Abstract
It has been proposed that somatosensory stimulation in the form of electromyographically triggered neuromuscular electrical stimulation (NMES) to the peripheral nerve can influence functional measures of motor performance in subjects with stroke and can additionally produce changes in cortical excitability. Using a controlled, double-blind design, we studied the effects of intensive (60 h/3 weeks) treatment at home with NMES compared with a sham treatment, applied to the extensor muscles of the hemiplegic forearm to facilitate hand opening in 16 chronic stroke subjects. We investigated improvement in functional use of the hand and change in cortical activation as measured by functional magnetic resonance imaging (fMRI). Following treatment, subjects improved on measures of grasp and release of objects (Box and Block Test and Jebsen Taylor Hand Function Test [JTHFT]: small objects, stacking, heavy cans), isometric finger extension strength, and self-rated Motor Activity Log (MAL): Amount of Use and How Well score. The sham subjects did not improve on any grasp and release measure or self-rated scale, but did improve on isometric finger extension strength. Importantly, however, following crossover, these subjects improved further in the measure of strength, grasp and release (Box and Block [JTHFT]: page turning), and self-rated MAL: Amount of Use score and How Well score. Using fMRI and a finger-tracking task, an index of cortical intensity in the ipsilateral somatosensory cortex increased significantly from pre-test to post-test following treatment. Cortical activation, as measured by voxel count, did not change. These findings suggest that NMES may have an important role in stimulating cortical sensory areas allowing for improved motor function.
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References
Abo M, Chen Z, Lai L, Reese T, Bjelke B (2001) Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. Neuroreport 12:1543–1547
Aizawa H, Inase M, Mushiake H, Shima K, Tanji J (1991) Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery. Exp Brain Res 84:668–671
American Heart Association (2000) Heart and Stroke Statistical Update. In: American Heart Association, Dallas
Aschersleben G, Gehrke J, Prinz W (2001) Tapping with peripheral nerve block, a role for tactile feedback in the timing of movements. Exp Brain Res 136:331–339
Backes WH, Mess WH, van Kranen-Mastenbroek V, Reulen JPH (2000) Somatosensory cortex responses to median nerve stimulation: fMRI effect of current amplitude and selective attention. Clin Neurophysiol 111:1738–1744
Backes WH, Mess WH, van Kranen-Mastenbroek V, Reulen JPH (2002) Somatosensory cortex responses to median nerve stimulation: fMRI effect of current amplitude and selective attention. Clin Neurophysiol 111:1738–1744
Brandstater M (1998) Stroke rehabilitation. In: Gans JDB (ed) Rehabilitation medicine: principles and practice, 3rd edn. Lippincott-Raven, Philadelphia, pp 1165–1190
Butefisch C, Davis B, Wise S, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci U S A 97:3661–3665
Calautti C, Baron JC (2003) Functional neuroimaging studies of motor recovery after stroke in adults—a review. Stroke 34:1553–1566
Calautti C, Leroy G, Guincestre JY, Baron JC (2001) Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm. Stroke 32:2534–2542
Cao Y, D’Olhaberriague L, Vikingstad EM, Levine SR, Welch KMA (1998) Pilot study of functional MRI to access cerebral activation of motor function after poststroke hemiparesis. Stroke 29:112–122
Caramia MD, Iani C, Bernardi G (1996) Cerebral plasticity after stroke as revealed by ipsilateral responses to magnetic stimulation. Neuroreport 7:1756–1760
Carey J (1990) Manual stretch: effect on finger movement control and force control in subjects with stroke with spastic extrinsic finger flexor muscles. Arch Phys Med Rehabil 71:888–894
Carey J, Bogard C, King B, Suman V (1994) Finger-movement tracking scores in healthy subjects. Percept Mot Skills 79:563–576
Carey J, Baxter T, Di Fabio R (1998) Tracking control in the nonparetic hand of subjects with stroke. Arch Phys Med Rehabil 79:435–441
Carey JR, Kimberley TJ, Lewis SM, Auerbach E, Dorsey L, Rundquist P, Ugurbil K (2002) Analysis of fMRI and finger tracking training in subjects with chronic stroke. Brain 125:773–788
Carey JR, Anderson KM, Kimberley TJ, Lewis SM, Auerbach EJ, Ugurbil K (2003) fMRI analysis of ankle movement tracking training in subject with stroke. Exp Brain Res (in press)
Carr LJ, Harrison LM, Stephens JA (1994) Evidence for bilateral innervation of certain homologous motorneuron pools in man. J Physiol 475:217–227
Cauraugh J, Light K, Kim S, Thigpen M, Behrman A (2000) Chronic motor dysfunction after stroke: recovering wrist and finger extension by electromyography-triggered neuromuscular stimulation. Stroke 31:1360–1364
Chae J, Yu D (2000) A critical review of neuromuscular electrical stimulation for treatment of motor dysfunction in hemiplegia. Assistive Technology 12:33–49
Chae J, Bethoux F, Bohinc T, Dobos L, Davis T, Friedl A (1998) Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia. Stroke 29:975–979
Cohen MS, DuBois RM (1999) Stability, repeatability, and the expression of signal magnitude in functional magnetic resonance imaging. J Magn Res Imaging 10:33–40
Cramer SC, Finklestein SP, Schaechter JD, Bush G, Rosen, BR (1999) Activation of distant motor cortex regions during ipsilateral and contralateral finger movements. J Neurophysiology 81:383–387
de Kroon JR, van der Lee JH, Ijzerman MJ, Lankhorst GJ (2002) Therapeutic electrical stimulation to improve motor control and functional abilities of the upper extremity after stroke: a systematic review. Clinical Rehabilitation 16:350–360
Desrosiers J, Bravo G, Hebert R, Dutil E, Mercier L (1994) Validation of the Box and Block Test as a measure of dexterity of elderly people: reliability, validity, and norms studies. Arch Phys Med Rehabil 75:751–755
Feys H, De Weerdt W, Selz B, Cox Steck G, Spichger R, Vereeck L, Putman D, Van Hoydonck G (1998) Effect of therapeutic intervention for the hemiplegic upper limb in the acutre phase of stroke. A single-blind, randomized, controlled multicenter trial. Stroke 29:785–792
Fields RW (1987) Electromyographically triggered electric muscle stimulation for chronic hemiplegia. Arch Phys Med Rehabil 68:407–414
Folstein M, Folstein S, McHugh P (1975) “Mini-mental state:” a practical method for grading the cognitive state of patients for the clinician. J Psychiat Res 12:189–198
Francisco G, Chae J, Chawla H, Kirshblum S, Zorowitz R, Lewis G, Pang S (1998) Electromyogram-triggered neuromuscular stimulation for improving the arm function of acute stroke survivors: a randomized pilot study. Arch Phys Med Rehabil 79:570–575
Fraser C, Power M, Hobday D, Hollander I, Tyrell P, Hobson A, Williams S, Thompson D (2002) Driving plasticity in human adult motor cortex is associated with improved motor function after brain injury. Neuron 34:831–840
Friel K, Heddings A, Nudo RJ (2000) Effects of postlesion experience on behavioral recovery and neurophysiologic reorganization after cortical injury in primates. Neurorehabil Neural Repair 14:187–198
Georgopoulos AP, Whang K, Georgopoulos MA, Tagaris GA, Amirikian B, Richter W, Kim SG, Ugurbil K (2001) Functional magnetic resonance imaging of visual object construction and shape discrimination: relations among task, hemispheric lateralization, and gender. J Cogn Neurosci 13:72–89
Hamdy S, Rothwell J, Aziz Q, Singh K, Thompson D (1998) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nature Neuroscience 1:64–68
Hummelsheim H, Maier-Loth M, Eickhof C (1997) The functional value of electrical muscle stimulation for the rehabilitation of the hand in stroke patients. Scand J Rehab Med 29:3-10
Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA (1969) An objective and standardized test of hand function. Arch Phys Med Rehabil 50:311–319
Johansson B, Haker E, von Arbin M, Britton M, Langstrom G, Terent A, Ursing D, Asplund K (2000) Acupuncture and transcutaneous nerve stimulation in stroke rehabilitation. Stroke 32:707–713
Jones TA, Schallert T (1994) Use-dependent growth of pyramidal neurons after neocortical damage. J Neurosci 14:2140–2152
Kaelin-Lang A, Luft A, Sawaki L, Burstein A, Sohn Y, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol-London 540:623–633
Kampe K, Jones R, Auer D (2000) Frequency dependence of the functional MRI response after electrical median nerve stimulation. Hum Brain Mapp 9:106–114
Khaslavskaia S, Ladouceur M, Sinkjaer T (2002) Increase in tibialis anterior motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve. Exp Brain Res 145:309–315
Kim SG, Hendrick K, Hu X, Merkle H, Ugurbil K (1994) Potential pitfalls of functional MRI using conventional gradient-recalled echo techniques. NMR Biomed 7:69–74
Kleim JA, Vij K, Ballard DH, Greenough WT (1997) Learning-dependent synaptic modifications in the cerebellar cortex of the adult rat persist for at least four weeks. J Neurosci 17:717–721
Kraft GH, Fitts SS, Hammond MC (1992) Techniques to improve function of the arm and hand in chronic hemiplegia. Arch Phys Med Rehabil 73:220–227
Lewis SM, Jerde TA, Tzagarakis C, Tsekos N, Amirikian B, Georgopoulos MA, Kim S-G, Ugurbil K, Georgopoulos AP (2002) Logarithmic transformations for BOLD fMRI data. Society for Neuroscience Abstracts
Mathiowetz V, Volland G, Kashman N, Weber K (1985) Adult norms for the Box and Block Test of manual dexterity. Am J Occup Ther 39:386–391
McKay DR, Ridding MC, Thompson PD, Miles TS (2002) Induction of persistent changes in the organisation of the human motor cortex. Exp Brain Res 143:342–349
Miltner WH, Bauder H, Sommer M, Dettmers C, Taub E (1999) Effects of constraint-induced movement therapy on patients with chronic motor deficits after stroke: a replication. Stroke 30:586–592
Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS (1994) Compensation in recovery of upper extremity function after stroke: the Copenhagen Stroke Study. Arch Phys Med Rehabil 75:852–857
Nelles G, Spiekermann G, Jueptner M, Leonhardt G, Muller S, Gerhard H, Diener HC (1999) Evolution of functional reorganization in hemiplegic stroke: a serial positron emission tomographic activation study. Ann Neurol 46:901–909
Nelles G, Jentzen W, Jueptner M, Muller S, Diener HC (2001) Arm training induced brain plasticity in stroke studied with serial positron Emission Tomography. NeuroImage 13:1146–1154
Nudo R, Milliken G (1996) Reorganization of movement representations in primary motor cortex following focal ischemic infarcts in adult squirrel monkeys. J Neurophys 75:5:2144–2149
Nudo R, Milliken G, Jenkins W, Merzenich M (1996a) Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys. J Neurosci 16(2): 785–807
Nudo R, Wise, Birukte M, SiFuentes, Milliken F, Garrett W (1996b) Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 272:1791–1794
Nudo RJ, Plautz EJ, Frost S (2001) Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24:1000–1019
Ono M, Kubik S, Abernathey CD (1990) Atlas of the cerebral sulci. Thieme Medical Publishers, New York
Panizza M, Nilsson J, Roth BJ, Basser PJ, Hallett M (1992) Relevance of stimulus duration for activation of motor and sensory fibers; implications for the study of H-reflexes and magnetic stimulation. Electroenceph Clin Neurophysiol 85:22–29
Plautz EJ, Milliken GW, Nudo RJ (2000) Effects of repetitive motor training on movement representations in adult squirrel monkeys: role of use versus learning. Neurobiol Learn Mem 74:27–55
Powell J, Pandyan A, Granat M (1999) Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke 30:1384–1389
Reding MJ, Potes E (1998) Rehabilitation outcome following initial unilateral hemispheric stroke. Life table analysis approach. Stroke 19:1354–1358
Remple MS, Bruneau RM, VandenBerg PM, Goertzen C, Kleim JA (2001) Sensitivity of cortical movement representations to motor experience: evidence that skill learning but not strength training induces cortical reorganization. Behav Brain Res 123:133–141
Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143
Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469
Smith GV, Alon G, Roys SR, Gullapalli RP (2003) Functional MRI determination of a dose-response relationship to lower extremity neuromuscular electrical stimulation in healthy subjects. ExpBrain Res 150: 33–39
Sonde L, Gip C, Fernaeus S, Nilsson C, Viitanen M (1998) Stimulation with low frequency (1/7 Hz) transcutaneous electric nerve stimulation increases motor function of the post-stroke paretic arm. Scand J Rehab Med 30:95–99
Spiegel J, Tintera J, Gawehn J, Stoeter P, Treede R (1999) Functional MRI of human primary somatosensory and motor cortex during median nerve stimulation. Clin Neurophysiol 110:47–52
Stefen K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584
Strupp J (1996) Stimulate: a GUI based, fMRI analysis software package. NeuroImage 3:S607
Talairach J, Tournoux P (1988) Co-planar stereotoxic atlas of the human brain. Thieme, New York
Taub E, Miller NE, Novack TA, Cook EWI, Fleming WC, Nepomuceno CS (1993) Technique to improve chronic motor deficit after stroke. Arch Phys Med Rehabil 74:347–354
Ugurbil K, Ogawa S, Kim SG, Chen W, Zhu XH (1999) Imaging brain activity using nuclear spins. In: Maraviglia B (ed) Magnetic resonance and brain function: approaches from physics. IOS Press, Amsterdam, pp 261–310
Vaughan JT, Adriany G, Garwood M, Andersen P, Ugurbil K (2001) The head cradle: an open faced, high performance TEM coil. In: Proceedings of the 9th Annual Meeting of ISMRM, Glasgow, p 15
Waldvogel D, van Gelderen P, Immisch I, Pfeiffer C, Hallett M (2000) The variability of serial fMRI data: correlation between a visual and a motor task. Neuroreport 11:3843–3847
Weiller C, Ramsay SC, Wise RJS, Friston KJ, Frackowiak RSJ (1993) Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol 33:181–189
Xiong J, Gao J, Lancaster J, Fox P (1995) Clustered pixels analysis for functional MRI activation studies of the human brain. Hum Brain Mapp 3:287–301
Ziemann U, Ishii K, Borgheresi A, Yaseen Z, Battaglia F, Hallett M, Cincotta M, Wassermann EM (1999) Dissociation of the pathways mediating ipsilateral and contralateral motor-evoked potentials in human hand and arm muscles. J Physiol 518:895–906
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We gratefully acknowledge the support for this work from the National Institute on Disability and Rehabilitation Research (US Department of Education #H133G010077) and the National Institutes of Health (National Centers for Research Resources P41RR08079 and M01RR00400).
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This work was completed at the University of Minnesota, Minneapolis, MN 55455, USA
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Kimberley, T.J., Lewis, S.M., Auerbach, E.J. et al. Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res 154, 450–460 (2004). https://doi.org/10.1007/s00221-003-1695-y
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DOI: https://doi.org/10.1007/s00221-003-1695-y