Neuroprosthetic technology for individuals with spinal cord injury

Journal of Spinal Cord Medicine

Volumn 36, Issue 4, 2013, Pages 258-272

  Collinger, Jennifer L ^a,b,c   Foldes, Stephen ^a,b,d   Bruns, Tim M ^b   Wodlinger, Brian ^b,d   Gaunt, Robert ^b,c   Weber, Douglas J ^a,b,c,d  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c University of Pittsburgh   (United States)

^d CENTER FOR THE NEURAL BASIS OF COGNITION   (United States)

Author keywords

Assistive technology; Brain computer interface; Central pattern generators; Electrical stimulation; Epidural stimulation; Neural interface; Neurogenic bladder; Neuroprosthesis; Paraplegia; Rehabilitation; Spinal cord injuries; Tetraplegia

Indexed keywords

BLADDER DYSFUNCTION; BRAIN COMPUTER INTERFACE; COMORBIDITY; ELECTROCORTICOGRAPHY; ELECTRODE; FUNCTIONAL ELECTRICAL STIMULATION; HUMAN; MICROELECTRODE; MICTURITION REFLEX; MOVEMENT (PHYSIOLOGY); MUSCLE ATROPHY; MUSCLE CONTRACTION; NERVE CONDUCTION; NERVE STIMULATION; NEUROPROSTHESIS; PARAPLEGIA; PRIMARY SOMATOSENSORY CORTEX; PROPRIOCEPTION; REVIEW; ROBOTIC EXOSKELETON; SENSATION; SENSORY CORTEX; SENSORY FEEDBACK; SPINAL CORD INJURY; SPINAL CORD STIMULATION;

BRAIN-COMPUTER INTERFACES; ELECTRIC STIMULATION THERAPY; ELECTROMYOGRAPHY; FEEDBACK, PHYSIOLOGICAL; HUMANS; PROSTHESES AND IMPLANTS; RECOVERY OF FUNCTION; SPINAL CORD INJURIES; URINARY BLADDER;

EID: 84880814828     PISSN: 10790268     EISSN: 20457723     Source Type: Journal    
DOI: 10.1179/2045772313Y.0000000128     Document Type: Review

References (178)

1. Anderson KD. Targeting recovery: priorities of the spinal cordinjured population. J Neurotrauma 2004;21(10):1371-83.
2. Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F. Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord 2004;42(9):526-32.
3. Collinger JL, Boninger ML, Bruns TM, Curley K, Wang W, Weber DJ. Functional priorities, assistive technology, and braincomputer interfaces after spinal cord injury. J Rehabil Res Dev 2013;50(2):145-60.
4. Brown-Triolo DL, Roach MJ, Nelson K, Triolo RJ. Consumer perspectives on mobility: implications for neuroprosthesis design. J Rehabil Res Dev 2002;39(6):659-69.
5. Gater DR, Dolbow D, Tsui B, Gorgey AS. Functional electrical stimulation therapies after spinal cord injury. NeuroRehabilitation 2011;28(3):231-48.
6. Peckham PH, Knutson JS. Functional electrical stimulation for neuromuscular applications. Ann Rev Biomed Eng 2005;7: 327-60.
7. Castro MJ, Apple DF, Hillegass E, Dudley G. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Applied Physiol Occup Physiol 1999;80(4):373-8.
8. Cope TC, Bodine SC, Fournier M, Edgerton VR. Soleus motor units in chronic spinal transected cats: physiological and morphological alterations. J Neurophysiol 1986;55(6):1202-20.
9. Lieber RL, Fridén JO, Hargens AR, Feringa ER. Long-term effects of spinal cord transection on fast and slow rat skeletal muscle. Exp Neurol 1986;91(3):435-48.
10. Gordon T, Mao J. Muscle atrophy and procedures for training after spinal cord injury. Phys Therapy 1994;74(1):50-60.
11. Polasek KH, Hoyen HA, Keith MW, Tyler DJ. Human nerve stimulation thresholds and selectivity using a multi-contact nerve cuff electrode. IEEE Trans Neural Sys Rehabil Eng 2007; 15(1):76-82.
12. Fisher LE, Miller ME, Bailey SN, Davis JA, Anderson JS, Rhode L, et al. Standing after spinal cord injury with four-contact nervecuff electrodes for quadriceps stimulation. IEEE Trans Neural Sys Rehabil Eng 2008;16(5):473-8.
13. Triolo RJ, Bieri C, Uhlir J, Kobetic R, Scheiner A, Marsolais EB. Implanted functional neuromuscular stimulation systems for individuals with cervical spinal cord injuries: Clinical case reports. Arch Phys Med Rehabil 1996;77(11):1119-28.
14. Dauty M, Perrouin Verbe B, Maugars Y, Dubois C, Mathe JF. Supralesional and sublesional bone mineral density in spinal cord-injured patients. Bone 2000;27(2):305-9.
15. Herr H. Exoskeletons and orthoses: classification, design challenges and future directions. J Neuroeng Rehabil 2009;6:21.
16. Graupe D, Cerrel-Bazo H, Kern H, Carraro U.Walking performance, medical outcomes and patient training in FES of innervated muscles for ambulation by thoracic-level complete paraplegics. Neurologic Res 2008;30(2):123-30.
17. Klose KJ, Jacobs PL, Broton JG, Guest RS, Needham-Shropshire BM, Lebwohl N, et al. Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 1. Ambulation performance and anthropometric measures. Arch Phys Med Rehabil 1997;78(8):789-93.
18. Brissot R, Gallien P, Le Bot MP, Beaubras A, Laisné D, Beillot J, et al. Clinical experience with functional electrical stimulationassisted gait with Parastep in spinal cord-injured patients. Spine 2000;25(4):501-8.
19. Davis JA, Triolo RJ, Uhlir JP, Bhadra N, Lissy DA, Nandurkar S, et al. Surgical technique for installing an eight-channel neuroprosthesis for standing. Clin Orthop Relat Res 2001;(385):237-52.
20. Fisher LE, Tyler DJ, Anderson JS, Triolo RJ. Chronic stability and selectivity of four-contact spiral nerve-cuff electrodes in stimulating the human femoral nerve. J Neural Eng 2009;6(4): 046010.
21. Dall PM, Müller B, Stallard I, Edwards J, Granat MH. The functional use of the reciprocal hip mechanism during gait for paraplegic patients walking in the Louisiana State University reciprocating gait orthosis. Prosthet Orthot Int 1999;23(2): 152-62.
22. Lotta S, Fiocchi A, Giovannini R, Silvestrin R, Tesio L, Raschi A, et al. Restoration of gait with orthoses in thoracic paraplegia: a multicentric investigation. Paraplegia 1994;32(9):608-15.
23. Kobetic R, To CS, Schnellenberger JR, Audu ML, Bulea TC, Gaudio R, et al. Development of hybrid orthosis for standing, walking, and stair climbing after spinal cord injury. J Rehabil Res Dev 2009;46(3):447-62.
24. del-Ama AJ, Koutsou AD, Moreno JC, de-los-Reyes A, Gil-Agudo A, Pons JL. Review of hybrid exoskeletons to restore gait following spinal cord injury. J Rehabil Res Dev 2012;49(4): 497-514.
25. Popović D, Stojanović A, Pjanović A, Radosavljević S, Popović M, Jović S, et al. Clinical evaluation of the bionic glove. Arch Phys Med Rehabil 1999;80(3):299-304.
26. Popović D, Popović M. Belgrade grasping system. J Electronics 1998;2:21-8.
27. Popovic MR, Keller T, Pappas IP, Dietz V, Morari M. Surfacestimulation technology for grasping and walking neuroprosthesis. IEE Eng Med Biol 2001;20(1):82-93.
28. Ijerman M, Stoffers T, Groon F, Klatte M, Snoek G, Vorsteveld J, et al. The NESS Handmaster orthosis: restoration of hand function in C5 and stroke patients by means of electrical stimulation. J Rehabil Sci 1996;9:86-9.
29. Popovic MR, Popovic DB, Keller T. Neuroprostheses for grasping. Neurolog Res 2002;24(5):443-52.
30. Hoshimiya N, Handa Y. A master-slave type multichannel functional electrical stimulation (FES) system for the control of the paralyzed upper extremities. Automedica 1989;11:209-20.
31. Keith MW, Peckham PH, Thrope GB, Stroh KC, Smith B, Buckett JR, et al. Implantable functional neuromuscular stimulation in the tetraplegic hand. J Hand Surg 1989;14(3):524-30.
32. Ragnarsson KT. Functional electrical stimulation after spinal cord injury: current use, therapeutic effects and future directions. Spinal Cord 2008;46(4):255-74.
33. Kilgore KL, Hoyen HA, Bryden AM, Hart RL, Keith MW, Peckham PH. An implanted upper-extremity neuroprosthesis using myoelectric control. J Hand Surg 2008;33(4):539-50.
34. Triolo R, Nathan R, Handa Y, Keith M, Betz RR, Carroll S, et al. Challenges to clinical deployment of upper limb neuroprostheses. J Rehabil Res Dev 1996;33(2):111-22.
35. Naples GG, Mortimer JT, Scheiner A, Sweeney JD. A spiral nerve cuff electrode for peripheral nerve stimulation. IEEE Trans Biomed Eng 1988;35(11):905-16.
36. Curtis KA, Kindlin CM, Reich KM, White DE. Functional reach in wheelchair users: the effects of trunk and lower extremity stabilization. Arch Phys Med Rehabil 1995;76(4):360-7.
37. Triolo RJ, Boggs L, Miller ME, Nemunaitis G, Nagy J, Bailey SN. Implanted electrical stimulation of the trunk for seated postural stability and function after cervical spinal cord injury: a single case study. Arch Phys Med Rehabil; 2009; 90(2):340-7.
38. Gagnon D, Verrier MC, Masani K, Nadeau S, Aissaoui R, Popovic MR. Effects of trunk impairments on manual wheelchair propulsion among individuals with a spinal cord injury: a brief overview and future challenges. Top Spinal Cord Inj Rehabil 2009;15(2):59-70.
39. Sherrington CS. The integrative action of the nervous system. New Haven, CT: Yale University Press; 1906.
40. Amemiya M, Yamaguchi T. Fictive locomotion of the forelimb evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat. Neurosci Lett 1984;50(1-3):91-6.
41. Cohen AH, Wallén P. The neuronal correlate of locomotion in fish. 'Fictive swimming' induced in an in vitro preparation of the lamprey spinal cord. Exp Brain Res 1980;41(1):11-8.
42. Rossignol S, Dubuc R, Gossard J-P. Dynamic sensorimotor interactions in locomotion. Physiol Rev 2006;86(1):89-154.
43. Rossignol S, Chau C, Brustein E, Bélanger M, Barbeau H, Drew T. Locomotor capacities after complete and partial lesions of the spinal cord. Acta Neurobiol Exp 1996;56(1):449-63.
44. Rossignol S, Bouyer L, Barthelemy D, Langlet C, Leblond H. Recovery of locomotion in the cat following spinal cord lesions. Brain Res Rev 2002;40(1-3):257-66.
45. Barbeau H, McCrea D, O'Donovan M, Rossignol S, Grill W, Lemay M. Tapping into spinal circuits to restore motor function. Brain Res Rev 1999;30(1):27-51.
46. Racz GB, McCarron RF, Talboys P. Percutaneous dorsal column stimulator for chronic pain control. Spine 1989;14(1):1-4.
47. Pinter MM, Gerstenbrand F, Dimitrijevic MR. Epidural electrical stimulation of posterior structures of the human lumbosacral cord: 3. Control Of spasticity. Spinal Cord 2000;38(9):524-31.
48. Dimitrijevic MR, Gerasimenko Y, Pinter MM. Evidence for a spinal central pattern generator in humans. Ann N Y Acad Sci 1998;860:360-76.
49. Carhart MR, He J, Herman R, D'Luzansky S, Willis WT. Epidural spinal-cord stimulation facilitates recovery of functional walking following incomplete spinal-cord injury. IEEE Trans Neural Syst Rehabil Eng 2004;12(1):32-42.
50. Huang H, He J, Herman R, Carhart MR. Modulation effects of epidural spinal cord stimulation on muscle activities during walking. IEEE Trans Neural Syst Rehabil Eng 2006;14(1):14-23.
51. Herman R, He J, D'Luzansky S, Willis W, Dilli S. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured. Spinal Cord 2002;40(2):65-8.
52. Harkema S, Gerasimenko Y, Hodes J, Burdick J, Angeli C, Chen Y, et al. Effect of epidural stimulation of the lumbosacral spinal cord on voluntary movement, standing, and assisted stepping after motor complete paraplegia: a case study. Lancet 2011; 377(9781):1938-47.
53. Shah PK, Gerasimenko Y, Shyu A, Zhong H, Roy RR, Edgerton VR. Variability in step training enhances locomotor recovery after a spinal cord injury. Eur J Neurosci 2012;36(1):2054-62.
54. Gad P, Woodbridge J, Lavrov I, Zhong H, Roy RR, Sarrafzadeh M, et al. Forelimb EMG-based trigger to control an electronic spinal bridge to enable hindlimb stepping after a complete spinal cord lesion in rats. J Neuroeng Rehabil 2012;9(1):38.
55. Pikov V, Bullara L, McCreery DB. Intraspinal stimulation for bladder voiding in cats before and after chronic spinal cord injury. J Neural Eng 2007;4(4):356-68.
56. McCreery D, Pikov V, Lossinsky A, Bullara L, Agnew W. Arrays for chronic functional microstimulation of the lumbosacral spinal cord. IEEE Trans Neural Sys Eng 2004;12(2):195-207.
57. Grill W, Bhadra N, Wang B. Bladder and urethral pressures evoked by microstimulation of the sacral spinal cord in cats. Brain Res 1999;836(1-2):19-30.
58. Tai C, Booth A, de Groat W, Roppolo J. Bladder and urethral sphincter responses evoked by microstimulation of S2 sacral spinal cord in spinal cord intact and chronic spinal cord injured cats. Exp Neurol 2004;190(1):171-83.
59. Nashold B, Friedman H, Grimes J. Electrical stimulation of the conus medullaris to control the bladder in the paraplegic patient. A 10-year review. Appl Neurophysiol 1981;44(4):225-32.
60. Mushahwar VK, Gillard DM, Gauthier MJA, Prochazka A. Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements. IEEE Trans Neural Sys Rehabil Eng 2002;10(1):68-81.
61. Saigal R, Renzi C, Mushahwar VK. Intraspinal microstimulation generates functional movements after spinal-cord injury. IEEE Trans Neural Sys Rehabil Eng 2004;12(4):430-40.
62. Mushahwar VK, Horch K. Muscle recruitment through electrical stimulation of the lumbo-sacral spinal cord. IEEE Trans Rehabil Eng 2000;8(1):22-9.
63. Holinski BJ, Mazurek KA, Everaert DG, Stein RB, Mushahwar VK. Restoring stepping after spinal cord injury using intraspinal microstimulation and novel control strategies. IEEE EMBC 2011; 2011:5798-801.
64. Mushahwar VK, Aoyagi Y, Stein RB, Prochazka A. Movements generated by intraspinal microstimulation in the intermediate gray matter of the anesthetized, decerebrate, and spinal cat. Can J Physiol Pharmacol 2004;82(8-9):702-14.
65. Gaunt RA, Prochazka A, Mushahwar VK, Guevremont L, Ellaway PH. Intraspinal microstimulation excites multisegmental sensory afferents at lower stimulus levels than local alpha-motoneuron responses. J Neurophysiol 2006;96(6):2995-3005.
66. Guevremont L, Renzi C, Norton J, Kowalczewski J, Saigal R, Mushahwar VK. Locomotor-related networks in the lumbosacral enlargement of the adult spinal cat: activation through intraspinal Microstimulation. IEEE Trans Neural Sys Rehabil Eng 2006; 14(3):266-72.
67. Bamford JA, Putman CT, Mushahwar VK. Intraspinal microstimulation preferentially recruits fatigue-resistant muscle fibres and generates gradual force in rat. J Physiol 2005;569(Pt 3): 873-84.
68. Gaunt RA, Prochazka A. Control of urinary bladder function with devices: successes and failures. Prog Brain Res 2006;152: 163-94.
69. Martens FMJ, Heesakkers JPFA. Clinical results of a brindley procedure: sacral anterior root stimulation in combination with a rhizotomy of the dorsal roots. Adv Urol 2011;2011(Article ID 709708):7.
70. Hohenfellner M, Humke J, Hampel C, Dahms S, Matzel KE, Roth S, et al. Chronic sacral neuromodulation for treatment of neurogenic bladder dysfunction: long-term results with unilateral implants. Urol 2001;58(6):887-92.
71. Sievert K-D, Amend B, Gakis G, Toomey P, Badke A, Kaps HP, et al. Early sacral neuromodulation prevents urinary incontinence after complete spinal cord injury. Ann Neurol 2010;67(1):74-84.
72. Shi P, Zhao X, Wang J, Lan N. Effects of acute sacral neuromodulation on bladder reflex in complete spinal cord injury rats. Neuromod 2012 Nov 5.
73. Peters KM, Carrico DJ, Perez-Marrero RA, Khan AU, Wooldridge LS, Davis GL, et al. Randomized trial of percutaneous tibial nerve stimulation versus sham efficacy in the treatment of overactive bladder syndrome: results from the SUmiT trial. J Urol 2010;183(4):1438-43.
74. Andrews BJ, Reynard JM. Transcutaneous posterior tibial nerve stimulation for treatment of detrusor hyperreflexia in spinal cord injury. J Urol 2003;170(3):926.
75. Amarenco G, Ismael SS, Even-Schneider A, Raibaut P, Demaille-Wlodyka S, Parratte B, et al. Urodynamic effect of acute transcutaneous posterior tibial nerve stimulation in overactive bladder. J Urol 2003;169(6):2210-15.
76. Martens FMJ, den Hollander PP, Snoek GJ, Koldewijn EL, van Kerrebroeck PEV, Heesakkers JPFA. Quality of life in complete spinal cord injury patients with a brindley bladder stimulator compared to a matched control group. Neurourol Urodynam 2011;30:551-5.
77. Sanders PM, Ijzerman MJ, Roach MJ, Gustafson KJ. Patient preferences for next generation neural prostheses to restore bladder function. Spinal Cord 2011;49(1):113-19.
78. Boger AS, Bhadra N, Gustafson KJ. High frequency sacral root nerve block allows bladder voiding. Neurourol Urodynam 2012; 31(5):677-82.
79. Mariano TY, Bhadra N, Gustafson KJ. Suppression of reflex urethral responses by sacral dermatome stimulation in an acute spinalized feline model. Neurourol Urodynam 2010;29:494-500.
80. McCoin JL, Bhadra N, Gustafson KJ. Electrical stimulation of sacral dermatomes can suppress aberrant urethral reflexes in felines with chronic spinal cord injury. Neurourol Urodyn 2013; 32(1):92-7.
81. Boggs JW, Wenzel BJ, Gustafson KJ, Grill WM. Bladder emptying by intermittent electrical stimulation of the pudendal nerve. J Neural Eng 2006;3(1):43-51.
82. Peters KM, Feber KM, Bennett RC. Sacral versus pudendal nerve stimulation for voiding dysfunction: a prospective, singleblinded, randomized, crossover trial. Neurourol Urodyn 2005; 24(7):643-7.
83. Tai C, Chen M, Shen B, Wang J, Liu H, Roppolo JR, et al. Plasticity of urinary bladder reflexes evoked by stimulation of pudendal afferent nerves after chronic spinal cord injury in cats. Exp Neurol 2011;228(1):109-17.
84. Opisso E, Borau A, Rijkhoff NJM. Urethral sphincter EMG-controlled dorsal penile/clitoral nerve stimulation to treat neurogenic detrusor overactivity. J Neural Eng 2011;8(3):036001.
85. Bruns TM, Bhadra N, Gustafson KJ. Variable patterned pudendal nerve stimuli improves reflex bladder activation. IEEE Trans Neural Sys Rehabil Eng 2008;16(2):140-8.
86. Snellings AE, Grill WM. Effects of stimulation site and stimulation parameters on bladder inhibition by electrical nerve stimulation. BJU Int 2012;110(1):136-43.
87. Kennelly MJ, Bennett ME, Grill WM, Grill JH, Boggs JW. Electrical stimulation of the urethra evokes bladder contractions and emptying in spinal injury men: Case studies. J Spinal Cord Med 2011;34(3):315-21.
88. Yoo PB, Klein SM, Grafstein NH, Amundsen CL, Horvath EE, Webster GD, et al. Pudendal nerve stimulation evokes reflex bladder contractions in persons with chronic spinal cord injury. Neurourol Urodyn 2007;26(7):1020-3.
89. McGee MJ, Yoo PB, Grill WM. Selective co-stimulation of pudendal afferents enhances reflex bladder activation. Conf Proc Eng Med Biol Soc., Boston, MA, USA; 2011:1057-60.
90. Tai C, Wang J, Wang X, de Groat WC, Roppolo Jr. Voiding reflex in chronic spinal cord injured cats induced by stimulating and blocking pudendal nerves. Neurourol Urodynam 2007; 26(6):879.
91. Sainburg RL, Poizner H, Ghez C. Loss of proprioception produces deficits in interjoint coordination. J Neurophysiol 1993; 70(5):2136-47.
92. Sainburg RL, Ghilardi MF, Poizner H, Ghez C. Control of limb dynamics in normal subjects and patients without proprioception. J Neurophysiol 1995;73(2):820-35.
93. Pei Y-C, Hsiao SS, Craig JC, Bensmaia SJ. Shape invariant coding of motion direction in somatosensory cortex. PLoS Biology 2010;8(2):e1000305.
94. Suminski AJ, Tkach DC, Fagg AH, Hatsopoulos NG. Incorporating feedback from multiple sensory modalities enhances brain-machine interface control. J Neurosci 2010; 30(50):16777-87.
95. London BM, Jordan LR, Jackson CR, Miller LE. Electrical stimulation of the proprioceptive cortex (area 3a) used to instruct a behaving monkey. IEEE Neural Sys Rehabil Eng 2008;16(1): 32-6.
96. Romo R, Hernandez A, Zainos A, Salinas E. Somatosensory discrimination based on cortical microstimulation. Nature 1998; 392(6674):387-90.
97. O'Doherty JE, Lebedev MA, Hanson TL, Fitzsimmons NA, Nicolelis MAL. A brain-machine interface instructed by direct intracortical microstimulation. Front Intergr Neurosci 2009; 3:20.
98. O'Doherty JE, Lebedev MA, Ifft PJ, Zhuang KZ, Shokur S, Bleuler H, et al. Active tactile exploration using a brainmachine-brain interface. Nature 2011;479(7372):228-31.
99. Berg J, Dammann J, Tenore F, Tabot G, Boback J, Manfredi L, et al. Behavioral demonstration of a somatosensory neuroprosthesis. IEEE Trans Neural Sys Rehabil Eng 2013 March 6.
100. Schmidt EM, Bak MJ, Hambrecht FT, Kufta CV, O'Rourke DK, Vallabhanath P. Feasibility of a visual prosthesis for the blind based on intracortical microstimulation of the visual cortex. Brain 1996;119(2):507-22.
101. Bak M, Girvin JP, Hambrecht FT, Kufta CV, Loeb GE, Schmidt EM. Visual sensations produced by intracortical microstimulation of the human occipital cortex. Med Biol Eng Comp 1990;28(3): 257-9.
102. McCreery D, Pikov V, Troyk PR. Neuronal loss due to prolonged controlled-current stimulation with chronically implanted microelectrodes in the cat cerebral cortex. J Neural Eng 2010;7(3): 36005.
103. Parker RA, Davis TS, House PA, Normann RA, Greger B. The functional consequences of chronic, physiologically effective intracortical microstimulation. Prog Brain Res 2011;194: 145-65.
104. Cui XT, Zhou DD. Poly (3,4-ethylenedioxythiophene) for chronic neural stimulation. IEEE Trans Neural Syst Rehabil Eng 2007; 15(4):502-8.
105. Robblee LS. Activated Ir: An electrode suitable for reversible charge injection in saline solution. J Electrochem Soc 1983; 130(3):731.
106. Cogan SF, Ehrlich J, Plante TD, Smirnov A, Shire DB, Gingerich M, et al. Sputtered iridium oxide films for neural stimulation electrodes. J Biomed Mater Res Part B, App Biomater 2009;89B(2): 353-61.
107. Hadjinicolaou AE, Leung RT, Garrett DJ, Ganesan K, Fox K, Nayagam DAX, et al. Electrical stimulation of retinal ganglion cells with diamond and the development of an all diamond retinal prosthesis. Biomaterials 2012;33(24):5812-20.
108. Garrett DJ, Ganesan K, Stacey A, Fox K, Meffin H, Prawer S. Ultra-nanocrystalline diamond electrodes: optimization towards neural stimulation applications. J Neural Eng 2012;9(1):16002.
109. Venkatraman S, Hendricks J, King ZA, Sereno AJ, Richardson-Burns S, Martin D, et al. In vitro and in vivo evaluation of PEDOT microelectrodes for neural stimulation and recording. IEEE Trans Neural Sys Rehabil Eng 2011;19(3):307-16.
110. Wilder AM, Hiatt SD, Dowden BR, Brown NAT, Normann RA, Clark GA. Automated stimulus-response mapping of high-electrode-count neural implants. IEEE Trans Neural Syst Rehabil Eng 2009;17(5):504-11.
111. Kurstjens GAM, Borau A, Rodríguez A, Rijkhoff NJM, Sinkjaer T. Intraoperative recording of electroneurographic signals from cuff electrodes on extradural sacral roots in spinal cord injured patients. J Urol 2005;174(4):1482-7.
112. Inmann A, Haugland M. Functional evaluation of natural sensory feedback incorporated in a hand grasp neuroprosthesis. Med Eng Phys 2004;26(6):439-47.
113. Haugland MK, Sinkjar T. Cutaneous whole nerve recordings used for correction of footdrop in hemiplegic man. IEEE Trans Rehabil Eng 1995;3(4):307-17.
114. Zariffa J, Nagai MK, Daskalakis ZJ, Popovic MR. Influence of the number and location of recording contacts on the selectivity of a nerve cuff electrode. IEEE Trans Neural Syst Rehabil Eng 2009;17(5):420-7.
115. Tyler DJ, Durand DM. Chronic response of the rat sciatic nerve to the flat interface nerve electrode. Ann Biomed Eng 2003;31(6): 633-42.
116. Wodlinger B, Durand DM. Selective recovery of fascicular activity in peripheral nerves. J Neural Eng 2011;8(5):056005.
117. Yoshida K, Horch KW. Closed-loop control of ankle position using muscle afferent feedback with functional neuromuscular stimulation. IEEE Trans Biomed Eng 1996;43(2):167-76.
118. Stein RB, Branner A, Fernandez E, Aoyagi Y, Normann RA. Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve. IEEE Trans Biomed Eng 2004;51(1):146-51.
119. Clark GA, Ledbetter NM, Warren DJ, Harrison RR. Recording Sensory and Motor Information from Peripheral Nerves with Utah Slanted Electrode Arrays. Conf Proc IEEE Eng Med Biol Soc. Boston, MA, USA: IEEE; 2011:4641-4.
120. Micera S, Jensen W, Sepulveda F, Riso RR, Sinkjaer T. Neurofuzzy extraction of angular information from muscle afferents for ankle control during standing in paraplegic subjects: an animal model. IEEE Trans Biomed Eng 2001;48(7):787-94.
121. Micera S, Navarro X, Carpaneto J, Citi L, Tonet O, Rossini PM, et al. On the use of longitudinal intrafascicular peripheral interfaces for the control of cybernetic hand prostheses in amputees. IEEE Trans Neural Syst Rehabil Eng 2008;16(5):453-72.
122. Moss CW, Kilgore KL, Peckham PH. A novel command signal for motor neuroprosthetic control. Neurorehabil Neural Repair 2011;25(9):847-54.
123. Nunez PL, Srinivasan R. Electric fields of the brain: The neurophysics of EEG, 2nd ed. USA: Oxford University Press; 2005.
124. Mason SG, Bashashati A, Fatourechi M, Navarro KF, Birch GE, Ason SGM, et al. A comprehensive survey of brain interface technology designs. Ann Biomed Eng 2007;35(2):137-69.
125. Wolpaw JR, Birbaumer N, McFarland DJ, Pfurtscheller G, Vaughan TM. Brain-computer interfaces for communication and control. Clin Neurophysiol 2002;113(6):767-91.
126. Donchin E, Spencer KM, Wijesinghe R. The mental prosthesis: assessing the speed of a P300-based brain-computer interface. IEEE Trans Rehabil Eng 2000;8(2):172-9.
127. Regan D. Steady-state evoked potentials. J Opt Soc Am 1977; 67(11):1475-89.
128. Bastos TF, Muller SMT, Benevides AB, Sarcinelli-Filho M. Robotic wheelchair commanded by SSVEP, motor imagery and word generation. Conf Proc IEEE Eng Med Biol Soc; 2011:4753-6.
129. Lacourse MG, Cohen MJ, Lawrence KE, Romero DH. Cortical potentials during imagined movements in individuals with chronic spinal cord injuries. Behav Brain Res 1999;104:73-88.
130. Gourab K, Schmit BD. Changes in movement-related β-band EEG signals in human spinal cord injury. Clin Neurophysiol 2010;121(12):2017-23.
131. Shoham S, Halgren E, Maynard EM, Normann RA. Motorcortical activity in tetraplegics. Nature 2001;413(6858):793.
132. McFarland DJ, Sarnacki WA, Wolpaw Jr. Electroencephalographic (EEG) control of three-dimensional movement. J Neural Eng 2010;7(3):036007.
133. Wolpaw JR, McFarland DJ. Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. Proc Nat Acad Soc USA 2004;101(51):17849-54.
134. Pfurtscheller G, Müller GR, Pfurtscheller J, Gerner HJ, Rupp R. 'Thought ' -control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia. Neurosci Lett 2003; 351(1):33-6.
135. Pfurtscheller G, Brunner C, Schlögl A, Lopes da Silva FH. Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks. NeuroImage 2006;31(1): 153-9.
136. Foldes ST, Taylor DM. Offline comparison of spatial filters for two-dimensional movement control with noninvasive field potentials. J Neural Eng 2011;8(4):046022.
137. Foldes ST, Taylor DM. Discreet discrete commands for assistive and neuroprosthetic devices. IEEE Trans Neural Sys Rehabil Eng 2010;18(3):236-44.
138. Leeb R, Sagha H, Chavarriaga R, Millán JDR. A hybrid braincomputer interface based on the fusion of electroencephalographic and electromyographic activities. J Neural Eng 2011; 8(2):025011.
139. Leuthardt EC, Schalk G, Wolpaw JR, Ojemann JG, Moran DW. A brain-computer interface using electrocorticographic signals in humans. J Neural Eng; 2004;1(2):63-71.
140. Pistohl T, Ball T, Schulze-Bonhage A, Aertsen A, Mehring C. Prediction of arm movement trajectories from ECoG-recordings in humans. J Neurosci Meth 2008;167(1):105-14.
141. Wang W, Degenhart AD, Collinger JL, Vinjamuri R, Sudre GP, Adelson PD, et al. Human motor cortical activity recorded with Micro-ECoG electrodes, during individual finger movements. Conf Proc IEEE Eng Med Biol Soc 2009;2009:586-9.
142. Acharya S, Fifer MS, Benz HL, Crone NE, Thakor N. Electrocorticographic amplitude predicts finger positions during slow grasping motions of the hand. J Neural Eng 2010;7(4): 046002.
143. Kubánek J, Miller KJ, Ojemann JG, Wolpaw JR, Schalk G. Decoding flexion of individual fingers using electrocorticographic signals in humans. J Neural Eng 2009;6(6):066001.
144. Vinjamuri R,Weber DJ, Degenhart AD, Collinger JL, Sudre GP, Adelson PD, et al. A fuzzy logic model for hand posture control using human cortical activity recorded by micro-ECog electrodes. Conf Proc IEEE Eng Med Biol Soc 2009;2009:4339-42.
145. Pistohl T, Schulze-Bonhage A, Aertsen A, Mehring C, Ball T. Decoding natural grasp types from human ECoG. NeuroImage 2012;59(1):248-60.
146. Wang W, Collinger JL, Degenhart AD, Tyler-Kabara EC, Schwartz AB, Moran DW, et al. An electrocorticographic brain interface in an individual with tetraplegia. PloS one 2013;8(2): e55344.
147. Yanagisawa T, HirataM, Saitoh Y, Goto T, Kishima H, Fukuma R, et al. Real-time control of a prosthetic hand using human electrocorticography signals. J Neurosurg 2011;114(6):1715-22.
148. Hill NJ, Lal TN, Schröder M, Hinterberger T, Wilhelm B, Nijboer F, et al. Classifying EEG and ECoG signals without subject training for fast BCI implementation: comparison of nonparalyzed and completely paralyzed subjects. IEEE Trans Neural Sys Rehabil Eng 2006;14(2):183-6.
149. Chao ZC, Nagasaka Y, Fujii N. Long-term asynchronous decoding of arm motion using electrocorticographic signals in monkeys. Front Neuroeng 2010;3:3.
150. Ashmore RC, Endler BM, Smalianchuk I, Degenhart AD, Hatsopoulos NG, Tyler-Kabara EC, et al. Stable online control of an electrocorticographic brain-computer interface using a static decoder. Conf Proc IEEE Eng Med Biol Soc 2012; 2012;1740-44.
151. Schwartz AB, Cui XT, Weber DJ, Moran DW. Brain-controlled interfaces: movement restoration with neural prosthetics. Neuron 2006;52(1):205-20.
152. Hochberg L, Serruya M, Friehs G, Mukand J, Saleh M, Caplan A, et al. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 2006;442(7099):164-71.
153. Hochberg L, Bacher D, Jarosiewicz B, Masse NY, Simeral JD, Vogel J, et al. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 2012;485(7398):372-5.
154. Collinger JL, Wodlinger B, Downey JE, Wang W, Tyler-Kabara EC, Weber DJ, et al. High-performance neuroprosthetic control by an individual with tetraplegia. Lancet 2013;381(9866):557-64.
155. Velliste M, Perel S, Spalding MC, Whitford AS, Schwartz AB. Cortical control of a prosthetic arm for self-feeding. Nature 2008;453(7198):1098-101.
156. Taylor DM, Tillery SIH, Schwartz AB. Information conveyed through brain-control: cursor versus robot. IEEE Trans Neural Sys Rehabil Eng 2003;11(2):195-9.
157. Moritz CT, Perlmutter SI, Fetz EE. Direct control of paralysed muscles by cortical neurons. Nature 2008;456(7222):639-42.
158. Ethier C, Oby ER, Bauman MJ, Miller LE. Restoration of grasp following paralysis through brain-controlled stimulation of muscles. Nature 2012:1-4.
159. Simeral JD, Kim SP, Black MJ, Donoghue JP, Hochberg LR. Neural control of cursor trajectory and click by a human with tetraplegia 1000 days after implant of an intracortical microelectrode array. J Neural Eng 2011;8(2):25027.
160. Polikov VS, Tresco PA, Reichert WM. Response of brain tissue to chronically implanted neural electrodes. J Neurosci Meth 2005; 148(1):1-18.
161. Ludwig KA, Uram JD, Yang J, Martin DC, Kipke DR. Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film. J Neural Eng 2006;3(1):59-70.
162. Skousen JL, Merriam SME, Srivannavit O, Perlin G, Wise KD, Tresco PA. Reducing surface area while maintaining implant penetrating profile lowers the brain foreign body response to chronically implanted planar silicon microelectrode arrays. Prog Brain Res 2011;194:167-80.
163. Marin C, Fernández E. Biocompatibility of intracortical microelectrodes: current status and future prospects. Front Neuroeng 2010;3:8.
164. Green RA, Lovell NH, Wallace GG, Poole-Warren LA. Conducting polymers for neural interfaces: challenges in developing an effective long-term implant. Biomater 2008;29(24-25): 3393-9.
165. Jun SB, Hynd MR, Dowell-Mesfin NM, Al-Kofahi Y, Roysam B, Shain W, et al. Modulation of cultured neural networks using neurotrophin release from hydrogel-coated microelectrode arrays. J Neural Eng 2008;5(2):203-13.
166. Azemi E, Lagenaur CF, Cui XT. The surface immobilization of the neural adhesion molecule L1 on neural probes and its effect on neuronal density and gliosis at the probe/tissue interface. Biomater 2011;32(3):681-92.
167. Gilja V, Chestek CA, Diester I, Henderson JM, Deisseroth K, Shenoy KV. Challenges and opportunities for next-generation intracortically based neural prostheses. IEEE Trans Biomed Eng 2011;58(7):1891-9.
168. Harrison RR, Kier RJ, Chestek CA, Gilja V, Nuyujukian P, Ryu S, et al. Wireless neural recording with single low-power integrated circuit. IEEE Trans Neural Syst Rehabil Eng 2009;17(4): 322-9.
169. Nurmikko AV, Donoghue JP, Hochberg LR, Patterson WR, Song Y-K, BullCW, et al. Listening to brain microcircuits for interfacing with external world-progress in wireless implantable microelectronic neuroengineering devices: Experimental systems are described for electrical recording in the brain using multiple microelectrodes and short range implantable or wearable broadcase units. Proc IEEE Inst Electr Electron Eng 2010;98(3):375-88.
170. Rush A, Troyk PR. Dual inductive link coil design for a neural recording system. Conf Proc IEEE Eng Med Biol Soc 2011; 2011:6397-400.
171. Wenzel BJ, Boggs JW, Gustafson KJ, Grill WM. Detecting the onset of hyper-reflexive bladder contractions from the electrical activity of the pudendal nerve. IEEE Trans Neural Syst Rehabil Eng 2005;13(3):428-35.
172. Sinkjaer T, Haugland M, Inmann A, Hansen M, Nielsen KD. Biopotentials as command and feedback signals in functional electrical stimulation systems. Med Eng Phys 2003;25(1): 29-40.
173. Weber DJ, Stein RB, Everaert DG, Prochazka A. Limb-state feedback from ensembles of simultaneously recorded dorsal root ganglion neurons. J Neural Eng 2007;4(3):S168-80.
174. Umeda T, Seki K, Sato M-aki, Nishimura Y, Kawato M, Isa T. Population coding of forelimb joint kinematics by peripheral afferents in monkeys. Gribble PL, editor. PLoS ONE 2012; 7(10):e47749.
175. Bruns TM, Wagenaar JB, Bauman MJ, Gaunt RA, Weber DJ. Real-time control of hind limb functional electrical stimulation using feedback from dorsal root ganglia recordings. J Neural Eng 2013;10(2):026020.
176. Bruns TM, Gaunt RA, Weber DJ. Multielectrode array recordings of bladder and perineal primary afferent activity from the sacral dorsal root ganglia. J Neural Eng 2011;8(5):056010.
177. Gaunt RA, Bruns TM, Crammond D, Tomycz N, Moossy JJ, Weber DJ. Single-and multi-unit activity recorded from the surface of the dorsal root ganglia with non-penetrating electrode arrays. Conf Proc IEEE Eng Med Biol Soc 2011:6713-16.
178. Martin J, Martin L, Stumbo N, Morrill J. The impact of consumer involvement on satisfaction with and use of assistive technology. Disabil Rehabil 2011;6(3):225-42.