Phys. Rehabil. Med. 48, 111-121.
43. Scivoletto, G., Ivanenko, Y., Morganti, B., Grasso, R., Zago, M., Lacquaniti, F., et al. (2007). Plasticity of spinal centers in spinal cord injury patients: new concepts for gait evaluation and training. Neurorehabil. Neural Repair 21, 358-365. doi: 10.1177/1545968306295561
44. Swinnen, E., Duerinck, S., Baeyens, J.-P., Meeusen, R., and Kerckhofs, E. (2010). Effectiveness of robot-assisted gait training in persons with spinal cord injury: a systematic review. J. Rehabil. Med. 42, 520-526. doi: 10.2340/16501977-0538
45. Sylos-Labini, F., Ivanenko, Y. P., Cappellini, G., Gravano, S., and Lacquaniti, F. (2011). Smooth changes in the EMG patterns during gait transitions under body weight unloading. J. Neurophysiol. 106, 1525-1536. doi: 10.1152/jn.00160.2011
46. Sylos-Labini, F., Ivanenko, Y. P., Maclellan, M. J., Cappellini, G., Poppele, R. E., and Lacquaniti, F. (2014). Locomotor-like leg movements evoked by rhythmic arm movements in humans. PLoS ONE 9:e90775. doi: 10.1371/journal.pone.0090775
47. Thompson, A. K., and Wolpaw, J. R. (2014). Operant conditioning of spinal reflexes: from basic science to clinical therapy. Front. Integr. Neurosci. 8:25. doi: 10.3389/fnint.2014.00025
48. Van Asseldonk, E. H. F., Veneman, J. F., Ekkelenkamp, R., Buurke, J. H., Van der Helm, F. C. T., and van der Kooij, H. (2008). The effects on kinematics and muscle activity of walking in a robotic gait trainer during zero-force control. IEEE Trans. Neural Syst. Rehabil. Eng. 16, 360-370. doi: 10.1109/TNSRE.2008.925074
49. Wang, L., Wang, S., van Asseldonk, E. H. F., and van der Kooij, H. (2013). "Actively controlled lateral gait assistance in a lower limb exoskeleton," in 2013 IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS) (Tokyo), 965-970.
50. Winter, D. A. (1989). Biomechanics of normal and pathological gait: implications for understanding human locomotor control. J. Mot. Behav. 21, 337-355. doi: 10.1080/00222895.1989.10735488
51. Winter, D. A. (1991). The Biomechanics and Motor Control of Human Gait: Normal, Elderly and Pathological. Waterloo, ON: University of Waterloo Press.
52. Yakovenko, S., Mushahwar, V., VanderHorst, V., Holstege, G., and Prochazka, A. (2002). Spatiotemporal activation of lumbosacral motoneurons in the locomotor step cycle. J. Neurophysiol. 87, 1542-1553.