Prediction of Muscle Activity from Cortical Signals to Restore Hand Grasp in Subjects with Spinal Cord Injury

Statistical Signal Processing for Neuroscience and Neurotechnology

Volumn , Issue , 2010, Pages 369-406

  Oby, Emily R ^a   Ethier, Christian ^a   Bauman, Matthew J ^a   Perreault, Eric J ^a   Ko, Jason H ^a   Miller, Lee E ^b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Biomedical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84882896583     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-0-12-375027-3.00011-9     Document Type: Chapter

References (88)

1. Alon G., McBride K. Persons with C5 or C6 tetraplegia achieve selected functional gains using a neuroprosthesis. Arch. Phys. Med. Rehabil. 2003, 84:119-124.
2. Anderson K.D. Targeting recovery: priorities of the spinal cord-injured population. J. Neurotrauma 2004, 21:1371-1383.
3. Batista A.P., Buneo C.A., Snyder L.H., Andersen R.A. Reach plans in eye-centered coordinates. Science 1999, 285:257-260.
4. Berniker M., Jarc A., Bizzi E., Tresch M.C. Simplified and effective motor control based on muscle synergies to exploit musculoskeletal dynamics. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:7601-7606.
5. Branner A., Stein R.B., Fernandez E., Aoyagi Y., Normann R.A. Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve. IEEE Trans. Biomed. Eng. 2004, 51:146-157.
6. Bussgang J.J., Ehrman L., Graham J.W. Analysis of nonlinear systems with multiple inputs. Proc. IEEE 1974, 62:1088-1119.
7. Carmena J.M., Lebedev M.A., Crist R.E., O'Doherty J.E., Santucci D.M., Dimitrov D., et al. Learning to control a brain-machine interface for reaching and grasping by primates. PLoS Biol. 2003, 1:193-208.
8. Cheney P.D., Fetz E.E. Functional classes of primate corticomotorneuronal cells and their relation to active force. J. Neurophysiol. 1980, 44:773-791.
9. Creasey G., Elefteriades J., DiMarco A., Talonen P., Bijak M., Girsch W., et al. Electrical stimulation to restore respiration. J. Rehabil. Res. Dev. 1996, 33:123-132.
10. Danziger Z., Fishbach A., Mussa-Ivaldi F.A. Adapting human-machine interfaces to user performance. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2008, 1:4486-4490.
11. d'Avella A., Saltiel P., Bizzi E. Combinations of muscle synergies in the construction of a natural motor behavior. Nat. Neurosci. 2003, 6:300-308.
12. Enoka R.M., Stuart D.G. Neurobiology of muscle fatigue. J. Appl. Physiol. 1992, 72:1631-1648.
13. Evarts E.V. Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 1968, 31:14-27.
14. Fagg A.H., Ojakangas G.W., Miller L.E., Hatsopoulos N.G. Kinetic trajectory decoding using motor cortical ensembles. IEEE Trans. Neural Syst. Rehabil. Eng. 2009, 17:487-496.
15. Fetz E.E., Cheney P.D. Postspike facilitation of forelimb muscle activity by primate corticomotoneuronal cells. J. Neurophysiol. 1980, 44:751-772.
16. Fetz E.E., Finocchio D.V. Correlations between activity of motor cortex cells and arm muscles during operantly conditioned response patterns. Exp. Brain Res. 1975, 23:217-240.
17. Fromm C., Evarts E.E. Relation of size and activity of motor cortex pyramidal tract neurons during skilled movements in the monkey. J. Neurosci. 1981, 1:453-460.
18. Galvani L. De viribus electricitatis in motu musculari commentarius. Bon. Sci. Art. Inst. Acad. Comm. 1791, 7:363-418.
19. Ganguly K., Carmena J.M. Emergence of a stable cortical map for neuroprosthetic control. PLoS Biol. 2009, 7:e1000153.
20. Gao Y., Black M.J., Bienenstock E., Wu W., Donoghue J.P. A quantitative comparison of linear and non-linear models of motor cortical activity for the encoding and decoding of arm motions. 1st International IEEE/EMBS Conference on Neural Engineering 2003, vol. 1:189-192. Capri, Italy.
21. Georgopoulos A.P., Ashe J., Smyrnis N., Taira M. The motor cortex and the coding of force. Science 1992, 256:1692-1695.
22. Georgopoulos A.P., Kalaska J.F., Caminiti R., Massey J.T. On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. J. Neurosci. 1982, 2:1527-1537.
23. Graupe D., Kohn K.H. Functional neuromuscular stimulator for short-distance ambulation by certain thoracic-level spinal-cord-injured paraplegics. Surg. Neurol. 1998, 50:202-207.
24. Handa Y., Hoshimiya N. Functional electrical stimulation for the control of the upper extremities. Med. Prog. Technol. 1987, 12:51-63.
25. Hart R.L., Kilgore K.L., Peckham P.H. A comparison between control methods for implanted FES hand-grasp systems. IEEE Trans. Rehabil. Eng. 1998, 6:208-218.
26. Hatsopoulos N., Joshi J., O'Leary J.G. Decoding continuous and discrete motor behaviors using motor and premotor cortical ensembles. J. Neurophysiol. 2004, 92:1165-1174.
27. Hepp-Reymond M.C., Wyss U.R., Anner R. Neuronal coding of static force in the primate motor cortex. J. Physiol. Paris 1978, 74:287-291.
28. Hochberg L.R., Serruya M.D., Friehs G.M., Mukand J.A., Saleh M., Caplan A.H., et al. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 2006, 442:164-171.
29. Holdefer R.N., Miller L.E. Primary motor cortical neurons encode functional muscle synergies. Exp. Brain Res. 2002, 146:233-243.
30. Hoshimiya N., Naito A., Yajima M., Handa Y. A multichannel FES system for the restoration of motor functions in high spinal cord injury patients: a respiration-controlled system for multijoint upper extremity. IEEE Trans. Biomed. Eng. 1989, 36:754-760.
31. Humphrey D.R., Schmidt E.M., Thompson W.D. Predicting measures of motor performance from multiple cortical spike trains. Science 1970, 170:758-761.
32. Hunter I.W., Korenberg M.J. The identification of nonlinear biological systems: Wiener and Hammerstein cascade models. Biol. Cybern. 1986, 55:135-144.
33. Jarosiewicz B., Chase S.M., Fraser G.W., Velliste M., Kass R.E., Schwartz A.B. Functional network reorganization during learning in a brain-computer interface paradigm. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:19486-19491.
34. Johnston T.E., Betz R.R., Smith B.T., Benda B.J., Mulcahey M.J., Davis R., et al. Implantable FES system for upright mobility and bladder and bowel function for individuals with spinal cord injury. Spinal Cord 2005, 43:713-723.
35. Kalaska J.F., Hyde M.L. Area 4 and area 5: differences between the load direction-dependent discharge variability of cells during active postural fixation. Exp. Brain Res. 1985, 59:197-202.
36. Kargo W.J., Giszter S.F. Rapid correction of aimed movements by summation of force-field primitives. J. Neurosci. 2000, 20:409-426.
37. Keith M.W., Peckham P.H., Thrope G.B., Stroh K.C., Smith B., Buckett J.R., et al. Implantable functional neuromuscular stimulation in the tetraplegic hand. J. Hand Surg. Am. 1989, 14:524-530.
38. Kennedy P.R., Bakay R.A. Restoration of neural output from a paralyzed patient by a direct brain connection. Neuroreport 1998, 9:1707-1711.
39. Kernell D., Donselaar Y., Eerbeek O. Effects of physiological amounts of high- and low-rate chronic stimulation on fast-twitch muscle of the cat hindlimb. II. Endurancerelated properties. J. Neurophysiol. 1987, 58:614-627.
40. Kim S.P., Simeral J.D., Hochberg L.R., Donoghue J.P., Black M.J. Neural control of computer cursor velocity by decoding motor cortical spiking activity in humans with tetraplegia. J. Neural Eng. 2008, 5:455-476.
41. Lauer R.T., Peckham P.H., Kilgore K.L. EEG-based control of a hand grasp neuroprosthesis. Neuroreport 1999, 10:1767-1771.
42. Lebedev M.A., Nicolelis M.A. Brain-machine interfaces: past, present and future. Trends Neurosci. 2006, 29:536-546.
43. Leventhal D.K., Durand D.M. Subfascicle stimulation selectivity with the flat interface nerve electrode. Ann. Biomed. Eng. 2003, 31:643-652.
44. Liberson W.T., Holmquest H.J., Scot D., Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch. Phys. Med. Rehabil. 1961, 42:101-105.
45. Miller L.E., van Kan P.L.E., Sinkjaer T., Andersen T., Harris G.D., Houk J.C. Correlation of primate red nucleus discharge with muscle activity during free-form arm movements. J. Physiol. London 1993, 469:213-243.
46. Moritz C.T., Perlmutter S.I., Fetz E.E. Direct control of paralysed muscles by cortical neurons. Nature 2008, 456:639-642.
47. Morrow M.M., Jordan L.R., Miller L.E. Direct comparison of the task-dependent discharge of M1 in hand space and muscle space. J. Neurophysiol. 2007, 97:1786-1798.
48. Muir R.B., Lemon R.N. Corticospinal neurons with a special role in precision grip. Brain Res. 1983, 261:312-316.
49. Musallam S., Corneil B.D., Greger B., Scherberger H., Andersen R.A. Cognitive control signals for neural prosthetics. Science 2004, 305:258-262.
50. Peckham P.H., Keith M.W., Kilgore K.L., Grill J.H., Wuolle K.S., Thrope G.B., et al. Efficacy of an implanted neuroprosthesis for restoring hand grasp in tetraplegia: a multicenter study. Arch. Phys. Med. Rehabil. 2001, 82:1380-1388.
51. Peckham P.H., Knutson J.S. Functional electrical stimulation for neuromuscular applications. Annu. Rev. Biomed. Eng. 2005, 7:327-360.
52. Peckham P.H., Marsolais E.B., Mortimer J.T. Restoration of key grip and release in the C6 tetraplegic patient through functional electrical stimulation. J. Hand Surg. Am. 1980, 5:462-469.
53. Peckham P.H., Mortimer J.T., Marsolais E.B. Alteration in the force and fatigability of skeletal muscle in quadriplegic humans following exercise induced by chronic electrical stimulation. Clin. Orthop. Relat. Res. 1976, 114:326-333.
54. Pfurtscheller G., Muller G.R., Pfurtscheller J., Gerner H.J., Rupp R. 'Thought'-control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia. Neurosci. Lett. 2003, 351:33-36.
55. Phillips C.G. Laying the ghost of 'muscles versus movements'. Can. J. Neurol. Sci. 1975, 66:209-218.
56. Piccolino M. Animal electricity and the birth of electrophysiology: the legacy of Luigi Galvani. Brain Res. Bull. 1998, 46:381-407.
57. Pohlmeyer E.A., Oby E.R., Perreault E.J., Solla S.A., Kilgore K.L., Kirsch R.F., et al. Toward the restoration of hand use to a paralyzed monkey: brain-controlled functional electrical stimulation of forearm muscles. PLoS ONE 2009, 4:e5924.
58. Pohlmeyer E.A., Perreault E.J., Slutzky M.W., Kilgore K.L., Kirsch R.F., Taylor D.M., Miller L.E. Real-time control of the hand by intracortically controlled functional neuromuscular stimulation. IEEE 10th International Conference on Rehab Robotics 2007, vol. 10:454-458. Noordwijk, The Netherlands.
59. Pohlmeyer E.A., Solla S.A., Perreault E.J., Miller L.E. Prediction of upper limb muscle activity from motor cortical discharge during reaching. J. Neural Eng. 2007, 4:369-379.
60. Popovic D., Stojanovic A., Pjanovic A., Radosavljevic S., Popovic M., Jovic S., et al. Clinical evaluation of the bionic glove. Arch. Phys. Med. Rehabil. 1999, 80:299-304.
61. Popovic D., Tomovic R., Schwirtlich L. Hybrid assistive system--the motor neuroprosthesis. IEEE Trans. Biomed. Eng. 1989, 36:729-737.
62. Popovic M.B. Control of neural prostheses for grasping and reaching. Med. Eng. Phys. 2003, 25:41-50.
63. Popovic M.R., Popovic D.B., Keller T. Neuroprostheses for grasping. Neurol. Res. 2002, 24:443-452.
64. Prochazka A., Gauthier M., Wieler M., Kenwell Z. The bionic glove: an electrical stimulator garment that provides controlled grasp and hand opening in quadriplegia. Arch. Phys. Med. Rehabil. 1997, 78:608-614.
65. Riehle A., Requin J. Neuronal correlates of the specification of movement direction and force in four cortical areas of the monkey. Behav. Brain Res. 1995, 70:1-13.
66. Sanchez J., Principe J., Carmena J., Lebedev M., Nicolelis M.A. Simultaneus prediction of four kinematic variables for a brain-machine interface using a single recurrent neural network. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2004, 7:5321-5324.
67. Santello M., Flanders M., Soechting J.F. Postural hand synergies for tool use. J. Neurosci. 1998, 18:10105-10115.
68. Santello M., Soechting J.F. Force synergies for multifingered grasping. Exp. Brain Res. 2000, 133:457-467.
69. Santhanam G., Ryu S.I., Yu B.M., Afshar A., Shenoy K.V. A high-performance brain-computer interface. Nature 2006, 442:195-198.
70. Schieber M.H. Individuated finger movements: rejecting the labeled-line hypothesis. Hand and Brian. The Neurophysiology and Psychology of Hand Movements 1996, 81-97. Academic Press, San Diego. A.M. Wing, P. Haggard, J.R. Flanagan (Eds.).
71. Scott S.H., Kalaska J.F. Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. J. Neurophysiol. 1997, 77:826-852.
72. Scott T.R., Peckham P.H., Kilgore K.L. Tri-state myoelectric control of bilateral upper extremity neuroprostheses for tetraplegic individuals. IEEE Trans. Rehabil. Eng. 1996, 4:251-263.
73. Sergio L.E., Hamel-Paquet C., Kalaska J.F. Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. J. Neurophysiol. 2005, 94:2353-2378.
74. Serruya M.D., Hatsopoulos N.G., Paninski L., Fellows M.R., Donoghue J.P. Instant neural control of a movement signal. Nature 2002, 416:141-142.
75. Shoham S., Paninski L.M., Fellows M.R., Hatsopoulos N.G., Donoghue J.P., Normann R.A. Statistical encoding model for a primary motor cortical brain-machine interface. IEEE Trans. Biomed. Eng. 2005, 52:1312-1322.
76. Snoek G.J., IJzerman M.J., in 't Groen F.A., Stoffers T.S., Zilvold G. Use of the NESS handmaster to restore handfunction in tetraplegia: clinical experiences in ten patients. Spinal Cord 2000, 38:244-249.
77. Solomonow M., Aguilar E., Reisin E., Baratta R.V., Best R., Coetzee T., et al. Reciprocating gait orthosis powered with electrical muscle stimulation (RGO II). Part I: Performance evaluation of 70 paraplegic patients. Orthopedics 1997, 20:315-324.
78. Taylor D.M., Tillery S.I., Schwartz A.B. Direct cortical control of 3D neuroprosthetic devices. Science 2002, 296:1829-1832.
79. Thach W.T. Correlation of neural discharge with pattern and force of muscular activity, joint position, and direction of next movement in motor cortex and cerebellum. J. Neurophysiol. 1978, 41:654-676.
80. Ting L.H., Macpherson J.M. A limited set of muscle synergies for force control during a postural task. J. Neurophysiol. 2005, 93:609-613.
81. Todorov E., Ghahramani Z. Analysis of the synergies underlying complex hand manipulation. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2004, 6:4637-4640.
82. Tresch M.C., Cheung V.C., d'Avella A. Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. J. Neurophysiol. 2006, 95:2199-2212.
83. Tresch M.C., Jarc A. The case for and against muscle synergies. Curr. Opin. Neurobiol. 2009, 19:601-607.
84. Vodovnik L., Kralj A., Stanic U., Acimovic R., Gros N. Recent applications of functional electrical stimulation to stroke patients in Ljubljana. Clin. Orthop. Relat. Res. 1978, 131:64-70.
85. Weber D.J., Stein R.B., Chan K.M., Loeb G.E., Richmond F.J., Rolf R., et al. Functional electrical stimulation using microstimulators to correct foot drop: a case study. Can. J. Physiol. Pharmacol. 2004, 82:784-792.
86. Wessberg J., Stambaugh C.R., Kralik J.D., Beck P.D., Laubach M., Chapin J.K., et al. Real-time prediction of hand trajectory by ensembles of cortical neurons in primates. Nature 2000, 408:361-365.
87. Westwick D.T., Pohlmeyer E.A., Solla S.A., Miller L.E., Perreault E.J. Identification of multiple-input systems with highly coupled inputs: application to EMG prediction from multiple intracortical electrodes. Neural Comput. 2006, 18:329-355.
88. Wuolle K.S., Van Doren C.L., Thrope G.B., Keith M.W., Peckham P.H. Development of a quantitative hand grasp and release test for patients with tetraplegia using a hand neuroprosthesis. J Hand Surg. Am. 1994, 19:209-218.