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Published in: Experimental Brain Research 3/2011

01-03-2011 | Research Article

Neuromuscular electrical stimulation has a global effect on corticospinal excitability for leg muscles and a focused effect for hand muscles

Authors: C. S. Mang, J. M. Clair, D. F. Collins

Published in: Experimental Brain Research | Issue 3/2011

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Abstract

The afferent volley generated during neuromuscular electrical stimulation (NMES) can increase the excitability of human corticospinal (CS) pathways to muscles of the leg and hand. Over time, such increases can strengthen CS pathways damaged by injury or disease and result in enduring improvements in function. There is some evidence that NMES affects CS excitability differently for muscles of the leg and hand, although a direct comparison has not been conducted. Thus, the present experiments were designed to compare the strength and specificity of NMES-induced changes in CS excitability for muscles of the leg and hand. Two hypotheses were tested: (1) For muscles innervated by the stimulated nerve (target muscles), CS excitability will increase more for the hand than for the leg. (2) For muscles not innervated by the stimulated nerve (non-target muscles), CS excitability will increase for muscles of the leg but not muscles of the hand. NMES was delivered over the common peroneal (CP) nerve in the leg or the median nerve at the wrist using a 1-ms pulse width in a 20 s on, 20 s off cycle for 40 min. The intensity was set to evoke an M-wave that was ~15% of the maximal M-wave in the target muscle: tibialis anterior (TA) in the leg and abductor pollicis brevis (APB) in the hand. Ten motor-evoked potentials (MEPs) were recorded from the target muscles and from 2 non-target muscles of each limb using transcranial magnetic stimulation delivered over the “hotspot” for each muscle before and after the NMES. MEP amplitude increased significantly for TA (by 45 ± 6%) and for APB (56 ± 8%), but the amplitude of these increases was not different. In non-target muscles, MEPs increased significantly for muscles of the leg (42 ± 4%), but not the hand. Although NMES increased CS excitability for target muscles to the same extent in the leg and hand, the differences in the effect on non-target muscles suggest that NMES has a “global” effect on CS excitability for the leg and a “focused” effect for the hand. These differences may reflect differences in the specificity of afferent projections to the cortex. Global increases in CS excitability for the leg could be advantageous for rehabilitation as NMES applied to one muscle could strengthen CS pathways and enhance function for multiple muscles.
Literature
go back to reference Classen J, Steinfelder B, Liepert J, Stefan K, Celnik P, Cohen LG, Hess A, Kunesch E, Chen R, Benecke R, Hallett M (2000) Cutaneomotor integration in humans is somatotopically organized at various levels of the nervous system and is task dependent. Exp Brain Res 130:48–59PubMedCrossRef Classen J, Steinfelder B, Liepert J, Stefan K, Celnik P, Cohen LG, Hess A, Kunesch E, Chen R, Benecke R, Hallett M (2000) Cutaneomotor integration in humans is somatotopically organized at various levels of the nervous system and is task dependent. Exp Brain Res 130:48–59PubMedCrossRef
go back to reference Conforto AB, Kaelin-Lang A, Cohen LG (2002) Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol 51:122–125PubMedCrossRef Conforto AB, Kaelin-Lang A, Cohen LG (2002) Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol 51:122–125PubMedCrossRef
go back to reference Deletis V, Schild JH, Beric A, Dimitrijevic MR (1992) Facilitation of motor evoked potentials by somatosensory afferent stimulation. Electroencephalogr Clin Neurophysiol 85:302–310PubMedCrossRef Deletis V, Schild JH, Beric A, Dimitrijevic MR (1992) Facilitation of motor evoked potentials by somatosensory afferent stimulation. Electroencephalogr Clin Neurophysiol 85:302–310PubMedCrossRef
go back to reference Everaert DG, Thompson AK, Chong SL, Stein RB (2010) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24(2):168–177PubMedCrossRef Everaert DG, Thompson AK, Chong SL, Stein RB (2010) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24(2):168–177PubMedCrossRef
go back to reference Hoffman LR, Field-Fote EC (2007) Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther 87:208–223PubMedCrossRef Hoffman LR, Field-Fote EC (2007) Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther 87:208–223PubMedCrossRef
go back to reference Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMedCrossRef Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMedCrossRef
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 145:309–315PubMedCrossRef 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 145:309–315PubMedCrossRef
go back to reference Kido TA, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500CrossRef Kido TA, Stein RB (2004) Short-term effects of functional electrical stimulation on motor-evoked potentials in ankle flexor and extensor muscles. Exp Brain Res 159:491–500CrossRef
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 Lagerquist O, Collins DF (2008) Stimulus pulse width influences H-reflex recruitment but not H(max)/M(max) ratio. Muscle Nerve 37(4):483–489PubMedCrossRef Lagerquist O, Collins DF (2008) Stimulus pulse width influences H-reflex recruitment but not H(max)/M(max) ratio. Muscle Nerve 37(4):483–489PubMedCrossRef
go back to reference Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42(6):886–893PubMedCrossRef Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42(6):886–893PubMedCrossRef
go back to reference Lagerquist O, Zehr EP, Baldwin ER, Klakowicz PM, Collins DF (2006) Diurnal changes in the amplitude of the Hoffmann reflex in the human soleus but not in the flexor carpi radialis muscle. Exp Brain Res 170:1–6PubMedCrossRef Lagerquist O, Zehr EP, Baldwin ER, Klakowicz PM, Collins DF (2006) Diurnal changes in the amplitude of the Hoffmann reflex in the human soleus but not in the flexor carpi radialis muscle. Exp Brain Res 170:1–6PubMedCrossRef
go back to reference Liberson WT, Holmquest HJ, Scot D, Dow M (1961) Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil 42:101–105PubMed Liberson WT, Holmquest HJ, Scot D, Dow M (1961) Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil 42:101–105PubMed
go back to reference Mang CS, Lagerquist O, Collins DF (2010) Changes in corticospinal excitability evoked by common peroneal nerve stimulation depend on stimulation frequency. Exp Brain Res 203:11–20PubMedCrossRef Mang CS, Lagerquist O, Collins DF (2010) Changes in corticospinal excitability evoked by common peroneal nerve stimulation depend on stimulation frequency. Exp Brain Res 203:11–20PubMedCrossRef
go back to reference McKay D, Brooker R, Giacomin P, Ridding M, Miles T (2002) Time course of induction of increased human motor cortex excitability by nerve stimulation. NeuroReport 13:1271–1273PubMedCrossRef McKay D, Brooker R, Giacomin P, Ridding M, Miles T (2002) Time course of induction of increased human motor cortex excitability by nerve stimulation. NeuroReport 13:1271–1273PubMedCrossRef
go back to reference Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045PubMed Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045PubMed
go back to reference Pitcher JB, Ridding MC, Miles TS (2003) Frequency-dependent, bi-directional plasticity in motor cortex of human adults. Clin Neurophysiol 114:1265–1271PubMedCrossRef Pitcher JB, Ridding MC, Miles TS (2003) Frequency-dependent, bi-directional plasticity in motor cortex of human adults. Clin Neurophysiol 114:1265–1271PubMedCrossRef
go back to reference Poon DE, Roy FD, Gorassini MA, Stein RB (2008) Interaction of paired cortical and peripheral nerve stimulation on human motor neurons. Exp Brain Res 188:13–21PubMedCrossRef Poon DE, Roy FD, Gorassini MA, Stein RB (2008) Interaction of paired cortical and peripheral nerve stimulation on human motor neurons. Exp Brain Res 188:13–21PubMedCrossRef
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 Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469PubMedCrossRef Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469PubMedCrossRef
go back to reference Roy FD, Gorassini MA (2008) Peripheral sensory activation of cortical circuits in the leg motor cortex of man. J Physiol 586(Pt 17):4091–4105PubMedCrossRef Roy FD, Gorassini MA (2008) Peripheral sensory activation of cortical circuits in the leg motor cortex of man. J Physiol 586(Pt 17):4091–4105PubMedCrossRef
go back to reference Sheffler LR, Chae J (2007) Neuromuscular electrical stimulation in neurorehabilitation. Muscle Nerve 35:562–590PubMedCrossRef Sheffler LR, Chae J (2007) Neuromuscular electrical stimulation in neurorehabilitation. Muscle Nerve 35:562–590PubMedCrossRef
go back to reference 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. Exp Brain Res 150:33–39PubMed 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. Exp Brain Res 150:33–39PubMed
go back to reference Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584PubMedCrossRef Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584PubMedCrossRef
go back to reference Tamm AS, Lagerquist O, Ley AL, Collins DF (2009) Chronotype influences diurnal variations in the excitability of the human motor cortex and the ability to generate torque during a maximum voluntary contraction. J Biol Rhythms 24:211–224PubMedCrossRef Tamm AS, Lagerquist O, Ley AL, Collins DF (2009) Chronotype influences diurnal variations in the excitability of the human motor cortex and the ability to generate torque during a maximum voluntary contraction. J Biol Rhythms 24:211–224PubMedCrossRef
go back to reference Walton C, Kalmar J, Cafarelli E (2003) Caffeine increases spinal excitability in humans. Muscle Nerve 28:359–364PubMedCrossRef Walton C, Kalmar J, Cafarelli E (2003) Caffeine increases spinal excitability in humans. Muscle Nerve 28:359–364PubMedCrossRef
go back to reference Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124:1171–1181PubMedCrossRef Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124:1171–1181PubMedCrossRef
Metadata
Title
Neuromuscular electrical stimulation has a global effect on corticospinal excitability for leg muscles and a focused effect for hand muscles
Authors
C. S. Mang
J. M. Clair
D. F. Collins
Publication date
01-03-2011
Publisher
Springer-Verlag
Published in
Experimental Brain Research / Issue 3/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-011-2556-8

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