Skip to main content

Functional Electrical Stimulation Therapy: Mechanisms for Recovery of Function Following Spinal Cord Injury and Stroke

  • Chapter
  • First Online:
Neurorehabilitation Technology

Abstract

Electrical stimulation is a tool that applies low-energy electrical pulses to artificially generate muscle contractions. If electrical stimulation is used to enable functional movements, such as walking and grasping, then this intervention is called functional electrical stimulation (FES). When FES is used as therapy instead of being used as an orthosis, it is called FES therapy or FET. In this chapter, we introduce recent findings and advances in the field of FET. The findings to date clearly show that FET for reaching and grasping is a therapeutic modality that should be implemented in every rehabilitation institution that is treating individuals with stroke and Spinal Cord Injury (SCI). There is also considerable evidence to support the use of FET as a therapeutic modality to treat drop-foot problem in stroke and incomplete populations. Although phase I randomized control trials have been completed with chronic SCI population using this new FET technology and preliminary findings are encouraging, further research and development are required before the multichannel FET for walking will be ready for clinical implementation. Finally, emerging evidence for the beneficial use of brain-computer interface (BCI) combined with FET (BCI-FET) for improving upper and lower limb function will also be presented.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Loeb GE, Ghez C. The motor unit and muscle action. In: Kandel ER, et al., editors. Principles of Neural Science, Fourth Ed. p. 674–94.

    Google Scholar 

  2. Reichel M, Breyer T, Mayr W, Rattay F. Simulation of the three-dimensional electrical field in the course of functional electrical stimulation. Artif Organs. 2002;26:252–5.

    PubMed  Google Scholar 

  3. Kern H, Hofer C, Mödlin M, Forstner C, Raschka-Högler D, Mayr W, Stöhr H. Denervated muscles in humans: limitations and problems of currently used functional electrical stimulation training protocols. Artif Organs. 2002;26:216–8.

    PubMed  Google Scholar 

  4. Nakagawa K, Bergquist AJ, Yamashita T, Yoshida T, Masani K. Motor point stimulation primarily activates motor nerve. Neurosci Lett. 2020;736:135246.

    CAS  PubMed  Google Scholar 

  5. Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF. Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol. 2011;111:2409–26.

    CAS  PubMed  Google Scholar 

  6. Rushton DN. Functional electrical stimulation and rehabilitation—an hypothesis. Med Eng Phys. 2003;25:75–8.

    CAS  PubMed  Google Scholar 

  7. Bersch I, Koch-Borner S, Fridén J. Electrical stimulation-a mapping system for hand dysfunction in tetraplegia. Spinal Cord. 2018;56:516–22.

    PubMed  Google Scholar 

  8. Botter A, Oprandi G, Lanfranco F, Allasia S, Maffiuletti NA, Minetto MA. Atlas of the muscle motor points for the lower limb: implications for electrical stimulation procedures and electrode positioning. Eur J Appl Physiol. 2011;111:2461–71.

    PubMed  Google Scholar 

  9. Lim D, Del CM, Bergquist AJ, Milosevic M, Masani K. Contribution of each motor point of quadriceps femoris to knee extension torque during neuromuscular electrical stimulation. IEEE Trans Neural Syst Rehabil Eng. 2021;29:389–96.

    PubMed  Google Scholar 

  10. Garcia-Garcia MG, Jovanovic LI, Popovic MR. Comparing preference related to comfort in torque-matched muscle contractions between two different types of functional electrical stimulation pulses in able-bodied participants. J Spinal Cord Med. 2021;44:S215–24.

    PubMed  PubMed Central  Google Scholar 

  11. Mesin L, Merlo E, Merletti R, Orizio C. Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle. J Electromyogr Kinesiol. 2010;20:580–9.

    CAS  PubMed  Google Scholar 

  12. Doucet BM, Lam A, Griffin L. Neuromuscular electrical stimulation for skeletal muscle function. Yale J Biol Med. 2012;85:201.

    PubMed  PubMed Central  Google Scholar 

  13. Bergquist AJ, Babbar V, Ali S, Popovic MR, Masani K. Fatigue reduction during aggregated and distributed sequential stimulation. Muscle Nerve. 2017;56:271–81.

    PubMed  Google Scholar 

  14. Masani K, Popovic MR. Functional electrical stimulation in rehabilitation and neurorehabilitation. In: Springer handbook of medical technology. Berlin, Heidelberg: Springer; 2011. p. 877–96.

    Google Scholar 

  15. Barss TS, Ainsley EN, Claveria-Gonzalez FC, Luu MJ, Miller DJ, Wiest MJ, Collins DF. Utilizing physiological principles of motor unit recruitment to reduce fatigability of electrically-evoked contractions: a narrative review. Arch Phys Med Rehabil. 2018;99:779–91.

    PubMed  Google Scholar 

  16. Malešević NM, Popović LZ, Schwirtlich L, Popović DB. Distributed low-frequency functional electrical stimulation delays muscle fatigue compared to conventional stimulation. Muscle Nerve. 2010;42:556–62.

    PubMed  Google Scholar 

  17. Nguyen R, Masani K, Micera S, Morari M, Popovic MR. Spatially distributed sequential stimulation reduces fatigue in paralyzed triceps surae muscles: a case study. Artif Organs. 2011;35:1174–80.

    PubMed  Google Scholar 

  18. Sayenko DG, Nguyen R, Popovic MR, Masani K. Reducing muscle fatigue during transcutaneous neuromuscular electrical stimulation by spatially and sequentially distributing electrical stimulation sources. Eur J Appl Physiol. 2014;114:793.

    PubMed  PubMed Central  Google Scholar 

  19. Sayenko DG, Nguyen R, Hirabayashi T, Popovic MR, Masani K. Method to reduce muscle fatigue during transcutaneous neuromuscular electrical stimulation in major knee and ankle muscle groups. Neurorehabil Neural Repair. 2015;29:722–33.

    PubMed  Google Scholar 

  20. Ye G, Ali S, Bergquist AJ, Popovic MR, Masani K. A generic sequential stimulation adapter for reducing muscle fatigue during functional electrical stimulation. Sensors. 2021;21(21):7248.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Kuhn A, Keller T, Micera S, Morari M. Array electrode design for transcutaneous electrical stimulation: a simulation study. Med Eng Phys. 2009;31:945–51.

    PubMed  Google Scholar 

  22. Micera S, Keller T, Lawrence M, Morari M, Popovic D. Wearable neural prostheses. IEEE Eng Med Biol Mag. 2010;29:64–9.

    PubMed  Google Scholar 

  23. Popović DB, Popović MB. Automatic determination of the optimal shape of a surface electrode: Selective stimulation. J Neurosci Methods. 2009;178:174–81.

    PubMed  Google Scholar 

  24. Smith B, Tang Z, Johnson MW, Pourmehdi S, Gazdik MM, Buckett JR, Hunter Peckham P. An externally powered, multichannel, implantable stimulator-telemeter for control of paralyzed muscle. IEEE Trans Biomed Eng. 1998;45:463–75.

    CAS  PubMed  Google Scholar 

  25. Davis R, Sparrow O, Cosendai G, Burridge J, Turk R, Wulff C, Schulman J. Post-stroke arm rehabilitation using 5–7 implanted microstimulators: implantation procedures, safety and efficacy. Undefined; 2007.

    Google Scholar 

  26. Popovic MB, Popovic DB, Sinkjær T, Stefanovic A, Schwirtlich L. Restitution of reaching and grasping promoted by functional electrical therapy. Artif Organs. 2002;26:271–5.

    PubMed  Google Scholar 

  27. Waters RL. The enigma of “carry-Over.” Disabil Rehabil. 1984;6:9–12.

    CAS  Google Scholar 

  28. Merletti R, Acimovic R, Grobelnik S, Cvilak G. Electrophysiological orthosis for the upper extremity in hemiplegia: feasibility study. Arch Phys Med Rehabil. 1975;56:507–13.

    CAS  PubMed  Google Scholar 

  29. Thrasher TA, Zivanovic V, McIlroy W, Popovic MR. Rehabilitation of reaching and grasping function in severe hemiplegic patients using functional electrical stimulation therapy. Neurorehabil Neural Repair. 2008;22:706–14.

    PubMed  Google Scholar 

  30. Kapadia NM, Zivanovic V, Furlan J, Craven BC, Mcgillivray C, Popovic MR. Functional electrical stimulation therapy for grasping in traumatic incomplete spinal cord injury: randomized control trial. Artif Organs. 2011;35:212–6.

    PubMed  Google Scholar 

  31. Goulet C, Arsenault AB, Bourbonnais D, Laramée MT, Lepage Y. Effects of transcutaneous electrical nerve stimulation on H-reflex and spinal spasticity. Scand J Rehabil Med. 1996;28:169–76.

    CAS  PubMed  Google Scholar 

  32. Kawashima N, Popovic MR, Zivanovic V. Effect of intensive functional electrical stimulation therapy on upper-limb motor recovery after stroke: case study of a patient with chronic stroke. Physiother Canada. 2013;65:20.

    Google Scholar 

  33. Milosevic M, Masugi Y, Obata H, Sasaki A, Popovic MR, Nakazawa K. Short-term inhibition of spinal reflexes in multiple lower limb muscles after neuromuscular electrical stimulation of ankle plantar flexors. Exp Brain Res. 2019;237:467–76.

    PubMed  Google Scholar 

  34. Shin HK, Cho SH, Jeon HS, Lee YH, Song JC, Jang SH, Lee CH, Kwon YH. Cortical effect and functional recovery by the electromyography-triggered neuromuscular stimulation in chronic stroke patients. Neurosci Lett. 2008;442:174–9.

    CAS  PubMed  Google Scholar 

  35. Sasaki K, Matsunaga T, Tomite T, Yoshikawa T, Shimada Y. Effect of electrical stimulation therapy on upper extremity functional recovery and cerebral cortical changes in patients with chronic hemiplegia. Biomed Res. 2012;33:89–96.

    CAS  PubMed  Google Scholar 

  36. Milosevic M, Nakanishi T, Sasaki A, Yamaguchi A, Nomura T, Popovic MR, Nakazawa K. Cortical re-organization after traumatic brain injury elicited using functional electrical stimulation therapy: a case report. Front Neurosci. 2021;15:1046.

    Google Scholar 

  37. Popovic MR, Popovic DB, Keller T. Neuroprostheses for grasping. Neurol Res. 2002;24:443–52.

    PubMed  Google Scholar 

  38. Kapadia N, Moineau B, Popovic MR. Functional electrical stimulation therapy for retraining reaching and grasping after spinal cord injury and stroke. Front Neurosci. 2020;14:718.

    PubMed  PubMed Central  Google Scholar 

  39. Taylor PN, Burridge JH, Dunkerley AL, Wood DE, Norton JA, Singleton C, Swain ID. Clinical use of the odstock dropped foot stimulator: its effect on the speed and effort of walking. Arch Phys Med Rehabil. 1999;80:1577–83.

    CAS  PubMed  Google Scholar 

  40. Stein RB, Everaert DG, Thompson AK, Chong SL, Whittaker M, Robertson J, Kuether G. Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabil Neural Repair. 2010;24:152–67.

    PubMed  Google Scholar 

  41. Hausdorff JM, Ring H. Effects of a new radio frequency-controlled neuroprosthesis on gait symmetry and rhythmicity in patients with chronic hemiparesis. Am J Phys Med Rehabil. 2008;87:4–13.

    PubMed  Google Scholar 

  42. Burridge JH, Haugland M, Larsen B, Svaneborg N, Iversen HK, Christensen PB, Pickering RM, Sinkjaer T. Patients’ perceptions of the benefits and problems of using the actigait implanted drop-foot stimulator. J Rehabil Med. 2008;40:873–5.

    PubMed  Google Scholar 

  43. Kenney L, Bultstra G, Buschman R, et al. An implantable two channel drop foot stimulator: initial clinical results. Artif Organs. 2002;26:267–70.

    PubMed  Google Scholar 

  44. Van Swigchem R, Vloothuis J, Den Boer J, Weerdesteyn V, Geurts ACH. Is transcutaneous peroneal stimulation beneficial to patients with chronic stroke using an ankle-foot orthosis? A within-subjects study of patients’ satisfaction, walking speed and physical activity level. J Rehabil Med. 2010;42:117–21.

    PubMed  Google Scholar 

  45. Daly JJ, Roenigk K, Holcomb J, Rogers JM, Butler K, Gansen J, McCabe J, Fredrickson E, Marsolais EB, Ruff RL. A randomized controlled trial of functional neuromuscular stimulation in chronic stroke subjects. Stroke. 2006;37:172–8.

    PubMed  Google Scholar 

  46. Burridge JH, Taylor PN, Hagan SA, Wood DE, Swain ID. The effects of common peroneal stimulation on the effort and speed of walking: A randomized controlled trial with chronic hemiplegic patients. Clin Rehabil. 1997;11:201–10.

    CAS  PubMed  Google Scholar 

  47. Granat MH, Maxwell DJ, Ferguson ACB, Lees KR, Barbenel JC. Peroneal stimulator; evaluation for the correction of spastic drop foot in hemiplegia. Arch Phys Med Rehabil. 1996;77:19–24.

    CAS  PubMed  Google Scholar 

  48. Kantrowitz A. Electronic physiological aids: a report of the maimonides Hospital. Maimonides Hospital, Brooklyn; 1960.

    Google Scholar 

  49. Strojnik P, Kralj A, UrŠIČ I. Programmed six-channel electrical stimulator for complex stimulation of leg muscles during walking. IEEE Trans Biomed Eng BME. 1979;26:112–6.

    Google Scholar 

  50. Kralj A, Bajd T, Turk R. Enhancement of gait restoration in spinal injured patients by functional electrical stimulation. Clin Orthop Relat Res. 1988;233:34–43.

    Google Scholar 

  51. Graupe D, Kohn KH. Functional neuromuscular stimulator for short-distance ambulation by certain thoracic-level spinal-cord-injured paraplegics. Surg Neurol. 1998;50:202–7.

    CAS  PubMed  Google Scholar 

  52. Graupe D, Davis R, Kordylewski H, Kohn KH. Ambulation by traumatic T4–12 paraplegics using functional neuromuscular stimulation. Crit Rev Neurosurg. 1998;8:221–31.

    CAS  PubMed  Google Scholar 

  53. Popovic D, Tomovic R, Schwirtlich L. Hybrid assistive system - the motor neuroprosthesis. IEEE Trans Biomed Eng. 1989;36:729–37.

    CAS  PubMed  Google Scholar 

  54. Solomonow M, Baratta R, Hirokawa S, Rightor N, Walker W, Beaudette P, Shoji H, D’Ambrosia R. The RGO generation II: muscle stimulation powered orthosis as a practical walking system for thoracic paraplegics. Orthopedics. 1989;12:1309–15.

    CAS  PubMed  Google Scholar 

  55. Bailey SN, Hardin EC, Kobetic R, Boggs LM, Pinault G, Triolo RJ. Neurotherapeutic and neuroprosthetic effects of implanted functional electrical stimulation for ambulation after incomplete spinal cord injury. J Rehabil Res Dev. 2010;47:7–16.

    PubMed  Google Scholar 

  56. Davis JA, Triolo RJ, Uhlir JP, Bhadra N, Lissy DA, Nandurkar S, Marsolais EB. Surgical technique for installing an eight-channel neuroprosthesis for standing. Clin Orthop Relat Res. 2001;237–52.

    Google Scholar 

  57. Davis JA, Triolo RJ, Uhlir J, Bieri C, Rohde L, Lissy D, Kukke S. Preliminary performance of a surgically implanted neuroprosthesis for standing and transfers--where do we stand? J Rehabil Res Dev. 38:609–17.

    Google Scholar 

  58. Hardin E, Kobetic R, Murray L, Corado-Ahmed M, Pinault G, Sakai J, Bailey SN, Ho C, Triolo RJ. Walking after incomplete spinal cord injury using an implanted FES system: a case report. J Rehabil Res Dev. 2007;44:333–46.

    PubMed  Google Scholar 

  59. Johnston TE, Betz RR, Smith BT, Benda BJ, Mulcahey MJ, Davis R, Houdayer TP, Pontari MA, Barriskill A, Creasey GH. Implantable FES system for upright mobility and bladder and bowel function for individuals with spinal cord injury. Spinal Cord. 2005;43:713–23.

    CAS  PubMed  Google Scholar 

  60. Popovic MR, Keller T. Modular transcutaneous functional electrical stimulation system. Med Eng Phys. 2005;27:81–92.

    PubMed  Google Scholar 

  61. Thrasher TA, Flett HM, Popovic MR. Gait training regimen for incomplete spinal cord injury using functional electrical stimulation. Spinal Cord. 2006;44:357–61.

    CAS  PubMed  Google Scholar 

  62. Pappas IPI, Popovic MR, Keller T, Dietz V, Morari M. A reliable gait phase detection system. IEEE Trans Neural Syst Rehabil Eng. 2001;9:113–25.

    CAS  PubMed  Google Scholar 

  63. Bajd T, Kralj A, Štefančič M, Lavrač N. Use of functional electrical stimulation in the lower extremities of incomplete spinal cord injured patients. Artif Organs. 1999;23:403–9.

    CAS  PubMed  Google Scholar 

  64. Wieler M, Stein RB, Ladouceur M, Whittaker M, Smith AW, Naaman S, Barbeau H, Bugaresti J, Aimone E. Multicenter evaluation of electrical stimulation systems for walking. Arch Phys Med Rehabil. 1999;80:495–500.

    CAS  PubMed  Google Scholar 

  65. Field-Fote EC, Lindley SD, Sherman AL. Locomotor training approaches for individuals with spinal cord injury: a preliminary report of walking-related outcomes. J Neurol Phys Ther. 2005;29:127–37.

    PubMed  Google Scholar 

  66. Field-Fote EC, Roach KE. Influence of a locomotor training approach on walking speed and distance in people with chronic spinal cord injury: a randomized clinical trial. Phys Ther. 2011;91:48.

    PubMed  PubMed Central  Google Scholar 

  67. Giangregorio L, Craven C, Richards K, Kapadia N, Hitzig SL, Masani K, Popovic MR. A randomized trial of functional electrical stimulation for walking in incomplete spinal cord injury: effects on body composition. J Spinal Cord Med. 2012;35:351.

    PubMed  PubMed Central  Google Scholar 

  68. Hitzig SL, Craven BC, Panjwani A, Kapadia N, Giangregorio LM, Richards K, Masani K, Popovic MR. Randomized trial of functional electrical stimulation therapy for walking in incomplete spinal cord injury: effects on quality of life and community participation. Top Spinal Cord Inj Rehabil. 2013;19:245–58.

    PubMed  PubMed Central  Google Scholar 

  69. Kapadia N, Masani K, Craven BC, Giangregorio LM, Hitzig SL, Richards K, Popovic MR. A randomized trial of functional electrical stimulation for walking in incomplete spinal cord injury: effects on walking competency. J Spinal Cord Med. 2014;37:511.

    PubMed  PubMed Central  Google Scholar 

  70. Chae J, Bethoux F, Bohinc T, Dobos L, Davis T, Friedl A. Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia. Stroke. 1998;29:975–9.

    CAS  PubMed  Google Scholar 

  71. Chae J, Harley MY, Hisel TZ, Corrigan CM, Demchak JA, Wong YT, Fang ZP. Intramuscular electrical stimulation for upper limb recovery in chronic hemiparesis: an exploratory randomized clinical trial. Neurorehabil Neural Repair. 2009;23:569–78.

    PubMed  Google Scholar 

  72. Chae J, Hart R. Intramuscular hand neuroprosthesis for chronic stroke survivors. Neurorehabil Neural Repair. 2003;17:109–17.

    PubMed  Google Scholar 

  73. Francisco G, Chae J, Chawla H, Kirshblum S, Zorowitz R, Lewis G, Pang S. Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute stroke survivors: a randomized pilot study. Arch Phys Med Rehabil. 1998;79:570–5.

    CAS  PubMed  Google Scholar 

  74. Handricks HT, IJzerman MJ, deKroon JR, Zilvold G. Functional electrical stimulation by means of the “Ness Handmaster Orthosis” in chronic stroke patients: an exploratory study. Clin Rehabil. 2001;15:217–20.

    Google Scholar 

  75. Kowalczewski J, Gritsenko V, Ashworth N, Ellaway P, Prochazka A. Upper-extremity functional electric stimulation-assisted exercises on a workstation in the subacute phase of stroke recovery. Arch Phys Med Rehabil. 2007;88:833–9.

    PubMed  Google Scholar 

  76. Sullivan JE, Hedman LD. Effects of home-based sensory and motor amplitude electrical stimulation on arm dysfunction in chronic stroke. Clin Rehabil. 2007;21:142–50.

    PubMed  Google Scholar 

  77. Sullivan JE, Hedman LD. A home program of sensory and neuromuscular electrical stimulation with upper-limb task practice in a patient 5 years after a stroke. Phys Ther. 2004;84:1045–54.

    PubMed  Google Scholar 

  78. Popovic DB, Popovic MB, Sinkjær T, Stefanovic A, Schwirtlich L. Therapy of paretic arm in hemiplegic subjects augmented with a neural prosthesis: a cross-over study. Can J Physiol Pharmacol. 2004;82:749–56.

    CAS  PubMed  Google Scholar 

  79. Popović D, Stojanović A, Pjanović A, Radosavljević S, Popović M, Jović S, Vulović D. Clinical evaluation of the bionic glove. Arch Phys Med Rehabil. 1999;80:299–304.

    PubMed  Google Scholar 

  80. 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;78:608–14.

    CAS  PubMed  Google Scholar 

  81. Rebersek S, Vodovnik L. Proportionally controlled functional electrical stimulation of hand. Arch Phys Med Rehabil. 1973;54:378–82.

    CAS  PubMed  Google Scholar 

  82. Popovic MR, Thrasher TA, Zivanovic V, Takaki J, Hajek V. Neuroprosthesis for retraining reaching and grasping functions in severe hemiplegic patients. Neuromodulation. 2005;8:58–72.

    PubMed  Google Scholar 

  83. Gritsenko V, Prochazka A. A functional electric stimulation-assisted exercise therapy system for hemiplegic hand function. Arch Phys Med Rehabil. 2004;85:881–5.

    PubMed  Google Scholar 

  84. Popovic MR, Keller T, Pappas IPI, Dietz V, Morari M. Surface-stimulation technology for grasping and walking neuroprostheses: Improving quality of life in stroke/spinal cord injury subjects with rapid prototyping and portable FES systems. IEEE Eng Med Biol Mag. 2001;20:82–93.

    CAS  PubMed  Google Scholar 

  85. Popovic MR, Curt A, Keller T, Dietz V. Functional electrical stimulation for grasping and walking: indications and limitations. Spinal Cord. 2001;39:403–12.

    CAS  PubMed  Google Scholar 

  86. Popović MB. Control of neural prostheses for grasping and reaching. Med Eng Phys. 2003;25:41–50.

    PubMed  Google Scholar 

  87. Anderson KD, Wilson JR, Korupolu R, Pierce J, Bowen JM, O’Reilly D, Kapadia N, Popovic MR, Thabane L, Musselman KE. Multicentre, single-blind randomised controlled trial comparing MyndMove neuromodulation therapy with conventional therapy in traumatic spinal cord injury: a protocol study. BMJ Open. 2020;10:e039650.

    PubMed  PubMed Central  Google Scholar 

  88. Glanz M, Klawansky S, Stason W, Berkey C, Chalmers TC. Functional electrostimulation in poststroke rehabilitation: a meta-analysis of the randomized controlled trials. Arch Phys Med Rehabil. 1996;77:549–53.

    CAS  PubMed  Google Scholar 

  89. Cauraugh JH, Kim S. Two coupled motor recovery protocols are better than one: electromyogram-triggered neuromuscular stimulation and bilateral movements. Stroke. 2002;33:1589–94.

    PubMed  Google Scholar 

  90. Ring H, Rosenthal N. Controlled study of neuroprosthetic functional electrical stimulation in sub-acute post-stroke rehabilitation. J Rehabil Med. 2005;37:32–6.

    PubMed  Google Scholar 

  91. Hebert DA, Bowen JM, Ho C, Antunes I, O’Reilly DJ, Bayley M. Examining a new functional electrical stimulation therapy with people with severe upper extremity hemiparesis and chronic stroke: a feasibility study. Br J Occup Ther. 2017;80:651–9.

    Google Scholar 

  92. Kapadia NM, Nagai MK, Zivanovic V, Bernstein J, Woodhouse J, Rumney P, Popovic MR. Functional electrical stimulation therapy for recovery of reaching and grasping in severe chronic pediatric stroke patients. J Child Neurol. 2014;29:493–9.

    PubMed  Google Scholar 

  93. Popovic MR, Thrasher TA. Neuroprostheses, encyclopedia of biomaterials and biomedical engineering. New York: Marcel Dekker Inc.; 2004.

    Google Scholar 

  94. Mangold S, Keller T, Curt A, Dietz V. Transcutaneous functional electrical stimulation for grasping in subjects with cervical spinal cord injury. Spinal Cord. 2005;43:1–13.

    CAS  PubMed  Google Scholar 

  95. Popovic MR, Thrasher TA, Adams ME, Takes V, Zivanovic V, Tonack MI. Functional electrical therapy: retraining grasping in spinal cord injury. Spinal Cord. 2006;44:143–51.

    CAS  PubMed  Google Scholar 

  96. Kapadia N, Zivanovic V, Popovic MR. Restoring voluntary grasping function in individuals with incomplete chronic spinal cord injury: pilot study. Top Spinal Cord Inj Rehabil. 2013;19:279.

    PubMed  PubMed Central  Google Scholar 

  97. Kapadia NM, Bagher S, Popovic MR. Influence of different rehabilitation therapy models on patient outcomes: hand function therapy in individuals with incomplete SCI. 2014;37:734–43. https://doi.org/10.1179/2045772314Y0000000203.

  98. Tomovic R, Popovic DB, Stein RB. Nonanalytical methods for motor control; 1995. https://doi.org/10.1142/2594.

  99. Andrews BJ, Baxendale RH, Barnett R, Phillips GF, Yamazaki T, Paul JP, Freeman PA. Hybrid FES orthosis incorporating closed loop control and sensory feedback. J Biomed Eng. 1988;10:189–95.

    CAS  PubMed  Google Scholar 

  100. Solomonow M. Biomechanics and physiology of a practical powered walking orthosis for paraplegics. In: Stein RB, Peckham P, Popovic D, editors. Neural prostheses: replacing motor function after disease or disability. London: Oxford University Press; 1992.

    Google Scholar 

  101. Takeoka A, Vollenweider I, Courtine G, Arber S. Muscle spindle feedback directs locomotor recovery and circuit reorganization after spinal cord injury. Cell. 2014;159:1626–39.

    CAS  PubMed  Google Scholar 

  102. Freeman CT, Hughes AM, Burridge JH, Chappell PH, Lewin PL, Rogers E. Iterative learning control of FES applied to the upper extremity for rehabilitation. Control Eng Pract. 2009;17:368–81.

    Google Scholar 

  103. Stauffer Y, Allemand Y, Bouri M, Fournier J, Clavel R, Metrailler P, Brodard R, Reynard F. The WalkTrainer - a new generation of walking reeducation device combining orthoses and muscle stimulation. IEEE Trans Neural Syst Rehabil Eng. 2009;17:38–45.

    CAS  PubMed  Google Scholar 

  104. Crema A, Mancuso M, Frisoli A, Salsedo F, Raschellà F, Micera S. A hybrid NMES-exoskeleton for real objects interaction. In: International IEEE/EMBS conference on neural engineering NER 2015 July; 2015. p. 663–666.

    Google Scholar 

  105. Bergamasco M. An exoskeleton structure for physical interaction with a human being; 2013.

    Google Scholar 

  106. Hesse S, Werner C, Pohl M, Rueckriem S, Mehrholz J, Lingnau ML. Computerized arm training improves the motor control of the severely affected arm after stroke: a single-blinded randomized trial in two centers. Stroke. 2005;36:1960–6.

    CAS  PubMed  Google Scholar 

  107. Bouton CE, Shaikhouni A, Annetta NV, et al. Restoring cortical control of functional movement in a human with quadriplegia. Nature. 2016;533(7602):247–50.

    CAS  PubMed  Google Scholar 

  108. Ajiboye AB, Willett FR, Young DR, et al. Restoration of reaching and grasping movements through brain-controlled muscle stimulation in a person with tetraplegia: a proof-of-concept demonstration. Lancet. 2017;389:1821–30.

    PubMed  PubMed Central  Google Scholar 

  109. Takemi M, Masakado Y, Liu M, Ushiba J. Event-related desynchronization reflects downregulation of intracortical inhibition in human primary motor cortex. J Neurophysiol. 2013;110:1158–66.

    PubMed  Google Scholar 

  110. Marquez-Chin C, Marquis A, Popovic MR. EEG-triggered functional electrical stimulation therapy for restoring upper limb function in chronic stroke with severe hemiplegia. Case Rep Neurol Med. 2016;2016:1–11.

    Google Scholar 

  111. Jovanovic LI, Kapadia N, Zivanovic V, Rademeyer HJ, Alavinia M, McGillivray C, Kalsi-Ryan S, Popovic MR, Marquez-Chin C. Brain–computer interface-triggered functional electrical stimulation therapy for rehabilitation of reaching and grasping after spinal cord injury: a feasibility study. Spinal Cord Ser Cases. 2021;71(7):1–11.

    Google Scholar 

  112. Suzuki Y, Jovanovic LI, Fadli RA, Yamanouchi Y, Marquez-Chin C, Popovic MR, Nomura T, Milosevic M. Evidence that brain-controlled functional electrical stimulation could elicit targeted corticospinal facilitation of hand muscles in healthy young adults. Neuromodulation Technol. Neural Interface [In press]. 2021.

    Google Scholar 

  113. Suzuki Y, Kaneko N, Sasaki A, Tanaka F, Nakazawa K, Nomura T, Milosevic M. Muscle-specific movement-phase-dependent modulation of corticospinal excitability during upper-limb motor execution and motor imagery combined with virtual action observation. Neurosci Lett. 2021;755: 135907.

    CAS  PubMed  Google Scholar 

  114. Osuagwu BCA, Wallace L, Fraser M, Vuckovic A. Rehabilitation of hand in subacute tetraplegic patients based on brain computer interface and functional electrical stimulation: a randomised pilot study. J Neural Eng. 2016. https://doi.org/10.1088/1741-2560/13/6/065002.

    Article  PubMed  Google Scholar 

  115. Biasiucci A, Leeb R, Iturrate I, et al. (2018) Brain-actuated functional electrical stimulation elicits lasting arm motor recovery after stroke. Nat Commun. 2018;91(9):1–13.

    Google Scholar 

  116. Daly JJ, Cheng R, Rogers J, Litinas K, Hrovat K, Dohring M. Feasibility of a new application of noninvasive Brain Computer Interface (BCI): a case study of training for recovery of volitional motor control after stroke. J Neurol Phys Ther. 2009;33:203–11.

    PubMed  Google Scholar 

  117. Mukaino M, Ono T, Shindo K, Fujiwara T, Ota T, Kimura A, Liu M, Ushiba J. Efficacy of brain-computer interface-driven neuromuscular electrical stimulation for chronic paresis after stroke. J Rehabil Med. 2014;46:378–82.

    PubMed  Google Scholar 

  118. Jovanovic LI, Kapadia N, Lo L, Zivanovic V, Popovic MR, Marquez-Chin C. Restoration of upper limb function after chronic severe hemiplegia: a case report on the feasibility of a brain-computer interface-triggered functional electrical stimulation therapy. Am J Phys Med Rehabil. 2020;99:e35–40.

    PubMed  Google Scholar 

  119. McCrimmon CM, King CE, Wang PT, Cramer SC, Nenadic Z, Do AH. Brain-controlled functional electrical stimulation for lower-limb motor recovery in stroke survivors. In: Annual international conference of the IEEE engineering in medicine and biology society. IEEE engineering in medicine and biology society annual international conference 2014; 2014. p.1247–50.

    Google Scholar 

  120. Li M, Liu Y, Wu Y, Liu S, Jia J, Zhang L. Neurophysiological substrates of stroke patients with motor imagery-based Brain-Computer Interface training. Int J Neurosci. 2014;124:403–15.

    CAS  PubMed  Google Scholar 

  121. Kim T, Kim S, Lee B. Effects of action observational training plus brain-computer interface-based functional electrical stimulation on paretic arm motor recovery in patient with stroke: a randomized controlled trial. Occup Ther Int. 2016;23:39–47.

    PubMed  Google Scholar 

  122. McCrimmon CM, King CE, Wang PT, Cramer SC, Nenadic Z, Do AH. Brain-controlled functional electrical stimulation therapy for gait rehabilitation after stroke: a safety study. J Neuroeng Rehabil. 2015. https://doi.org/10.1186/S12984-015-0050-4.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Chung EJ, Park SI, Jang YY, Lee BH. Effects of brain-computer interface-based functional electrical stimulation on balance and gait function in patients with stroke: preliminary results. J Phys Ther Sci. 2015;27:513.

    PubMed  PubMed Central  Google Scholar 

  124. Mrachacz-Kersting N, Stevenson AJT, Jørgensen HRM, Severinsen KE, Aliakbaryhosseinabadi S, Jiang N, Farina D. Brain state-dependent stimulation boosts functional recovery following stroke. Ann Neurol. 2019;85:84–95.

    PubMed  Google Scholar 

  125. King CE, Wang PT, McCrimmon CM, Chou CC, Do AH, Nenadic Z. The feasibility of a brain-computer interface functional electrical stimulation system for the restoration of overground walking after paraplegia. J Neuroeng Rehabil. 2015;12:1–11.

    Google Scholar 

  126. Granat MH, Ferguson ACB, Andrews BJ, Delargy M. The role of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injury–observed benefits during gait studies. Paraplegia. 1993;31:207–15.

    CAS  PubMed  Google Scholar 

  127. Willer C, Ramsay SC, Wise RJS, Friston KJ, Frackwiak RSJ. Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction. Ann Neurol. 1993;33:181–9.

    Google Scholar 

  128. Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD. Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp brain Res. 2000;131:135–43.

    CAS  PubMed  Google Scholar 

  129. Milosevic M, Marquez-Chin C, Masani K, Hirata M, Nomura T, Popovic MR, Nakazawa K. Why brain-controlled neuroprosthetics matter: mechanisms underlying electrical stimulation of muscles and nerves in rehabilitation. Biomed Eng Online. 2020. https://doi.org/10.1186/s12938-020-00824-w.

    Article  PubMed  PubMed Central  Google Scholar 

  130. Carson RG, Buick AR. Neuromuscular electrical stimulation-promoted plasticity of the human brain. J Physiol. 2021;599:2375–99.

    CAS  PubMed  Google Scholar 

  131. Insausti-Delgado A, López-Larraz E, Omedes J, Ramos-Murguialday A. Intensity and dose of neuromuscular electrical stimulation influence sensorimotor cortical excitability. Front Neurosci. 2021. https://doi.org/10.3389/FNINS.2020.593360.

    Article  PubMed  PubMed Central  Google Scholar 

  132. Arendsen LJ, Guggenberger R, Zimmer M, Weigl T, Gharabaghi A. Peripheral electrical stimulation modulates cortical beta-band activity. Front Neurosci. 2021. https://doi.org/10.3389/FNINS.2021.632234.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Blickenstorfer A, Kleiser R, Keller T, Keisker B, Meyer M, Riener R, Kollias S. Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI. Hum Brain Mapp. 2009;30:963–75.

    PubMed  Google Scholar 

  134. Chae J, Yu D. Neuromuscular stimulation for motor relearning in hemiplegia. Crit Rev Phys Rehabil Med. 1999;11:22.

    Google Scholar 

  135. Gregory CM, Bickel CS. Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther. 2005;85:358–64.

    PubMed  Google Scholar 

  136. Prochazka A. Sensory control of normal movement and of movement aided by neural prostheses. J Anat. 2015;227:167–77.

    PubMed  PubMed Central  Google Scholar 

  137. Suppa A, Quartarone A, Siebner H, Chen R, Di Lazzaro V, Del Giudice P, Paulus W, Rothwell JC, Ziemann U, Classen J. The associative brain at work: evidence from paired associative stimulation studies in humans. Clin Neurophysiol. 2017;128:2140–64.

    CAS  PubMed  Google Scholar 

  138. Bunday KL, Perez MA. Motor recovery after spinal cord injury enhanced by strengthening corticospinal synaptic transmission. Curr Biol. 2012;22:2355–61.

    CAS  PubMed  PubMed Central  Google Scholar 

  139. Taylor JL, Martin PG. Voluntary motor output is altered by spike-timing-dependent changes in the human corticospinal pathway. J Neurosci. 2009;29:11708–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  140. McGie SC, Masani K, Popovic MR. Failure of spinal paired associative stimulation to induce neuroplasticity in the human corticospinal tract. J Spinal Cord Med. 2014;37:565–74.

    PubMed  PubMed Central  Google Scholar 

  141. Popovic MR, Kapadia N, Zivanovic V, Furlan JC, Craven BC, McGillivray C. Functional electrical stimulation therapy of voluntary grasping versus only conventional rehabilitation for patients with sub-acute incomplete tetraplegia: a randomized clinical trial. Neurorehabil Neural Repair. 2011;25:433–42.

    PubMed  Google Scholar 

  142. Kawai R, Markman T, Poddar R, Ko R, Fantana AL, Dhawale AK, Kampff AR, Ölveczky BP. Motor cortex is required for learning but not for executing a motor skill. Neuron. 2015;86:800–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Mrachacz-Kersting N, Ibáñez J, Farina D. Towards a mechanistic approach for the development of non-invasive brain-computer interfaces for motor rehabilitation. J Physiol. 2021;599:2361–74.

    CAS  PubMed  Google Scholar 

  144. Kato K, Sawada M, Nishimura Y. Bypassing stroke-damaged neural pathways via a neural interface induces targeted cortical adaptation. Nat Commun. 2019;101(10):1–13.

    Google Scholar 

  145. Nudo RJ. Recovery after brain injury: mechanisms and principles. Front Hum Neurosci. 2013;7:887.

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Milos R. Popovic .

Editor information

Editors and Affiliations

Ethics declarations

M.R.P. is a shareholder and director in the company MyndTec Inc. M.M. is an Executive Board Member of the International Functional Electrical Stimulation Society (IFESS), a non-profit organization dedicated to promoting the awareness, knowledge, and understanding of electrical stimulation technologies and their applications.

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Popovic, M.R., Masani, K., Milosevic, M. (2022). Functional Electrical Stimulation Therapy: Mechanisms for Recovery of Function Following Spinal Cord Injury and Stroke. In: Reinkensmeyer, D.J., Marchal-Crespo, L., Dietz, V. (eds) Neurorehabilitation Technology. Springer, Cham. https://doi.org/10.1007/978-3-031-08995-4_19

Download citation

  • DOI: https://doi.org/10.1007/978-3-031-08995-4_19

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-031-08994-7

  • Online ISBN: 978-3-031-08995-4

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics