New functional electrical stimulation approaches to standing and walking

Spinal cord injury (SCI) is a devastating neurological trauma that is prevalent predominantly in young individuals. Several interventions in the areas of neuroregeneration, pharmacology and rehabilitation engineering/neuroscience are currently under investigation for restoring function after SCI. In this paper, we focus on the use of neuroprosthetic devices for restoring standing and ambulation as well as improving general health and wellness after SCI. Four neuroprosthetic approaches are discussed along with their demonstrated advantages and their future needs for improved clinical applicability. We first introduce surface functional electrical stimulation (FES) devices for restoring ambulation and highlight the importance of these devices for facilitating exercise activities and systemic physiological activation. Implanted muscle-based FES devices for restoring standing and walking that are currently undergoing clinical trials are then presented. The use of implanted peripheral nerve intraneural arrays of multi-site microelectrodes for providing fine and graded control of force during sit-to-stand maneuvers is subsequently demonstrated. Finally, intraspinal microstimulation (ISMS) of the lumbosacral spinal cord for restoring standing and walking is introduced and its results to date are presented. We conclude with a general discussion of the common needs of the neuroprosthetic devices presented in this paper and the improvements that may be incorporated in the future to advance their clinical utility and user satisfaction.

[1]  Warren M. Grill,et al.  Selective Microstimulation of Central Nervous System Neurons , 2000, Annals of Biomedical Engineering.

[2]  Ronald J Triolo,et al.  Long-term user perceptions of an implanted neuroprosthesis for exercise, standing, and transfers after spinal cord injury. , 2003, Journal of rehabilitation research and development.

[3]  R. Triolo,et al.  Preliminary performance of a surgically implanted neuroprosthesis for standing and transfers--where do we stand? , 2001, Journal of rehabilitation research and development.

[4]  O Kiehn,et al.  Distribution of Networks Generating and Coordinating Locomotor Activity in the Neonatal Rat Spinal Cord In Vitro: A Lesion Study , 1996, The Journal of Neuroscience.

[5]  Dennis D. Roscoe,et al.  An Externally Powered, Multichannel, Implantable Stimulator for Versatile Control of Paralyzed Muscle , 1987, IEEE Transactions on Biomedical Engineering.

[6]  S Grillner,et al.  Central pattern generators for locomotion, with special reference to vertebrates. , 1985, Annual review of neuroscience.

[7]  V. Vanderhorst,et al.  Organization of lumbosacral motoneuronal cell groups innervating hindlimb, pelvic floor, and axial muscles in the cat , 1997, The Journal of comparative neurology.

[8]  Liberson Wt,et al.  Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. , 1961, Archives of physical medicine and rehabilitation.

[9]  P. Jacobs,et al.  Peak exercise capacity of electrically induced ambulation in persons with paraplegia. , 2002, Medicine and science in sports and exercise.

[10]  V. Mushahwar,et al.  Selective activation of muscle groups in the feline hindlimb through electrical microstimulation of the ventral lumbo-sacral spinal cord. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[11]  V. Mushahwar,et al.  Proposed specifications for a lumbar spinal cord electrode array for control of lower extremities in paraplegia. , 1997, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[12]  A. Prochazka,et al.  Spinal Cord Microstimulation Generates Functional Limb Movements in Chronically Implanted Cats , 2000, Experimental Neurology.

[13]  K. Klose,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. , 1997, Archives of physical medicine and rehabilitation.

[14]  N Bhadra,et al.  Surgical technique for installing an eight-channel neuroprosthesis for standing. , 2001, Clinical orthopaedics and related research.

[15]  K J Klose,et al.  Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 2. Effects on physiological responses to peak arm ergometry. , 1997, Archives of physical medicine and rehabilitation.

[16]  Anirban Dutta,et al.  Ambulation After Incomplete Spinal Cord Injury With EMG-Triggered Functional Electrical Stimulation , 2008, IEEE Transactions on Biomedical Engineering.

[17]  W. Mayr,et al.  Technology and long-term application of an epineural electrode. , 1989, ASAIO transactions.

[18]  Intraoperative Testing of Selectivity of Spiral Nerve Cuff Electrodes , 2005, Conference Proceedings. 2nd International IEEE EMBS Conference on Neural Engineering, 2005..

[19]  P. Peckham,et al.  Functional electrical stimulation for neuromuscular applications. , 2005, Annual review of biomedical engineering.

[20]  K. Klose,et al.  Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 3. Lack of effect on bone mineral density. , 1997, Archives of physical medicine and rehabilitation.

[21]  V. Mushahwar,et al.  Intraspinal microstimulation preferentially recruits fatigue‐resistant muscle fibres and generates gradual force in rat , 2005, The Journal of physiology.

[22]  T. Nichols,et al.  Distribution of heterogenic reflexes among the quadriceps and triceps surae muscles of the cat hind limb. , 2003, Journal of neurophysiology.

[23]  T. Bajd,et al.  Electrical stimulation providing functional use of paraplegic patient muscles. , 1980, Medical progress through technology.

[24]  D. Green.  Prophylaxis of thromboembolism in spinal cord-injured patients. , 1992, Chest.

[25]  R. Normann,et al.  Interleaved, multisite electrical stimulation of cat sciatic nerve produces fatigue-resistant, ripple-free motor responses , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  E. Jankowska,et al.  An electrophysiological demonstration of the axonal projections of single spinal interneurones in the cat , 1972, The Journal of physiology.

[27]  E. Jankowska.  Interneuronal relay in spinal pathways from proprioceptors , 1992, Progress in Neurobiology.

[28]  P. Jacobs,et al.  Modes, Benefits, And Risks Of Voluntary And Electrically Induced Exercise In Persons With Spinal Cord Injury , 2001, The journal of spinal cord medicine.

[29]  K. Horch,et al.  Reduced fatigue in electrically stimulated muscle using dual channel intrafascicular electrodes with interleaved stimulation , 1993, Annals of Biomedical Engineering.

[30]  D. Graupe.  An overview of the state of the art of noninvasive FES for independent ambulation by thoracic level paraplegics , 2002, Neurological research.

[31]  Mehdi M Mirbagheri,et al.  The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies , 2002, Brain Research Reviews.

[32]  Christine Haberler,et al.  No tissue damage by chronic deep brain stimulation in Parkinson's disease , 2000, Annals of neurology.

[33]  Gary A. Dudley,et al.  Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury , 1999, European Journal of Applied Physiology and Occupational Physiology.

[34]  P H Peckham,et al.  Tissue response to chronically stimulated implanted epimysial and intramuscular electrodes. , 1997, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[35]  V. Mushahwar,et al.  Strategies for Generating Prolonged Functional Standing Using Intramuscular Stimulation or Intraspinal Microstimulation , 2007, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[36]  S. Rossignol,et al.  Recovery of locomotion after ventral and ventrolateral spinal lesions in the cat. II. Effects of noradrenergic and serotoninergic drugs. , 1999, Journal of neurophysiology.

[37]  K W Horch,et al.  Muscle recruitment through electrical stimulation of the lumbo-sacral spinal cord. , 2000, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[38]  E. Henneman.  The size-principle: a deterministic output emerges from a set of probabilistic connections. , 1985, The Journal of experimental biology.

[39]  A. Prochazka,et al.  Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[40]  V. Mushahwar,et al.  A Physiologically-based Controller for Generating Overground Locomotion using Functional Electrical Stimulation , 2007 .

[41]  I. McDowell,et al.  Measuring health: A guide to rating scales and questionnaires, 3rd ed. , 2006 .

[42]  R. Stein,et al.  Selective stimulation of cat sciatic nerve using an array of varying-length microelectrodes. , 2001, Journal of neurophysiology.

[43]  L Demers,et al.  Development of the Quebec User Evaluation of Satisfaction with assistive Technology (QUEST). , 1996, Assistive technology : the official journal of RESNA.

[44]  M. Nash,et al.  Lower extremity blood flow and responses to occlusion ischemia differ in exercise-trained and sedentary tetraplegic persons. , 1996, Archives of physical medicine and rehabilitation.

[45]  P. Jacobs,et al.  Hypokinetic circulation in persons with paraplegia. , 2002, Medicine and science in sports and exercise.

[46]  Daniel McDonnall,et al.  Selective motor unit recruitment via intrafascicular multielectrode stimulation. , 2004, Canadian journal of physiology and pharmacology.

[47]  Eduardo Fernández,et al.  Long-term stimulation and recording with a penetrating microelectrode array in cat sciatic nerve , 2004, IEEE Transactions on Biomedical Engineering.

[48]  E. Field-Fote.  Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury. , 2001, Archives of physical medicine and rehabilitation.

[49]  L. Bullara,et al.  Arrays for chronic functional microstimulation of the lumbosacral spinal cord , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[50]  R. Triolo,et al.  Consumer perspectives on mobility: implications for neuroprosthesis design. , 2002, Journal of rehabilitation research and development.

[51]  E. Mammen,et al.  Deep vein thrombosis in spinal cord injury. Summary and recommendations. , 1992, Chest.

[52]  W J SHARRARD,et al.  The distribution of the permanent paralysis in the lower limb in poliomyelitis; a clinical and pathological study. , 1955, The Journal of bone and joint surgery. British volume.

[53]  G. Romanes,et al.  The motor cell columns of the lumbo‐sacral spinal cord of the cat , 1951, The Journal of comparative neurology.

[54]  B. Smith,et al.  In-line lead connector for use with implanted neuroprosthesis , 1991, IEEE Transactions on Biomedical Engineering.

[55]  R. Stein,et al.  Electrical stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? , 2000, Archives of physical medicine and rehabilitation.

[56]  E Jankowska,et al.  Direct and indirect activation of nerve cells by electrical pulses applied extracellularly. , 1976, The Journal of physiology.

[57]  G. Dudley,et al.  Weight-supported treadmill vs over-ground training for walking after acute incomplete SCI , 2006, Neurology.

[58]  J. Mortimer,et al.  Comparison of joint torque evoked with monopolar and tripolar-cuff electrodes , 2003, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[59]  D. Cardenas,et al.  Upper extremity pain after spinal cord injury , 1999, Spinal Cord.

[60]  A. Spungen,et al.  Disorders of carbohydrate and lipid metabolism in veterans with paraplegia or quadriplegia: a model of premature aging. , 1994, Metabolism: clinical and experimental.

[61]  A Chantraine,et al.  Bone metabolism in spinal cord injured individuals and in others who have prolonged immobilisation. A review , 1995, Paraplegia.

[62]  A Prochazka,et al.  Intraspinal microstimulation excites multisegmental sensory afferents at lower stimulus levels than local alpha-motoneuron responses. , 2006, Journal of neurophysiology.

[63]  M. Castro,et al.  Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. , 1999, Journal of applied physiology.

[64]  K. Anderson.  Targeting recovery: priorities of the spinal cord-injured population. , 2004, Journal of neurotrauma.

[65]  R. Triolo,et al.  Performance of epimysial stimulating electrodes in the lower extremities of individuals with spinal cord injury , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[66]  Tapping into the Spinal Cord for Restoring Function after Spinal Cord Injury , 2007 .

[67]  R. Stein,et al.  Reanimating limbs after injury or disease , 2005, Trends in Neurosciences.

[68]  Kenneth W. Horch,et al.  Intraspinal microstimulation using cylindrical multielectrodes , 2006, IEEE Transactions on Biomedical Engineering.

[69]  B. Renshaw.  ACTIVITY IN THE SIMPLEST SPINAL REFLEX PATHWAYS , 1940 .

[70]  S. Rossignol.  Locomotion and its recovery after spinal injury , 2000, Current Opinion in Neurobiology.

[71]  S. Rossignol,et al.  Initiation and modulation of the locomotor pattern in the adult chronic spinal cat by noradrenergic, serotonergic and dopaminergic drugs , 1991, Brain Research.

[72]  K J Klose,et al.  Evaluation of a training program for persons with SCI paraplegia using the Parastep 1 ambulation system: part 5. Lower extremity blood flow and hyperemic responses to occlusion are augmented by ambulation training. , 1997, Archives of physical medicine and rehabilitation.

[73]  R. Kobetic,et al.  Walking after incomplete spinal cord injury using an implanted FES system: a case report. , 2007, Journal of rehabilitation research and development.

[74]  R. Normann,et al.  A method for pneumatically inserting an array of penetrating electrodes into cortical tissue , 2006, Annals of Biomedical Engineering.

[75]  V. Mushahwar,et al.  Intraspinal microstimulation generates functional movements after spinal-cord injury , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.