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Published in: Experimental Brain Research 1/2008

01-10-2008 | Research Article

Cortical excitability changes following grasping exercise augmented with electrical stimulation

Authors: Gergely I. Barsi, Dejan B. Popovic, Ina M. Tarkka, Thomas Sinkjær, Michael J. Grey

Published in: Experimental Brain Research | Issue 1/2008

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Abstract

Rehabilitation with augmented electrical stimulation can enhance functional recovery after stroke, and cortical plasticity may play a role in this process. The purpose of this study was to compare the effects of three training paradigms on cortical excitability in healthy subjects. Cortical excitability was evaluated by analysing the input–output relationship between transcranial magnetic stimulation intensity and motor evoked potentials (MEPs) from the flexor muscles of the fingers. The study was performed with 25 healthy volunteers who underwent 20-min simulated therapy sessions of: (1) functional electrical stimulation (FES) of the finger flexors and extensors, (2) voluntary movement (VOL) with sensory stimulation, and (3) therapeutic FES (TFES) where the electrical stimulation augmented voluntary activation. TFES training produced a significant increase in MEP magnitude throughout the stimulation range, suggesting an increase in cortical excitability. In contrast, neither the FES nor voluntary movement alone had such an effect. These results suggest that the combination of voluntary effort and FES has greater potential to induce plasticity in the motor cortex and that TFES might be a more effective approach in rehabilitation after stroke than FES or repetitive voluntary training alone.
Literature
go back to reference Andersen B, Westlund B, Krarup C (2003) Failure of activation of spinal motoneurons after muscle fatigue in healthy subjects studied by transcranial magnetic stimulation. J Physiol 551:345–356PubMedCrossRef Andersen B, Westlund B, Krarup C (2003) Failure of activation of spinal motoneurons after muscle fatigue in healthy subjects studied by transcranial magnetic stimulation. J Physiol 551:345–356PubMedCrossRef
go back to reference Cantello R, Gianelli M, Civardi C, Mutani R (1992) Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 42:1951–1959PubMed Cantello R, Gianelli M, Civardi C, Mutani R (1992) Magnetic brain stimulation: the silent period after the motor evoked potential. Neurology 42:1951–1959PubMed
go back to reference Castro-Alamancos M, Garcia-Segura L, Borrell J (1992) Transfer of function to a specific area of the cortex after induced recovery from brain damage. Eur J Neurosci 4:853–863PubMedCrossRef Castro-Alamancos M, Garcia-Segura L, Borrell J (1992) Transfer of function to a specific area of the cortex after induced recovery from brain damage. Eur J Neurosci 4:853–863PubMedCrossRef
go back to reference Chae J, Yu D (1999) Neuromuscular stimulation for motor relearning in hemiplegia. Crit Rev Phys Med Rehabil Med 11:279–297 Chae J, Yu D (1999) Neuromuscular stimulation for motor relearning in hemiplegia. Crit Rev Phys Med Rehabil Med 11:279–297
go back to reference Chen R (2000) Studies of human motor physiology with transcranial magnetic stimulation. Muscle Nerve Suppl 9:26–32CrossRef Chen R (2000) Studies of human motor physiology with transcranial magnetic stimulation. Muscle Nerve Suppl 9:26–32CrossRef
go back to reference Classen J, Liepert J, Wise SP, Hellett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123PubMed Classen J, Liepert J, Wise SP, Hellett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123PubMed
go back to reference Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticopinal pathway. Exp Brain Res 114:329–338PubMedCrossRef Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticopinal pathway. Exp Brain Res 114:329–338PubMedCrossRef
go back to reference Di Piero V, Chollet F, Mac Carthy P, Lenzi G, Frackowiak R (1992) Motor recovery after acute ischaemic stroke: a metabolic study. J Neurol Neurosurg Psychiatr 55:990–996PubMed Di Piero V, Chollet F, Mac Carthy P, Lenzi G, Frackowiak R (1992) Motor recovery after acute ischaemic stroke: a metabolic study. J Neurol Neurosurg Psychiatr 55:990–996PubMed
go back to reference Fuhr P, Cohen LG, Roth BJ, Hallet M (1991) Latency of motor evoked potentials to focal transcranial stimulation varies as a function of scalp position stimulated. Electroencephalogr Clin Neurophysiol 81(2):81–89PubMedCrossRef Fuhr P, Cohen LG, Roth BJ, Hallet M (1991) Latency of motor evoked potentials to focal transcranial stimulation varies as a function of scalp position stimulated. Electroencephalogr Clin Neurophysiol 81(2):81–89PubMedCrossRef
go back to reference Gritsenko V, Prochazka A (2004) A functional electric stimulation-assisted exercise therapy system for hemiplegic hand function. Arch Phys Med Rehabil 85:881–885PubMedCrossRef Gritsenko V, Prochazka A (2004) A functional electric stimulation-assisted exercise therapy system for hemiplegic hand function. Arch Phys Med Rehabil 85:881–885PubMedCrossRef
go back to reference Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374PubMedCrossRef Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10(5):361–374PubMedCrossRef
go back to reference Ho KH, Nithi K, Mills KR (1998) Covariation between human intrinsic hand muscles of the silent periods and compound muscle action potentials evoked by magnetic brain stimulation: evidence for common inhibitory connections. Exp Brain Res 122:433–440PubMedCrossRef Ho KH, Nithi K, Mills KR (1998) Covariation between human intrinsic hand muscles of the silent periods and compound muscle action potentials evoked by magnetic brain stimulation: evidence for common inhibitory connections. Exp Brain Res 122:433–440PubMedCrossRef
go back to reference Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534PubMed Inghilleri M, Berardelli A, Cruccu G, Manfredi M (1993) Silent period evoked by transcranial stimulation of the human cortex and cervicomedullary junction. J Physiol 466:521–534PubMed
go back to reference Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251(4996):944–947PubMedCrossRef Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251(4996):944–947PubMedCrossRef
go back to reference Jenkins WM, Merzenich MM (1987) Reorganisation of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. In: Seil FJ, Herbert E, Carlson B (eds) Progress in brain research, vol 71. Elsevier, Amsterdam, p 249 Jenkins WM, Merzenich MM (1987) Reorganisation of neocortical representations after brain injury: a neurophysiological model of the bases of recovery from stroke. In: Seil FJ, Herbert E, Carlson B (eds) Progress in brain research, vol 71. Elsevier, Amsterdam, p 249
go back to reference Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502PubMedCrossRef Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502PubMedCrossRef
go back to reference 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(3):309–315PubMedCrossRef 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(3):309–315PubMedCrossRef
go back to reference Kido Thompson A, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500PubMedCrossRef Kido Thompson A, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500PubMedCrossRef
go back to reference Knash ME, Kido A, Gorassini M, Chan KM, Stein RB (2003) Electrical stimulation of the human common peroneal nerve elicits lasting facilitation of cortical motor-evoked potentials. Exp Brain Res 153:366–377PubMedCrossRef Knash ME, Kido A, Gorassini M, Chan KM, Stein RB (2003) Electrical stimulation of the human common peroneal nerve elicits lasting facilitation of cortical motor-evoked potentials. Exp Brain Res 153:366–377PubMedCrossRef
go back to reference McDonnell MN, Ridding MC (2006) Afferent stimulation facilitates performance on a novel motor task. Exp Brain Res 170:109–115PubMedCrossRef McDonnell MN, Ridding MC (2006) Afferent stimulation facilitates performance on a novel motor task. Exp Brain Res 170:109–115PubMedCrossRef
go back to reference Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438PubMedCrossRef Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438PubMedCrossRef
go back to reference Nudo RJ (2003) Functional and structural plasticity in motor cortex: implication for stroke recovery. Phys Med Rehabil Clin N Am 14(1 Suppl):857–876 Nudo RJ (2003) Functional and structural plasticity in motor cortex: implication for stroke recovery. Phys Med Rehabil Clin N Am 14(1 Suppl):857–876
go back to reference Nudo RJ (2007) Postinfarct cortical plasticity and behavioral recovery. Stroke 38(2 Suppl):840–845PubMedCrossRef Nudo RJ (2007) Postinfarct cortical plasticity and behavioral recovery. Stroke 38(2 Suppl):840–845PubMedCrossRef
go back to reference Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V (2006) Effects of ageing on motor cortex excitability. Neurosci Res 55:74–77PubMedCrossRef Oliviero A, Profice P, Tonali PA, Pilato F, Saturno E, Dileone M, Ranieri F, Di Lazzaro V (2006) Effects of ageing on motor cortex excitability. Neurosci Res 55:74–77PubMedCrossRef
go back to reference Peckham PH, Knutson JS (2005) Functional electrical stimulation for neuromuscular applications. Annu Rev Biomed Eng 7:327–360PubMedCrossRef Peckham PH, Knutson JS (2005) Functional electrical stimulation for neuromuscular applications. Annu Rev Biomed Eng 7:327–360PubMedCrossRef
go back to reference Perez MA, Lungholt BKS, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205PubMedCrossRef Perez MA, Lungholt BKS, Nyborg K, Nielsen JB (2004) Motor skill training induces changes in the excitability of the leg cortical area in healthy humans. Exp Brain Res 159:197–205PubMedCrossRef
go back to reference Pitcher JB, Miles TS (2002) Alterations in corticospinal excitability with imposed vs. voluntary fatigue in human hand muscles. J Appl Physiol 92:2132–2138 Pitcher JB, Miles TS (2002) Alterations in corticospinal excitability with imposed vs. voluntary fatigue in human hand muscles. J Appl Physiol 92:2132–2138
go back to reference Popovic MB, Popovic DB, Sinkjaer T, Stefanovic A, Schwirtlich L (2002) Restitution of reaching and grasping promoted by functional electrical therapy. Artif Organs 26(3):271–275PubMedCrossRef Popovic MB, Popovic DB, Sinkjaer T, Stefanovic A, Schwirtlich L (2002) Restitution of reaching and grasping promoted by functional electrical therapy. Artif Organs 26(3):271–275PubMedCrossRef
go back to reference Popovic MB, Popovic DB, Sinkjaer T, Stefanovic A, Schwirtlich L (2003) Clinical evaluation of functional electrical therapy in acute hemiplegic subjects. J Rehabil Res Dev 40:443–453PubMedCrossRef Popovic MB, Popovic DB, Sinkjaer T, Stefanovic A, Schwirtlich L (2003) Clinical evaluation of functional electrical therapy in acute hemiplegic subjects. J Rehabil Res Dev 40:443–453PubMedCrossRef
go back to reference Popovic DB, Popovic MB, Sinkjaer T, Stefanovic A, Schwirtlich L (2004) Therapy of paretic arm in hemiplegic subjects augmented with a neural prosthesis: a cross-over study. Can J Physiol Pharmacol 82:749–756PubMedCrossRef Popovic DB, Popovic MB, Sinkjaer T, Stefanovic A, Schwirtlich L (2004) Therapy of paretic arm in hemiplegic subjects augmented with a neural prosthesis: a cross-over study. Can J Physiol Pharmacol 82:749–756PubMedCrossRef
go back to reference Popovic MR, Thrasher TA, Adams ME, Takes V, Zivanovic V, Tonack MI (2006) Functional electrical therapy: retraining grasping in spinal cord injury. Spinal Cord 44(3):143–151PubMedCrossRef Popovic MR, Thrasher TA, Adams ME, Takes V, Zivanovic V, Tonack MI (2006) Functional electrical therapy: retraining grasping in spinal cord injury. Spinal Cord 44(3):143–151PubMedCrossRef
go back to reference Powell J, Pandyan D, Granat M, Cameron M, Stott DJ (1990) Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke 30:1384–1389 Powell J, Pandyan D, Granat M, Cameron M, Stott DJ (1990) Electrical stimulation of wrist extensors in poststroke hemiplegia. Stroke 30:1384–1389
go back to reference Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes. Cambridge University Press, Cambridge Press WH, Flannery BP, Teukolsky SA, Vetterling WT (1986) Numerical recipes. Cambridge University Press, Cambridge
go back to reference Ridding MC, Rothwell JC (1995) Reorganisation in human motor cortex. Can J Physiol Pharmacol 73(2):218–222PubMed Ridding MC, Rothwell JC (1995) Reorganisation in human motor cortex. Can J Physiol Pharmacol 73(2):218–222PubMed
go back to reference Ridding MC, Rothwell JC (1997) Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol 105:340–344PubMedCrossRef Ridding MC, Rothwell JC (1997) Stimulus/response curves as a method of measuring motor cortical excitability in man. Electroencephalogr Clin Neurophysiol 105:340–344PubMedCrossRef
go back to reference Ridding MC, Rothwell JC (1999) Afferent input and cortical organisation: a study with magnetic stimulation. Exp Brain Res 126:536–544PubMedCrossRef Ridding MC, Rothwell JC (1999) Afferent input and cortical organisation: a study with magnetic stimulation. Exp Brain Res 126:536–544PubMedCrossRef
go back to reference 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 131:135–143PubMedCrossRef 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 131:135–143PubMedCrossRef
go back to reference Rossini PM, Pauri F (2000) Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas ‘plastic’ reorganisation. Brain Res Rev 33:131–154PubMedCrossRef Rossini PM, Pauri F (2000) Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas ‘plastic’ reorganisation. Brain Res Rev 33:131–154PubMedCrossRef
go back to reference Rosenkranz K, Rothwell JC (2004) The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex. J Physiol 561(Pt 1):307–320 Rosenkranz K, Rothwell JC (2004) The effect of sensory input and attention on the sensorimotor organization of the hand area of the human motor cortex. J Physiol 561(Pt 1):307–320
go back to reference Sacco P, Newberry R, McFadden L, Brown T, McComas AJ (1998) Depression of human electromyographic activity by fatigue of synergistic muscle. Muscle Nerve 20:710–717CrossRef Sacco P, Newberry R, McFadden L, Brown T, McComas AJ (1998) Depression of human electromyographic activity by fatigue of synergistic muscle. Muscle Nerve 20:710–717CrossRef
go back to reference Seitz RJ, Bütefisch CM, Kleiser R, Hömberg V (2004) Reorganisation of cerebral circuits in human ischemic brain disease. Restor Neurol Neurosci 22(3–5):207–229PubMed Seitz RJ, Bütefisch CM, Kleiser R, Hömberg V (2004) Reorganisation of cerebral circuits in human ischemic brain disease. Restor Neurol Neurosci 22(3–5):207–229PubMed
go back to reference Siebner HR, Rothwell JC (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16PubMedCrossRef Siebner HR, Rothwell JC (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp Brain Res 148:1–16PubMedCrossRef
go back to reference Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmitt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human ageing. Neurology 53(7):1458–1461PubMed Smith CD, Umberger GH, Manning EL, Slevin JT, Wekstein DR, Schmitt FA, Markesbery WR, Zhang Z, Gerhardt GA, Kryscio RJ, Gash DM (1999) Critical decline in fine motor hand movements in human ageing. Neurology 53(7):1458–1461PubMed
go back to reference Stetkarova I, Leis AA, Stokic DS, Delapasse JS, Tarkka IM (1994) Characteristics of the silent period after transcranial magnetic stimulation. Am J Phys Med Rehabil 73:98–102PubMedCrossRef Stetkarova I, Leis AA, Stokic DS, Delapasse JS, Tarkka IM (1994) Characteristics of the silent period after transcranial magnetic stimulation. Am J Phys Med Rehabil 73:98–102PubMedCrossRef
go back to reference Taylor JL, Allen GM, Butler JE, Gandevia SC (1997) Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation. Exp Brain Res 117:472–478PubMedCrossRef Taylor JL, Allen GM, Butler JE, Gandevia SC (1997) Effect of contraction strength on responses in biceps brachii and adductor pollicis to transcranial magnetic stimulation. Exp Brain Res 117:472–478PubMedCrossRef
go back to reference Taylor JL, Butler JE, Gandevia SC (1999) Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contraction. Exp Brain Res 127:108–115PubMedCrossRef Taylor JL, Butler JE, Gandevia SC (1999) Altered responses of human elbow flexors to peripheral-nerve and cortical stimulation during a sustained maximal voluntary contraction. Exp Brain Res 127:108–115PubMedCrossRef
go back to reference Thrasher TA, Flett HM, Popovic MR (2006) Gait training regimen for incomplete spinal cord injury using functional electrical stimulation. Spinal Cord 44(6):351–367CrossRef Thrasher TA, Flett HM, Popovic MR (2006) Gait training regimen for incomplete spinal cord injury using functional electrical stimulation. Spinal Cord 44(6):351–367CrossRef
go back to reference Winslow J, Jacobs PL, Tepavac D (2003) Fatigue compensation during FES using surface EMG. J Electromyogr Kinesiol 13:555–568PubMedCrossRef Winslow J, Jacobs PL, Tepavac D (2003) Fatigue compensation during FES using surface EMG. J Electromyogr Kinesiol 13:555–568PubMedCrossRef
Metadata
Title
Cortical excitability changes following grasping exercise augmented with electrical stimulation
Authors
Gergely I. Barsi
Dejan B. Popovic
Ina M. Tarkka
Thomas Sinkjær
Michael J. Grey
Publication date
01-10-2008
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 1/2008
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-008-1495-5

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