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01-02-2004 | Research Article

Electrical stimulation driving functional improvements and cortical changes in subjects with stroke

Authors: Teresa J. Kimberley, Scott M. Lewis, Edward J. Auerbach, Lisa L. Dorsey, Jeanne M. Lojovich, James R. Carey

Published in: Experimental Brain Research | Issue 4/2004

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.

Abo M, Chen Z, Lai L, Reese T, Bjelke B (2001) Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. Neuroreport 12:1543–1547PubMed

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 84:668–671PubMed

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 136:331–339CrossRefPubMed

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 111:1738–1744CrossRefPubMed

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 111:1738–1744CrossRef

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 97:3661–3665PubMed

Calautti C, Baron JC (2003) Functional neuroimaging studies of motor recovery after stroke in adults—a review. Stroke 34:1553–1566CrossRefPubMed

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 32:2534–2542PubMed

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 29:112–122PubMed

Caramia MD, Iani C, Bernardi G (1996) Cerebral plasticity after stroke as revealed by ipsilateral responses to magnetic stimulation. Neuroreport 7:1756–1760PubMed

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 71:888–894PubMed

Carey J, Bogard C, King B, Suman V (1994) Finger-movement tracking scores in healthy subjects. Percept Mot Skills 79:563–576PubMed

Carey J, Baxter T, Di Fabio R (1998) Tracking control in the nonparetic hand of subjects with stroke. Arch Phys Med Rehabil 79:435–441PubMed

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 125:773–788CrossRefPubMed

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 475:217–227PubMed

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 31:1360–1364PubMed

Chae J, Yu D (2000) A critical review of neuromuscular electrical stimulation for treatment of motor dysfunction in hemiplegia. Assistive Technology 12:33–49PubMed

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 29:975–979PubMed

Cohen MS, DuBois RM (1999) Stability, repeatability, and the expression of signal magnitude in functional magnetic resonance imaging. J Magn Res Imaging 10:33–40CrossRef

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 16:350–360CrossRefPubMed

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 75:751–755PubMed

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 29:785–792PubMed

Fields RW (1987) Electromyographically triggered electric muscle stimulation for chronic hemiplegia. Arch Phys Med Rehabil 68:407–414PubMed

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 12:189–198CrossRefPubMed

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 79:570–575PubMed

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 34:831–840PubMed

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 14:187–198PubMed

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 13:72–89CrossRefPubMed

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 1:64–68CrossRefPubMed

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 50:311–319PubMed

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 14:2140–2152PubMed

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 9:106–114CrossRefPubMed

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 145:309–315CrossRefPubMed

Kim SG, Hendrick K, Hu X, Merkle H, Ugurbil K (1994) Potential pitfalls of functional MRI using conventional gradient-recalled echo techniques. NMR Biomed 7:69–74PubMed

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 17:717–721PubMed

Kraft GH, Fitts SS, Hammond MC (1992) Techniques to improve function of the arm and hand in chronic hemiplegia. Arch Phys Med Rehabil 73:220–227PubMed

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 39:386–391PubMed

McKay DR, Ridding MC, Thompson PD, Miles TS (2002) Induction of persistent changes in the organisation of the human motor cortex. Exp Brain Res 143:342–349CrossRefPubMed

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 30:586–592PubMed

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 75:852–857PubMed

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 46:901–909CrossRefPubMed

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 13:1146–1154CrossRefPubMed

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): 785–807PubMed

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 24:1000–1019CrossRefPubMed

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 85:22–29CrossRefPubMed

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 74:27–55CrossRefPubMed

Powell J, Pandyan A, Granat M (1999) Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke 30:1384–1389PubMed

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 123:133–141CrossRefPubMed

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 131:135–143CrossRefPubMed

Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469PubMed

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 30:95–99CrossRef

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 110:47–52CrossRefPubMed

Stefen K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123:572–584CrossRefPubMed

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 74:347–354PubMed

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 11:3843–3847PubMed

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 33:181–189PubMed

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 518:895–906PubMed

Title: Electrical stimulation driving functional improvements and cortical changes in subjects with stroke
Authors: Teresa J. Kimberley
Scott M. Lewis
Edward J. Auerbach
Lisa L. Dorsey
Jeanne M. Lojovich
James R. Carey
Publication date: 01-02-2004
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 4/2004
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-003-1695-y

At a glance: The STEP trials

Springer Medicine

Electrical stimulation driving functional improvements and cortical changes in subjects with stroke

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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