Abstract
Neuromuscular electrical stimulation (NMES) generates contractions by depolarising axons beneath the stimulating electrodes. The depolarisation of motor axons produces contractions by signals travelling from the stimulation location to the muscle (peripheral pathway), with no involvement of the central nervous system (CNS). The concomitant depolarisation of sensory axons sends a large volley into the CNS and this can contribute to contractions by signals travelling through the spinal cord (central pathway) which may have advantages when NMES is used to restore movement or reduce muscle atrophy. In addition, the electrically evoked sensory volley increases activity in CNS circuits that control movement and this can also enhance neuromuscular function after CNS damage. The first part of this review provides an overview of how peripheral and central pathways contribute to contractions evoked by NMES and describes how differences in NMES parameters affect the balance between transmission along these two pathways. The second part of this review describes how NMES location (i.e. over the nerve trunk or muscle belly) affects transmission along peripheral and central pathways and describes some implications for motor unit recruitment during NMES. The third part of this review summarises some of the effects that the electrically evoked sensory volley has on CNS circuits, and highlights the need to identify optimal stimulation parameters for eliciting plasticity in the CNS. A goal of this work is to identify the best way to utilize the electrically evoked sensory volley generated during NMES to exploit mechanisms inherent to the neuromuscular system and enhance neuromuscular function for rehabilitation.
Similar content being viewed by others
References
Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74:532–537
Adrian ED, Bronk DW (1929) The discharge of impulses in motor nerve fibres: Part II. The frequency of discharge in reflex and voluntary contractions. J Physiol 67:i3–i151
Baker LL, Wederich CL, McNeal DR, Newsam CJ, Waters RL (2000) Neuromuscular electrical stimulation: a pratical guide. Los Amigos Research and Educational Institute, Downey
Baldwin ER, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240
Bawa P, Pang MY, Olesen KA, Calancie B (2006) Rotation of motoneurons during prolonged isometric contractions in humans. J Neurophysiol 96:1135–1140
Bergquist AJ, Clair JM, Collins DF (2011) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared to a muscle belly: triceps surae. J Appl Physiol 110:627–637
Bigland-Ritchie B, Zijdewind I, Thomas CK (2000) Muscle fatigue induced by stimulation with and without doublets. Muscle Nerve 23:1348–1355
Binder-Macleod SA, Clamann HP (1989) Force output of cat motor units stimulated with trains of linearly varying frequency. J Neurophysiol 61:208–217
Binder-Macleod SA, Scott WB (2001) Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 172:195–203
Blair EA, Erlanger J (1933) A comparison of the characteristics of axons through their individual electrical responses. Am J Physiol 106:524–564
Blickenstorfer A, Kleiser R, Keller T, Keisker B, Meyer M, Riener R, Kollias S (2008) Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI. Hum Brain Mapp 3:963–975
Blouin JS, Walsh LD, Nickolls P, Gandevia SC (2009) High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles. J Appl Physiol 106:370–377
Boerio D, Jubeau M, Zory R, Maffiuletti NA (2005) Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 37:973–978
Buchthal F, Schmalbruch H (1970) Contraction times of twitches evoked by H-reflexes. Acta Physiol Scand 80:378–382
Burke D, Schiller HH (1976) Discharge pattern of single motor units in the tonic vibration reflex of human triceps surae. J Neurol Neurosurg Psychiatry 39:729–741
Burke D, Gandevia SC, McKeon B (1983) The afferent volleys responsible for spinal proprioceptive reflexes in man. J Physiol 339:535–552
Burke D, Kiernan MC, Bostock H (2001) Excitability of human axons. Clin Neurophysiol 112:1575–1585
Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R (1997) Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord 35:86–91
Clair JM, Anderson-Reid JM, Graham CM, Collins DF (2011) Post-activation depression and recovery of reflex transmission during repetitive electrical stimulation of the human tibial nerve. J Neurophysiol [Epub ahead of Print]
Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123
Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109
Collins DF, Burke D, Gandevia SC (2001) Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci 21:4059–4065
Collins DF, Burke D, Gandevia SC (2002a) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538:289–301
Collins DF, Gorassini M, Bennett D, Burke D, Gandevia SC (2002b) Recent evidence for plateau potentials in human motoneurones. Adv Exp Med Biol 508:227–235
Conforto AB, Kaelin-Lang A, Cohen LG (2002) Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol 51:122–125
Crone C, Nielsen J (1989) Methodological implications of the post activation depression of the soleus H-reflex in man. Exp Brain Res 78:28–32
Crone C, Nielsen J, Petersen N, Ballegaard M, Hultborn H (1994) Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain 117(Pt 5):1161–1168
Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 1:170–176
Deuchert M, Ruben J, Schwiemann J, Meyer R, Thees S, Krause T, Blankenburg F, Villringer K, Kurth R, Curio G, Villringer A (2002) Event-related fMRI of the somatosensory system using electrical finger stimulation. NeuroReport 13:365–369
Doherty TJ, Brown WF (1993) The estimated numbers and relative sizes of thenar motor units as selected by multiple point stimulation in young and older adults. Muscle Nerve 16:355–366
Dudley-Javoroski S, Shields RK (2008) Muscle and bone plasticity after spinal cord injury: review of adaptations to disuse and to electrical muscle stimulation. J Rehabil Res Dev 45:283–296
Everaert DG, Thompson AK, Chong SL, Stein RB (2010) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24:168–177
Feiereisen P, Duchateau J, Hainaut K (1997) Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior. Exp Brain Res 114:117–123
Field-Fote EC (2004) Electrical stimulation modifies spinal and cortical neural circuitry. Exerc Sport Sci Rev 32:155–160
Fraser C, Power M, Hamdy S, Rothwell J, 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
Frigon A, Thompson CK, Johnson MD, Manuel M, Hornby TG, Heckman CJ (2011) Extra forces evoked during electrical stimulation of the muscle or its nerve are generated and modulated by a length-dependent intrinsic property of muscle in humans and cats. J Neurosci 31:5579–5588
Gondin J, Giannesini B, Vilmen C, Dalmasso C, le Fur Y, Cozzone PJ, Bendahan D (2010) Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation. Muscle Nerve 41:667–678
Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, Pellegrino MA, Bottinelli R (2011) Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 110:433–450
Gorman PH, Mortimer JT (1983) The effect of stimulus parameters on the recruitment characteristics of direct nerve stimulation. IEEE Trans Biomed Eng 30:407–414
Gottlieb GL, Agarwal GC (1976) Extinction of the Hoffmann reflex by antidromic conduction. Electroencephalogr Clin Neurophysiol 41:19–24
Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85:358–364
Gregory CM, Dixon W, Bickel CS (2007) Impact of varying pulse frequency and duration on muscle torque production and fatigue. Muscle Nerve 35:504–509
Grill WM, Mortimer JT (1996) The effect of stimulus pulse duration on selectivity of neural stimulation. IEEE Trans Biomed Eng 43:161–166
Hagbarth KE, Eklund G (1966) Tonic vibration reflexes (TVR) in spasticity. Brain Res 2:201–203
Hamdy S, Rothwell JC, Aziz Q, Singh KD, Thompson DG (1998) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1:64–68
Henneman E (1957) Relation between size of neurons and their susceptibility to discharge. Science 126:1345–1347
Hoffman LR, Field-Fote EC (2007) Cortical reorganization following bimanual training and somatosensory stimulation in cervical spinal cord injury: a case report. Phys Ther 87:208–223
Hortobagyi T, Scott K, Lambert J, Hamilton G, Tracy J (1999) Cross-education of muscle strength is greater with stimulated than voluntary contractions. Mot Control 3:205–219
Hugon M (1973) Methodology of the Hoffmann Reflex in Man. New Dev Electromyogr Clin Neurophysiol 3:277–293
Jacobs PL, Nash MS (2004) Exercise recommendations for individuals with spinal cord injury. Sports Med 34:727–751
Jubeau M, Gondin J, Martin A, Sartorio A, Maffiuletti NA (2007) Random motor unit activation by electrostimulation. Int J Sports Med 28:901–904
Jusic A, Baraba R, Bogunovic A (1995) H-reflex and F-wave potentials in leg and arm muscles. Electromyogr Clin Neurophysiol 35:471–478
Kasai T, Kawanishi M, Yahagi S (1992) The effects of wrist muscle vibration on human voluntary elbow flexion-extension movements. Exp Brain Res 90:217–220
Kesar T, Chou LW, Binder-Macleod SA (2007) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 4:662–671
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
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 159:491–500
Kiernan MC, Mogyoros I, Burke D (1996) Differences in the recovery of excitability in sensory and motor axons of human median nerve. Brain 119:1099–1105
Kim CK, Bangsbo J, Strange S, Karpakka J, Saltin B (1995) Metabolic response and muscle glycogen depletion pattern during prolonged electrically induced dynamic exercise in man. Scand J Rehabil Med 27:51–58
Klakowicz PM, Baldwin ER, Collins DF (2006) Contribution of m-waves and h-reflexes to contractions evoked by tetanic nerve stimulation in humans. J Neurophysiol 96:1293–1302
Knaflitz M, Merletti R, de Luca CJ (1990) Inference of motor unit recruitment order in voluntary and electrically elicited contractions. J Appl Physiol 68:1657–1667
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 153:366–377
Knight CA, Kamen G (2005) Superficial motor units are larger than deeper motor units in human vastus lateralis muscle. Muscle Nerve 31:475–480
Lagerquist O, Collins DF (2008) Stimulus pulse-width influences H-reflex recruitment but not H(max)/M(max) ratio. Muscle Nerve 37:483–489
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 42:886–893
Lagerquist O, Walsh LD, Blouin JS, Collins DF, Gandevia SC (2009) Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation. J Appl Physiol 107:161–167
Lang AH, Vallbo ÅB (1967) Motoneuron activation by low intensity tetanic stimulation of muscle afferents in man. Exp Neurol 18:383–391
Lexell J, Henriksson-Larsen K, Sjostrom M (1983) Distribution of different fibre types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 117:115–122
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 42:101–105
Liepert J, Bauder H, Wolfgang HR, Miltner WH, Taub E, Weiller C (2000) Treatment-induced cortical reorganization after stroke in humans. Stroke 31:1210–1216
Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234
Maffiuletti NA, Zory R, Miotti D, Pellegrino MA, Jubeau M, Bottinellu R (2006) Neuromuscular adaptations to electrostimulation resistance training. Am J Phys Med Rehabil 85:167–175
Magalhaes FH, Kohn AF (2010) Vibration-induced extra torque during electrically-evoked contractions of the human calf muscles. J Neuroeng Rehabil 7:26
Major LA, Jones KE (2005) Simulations of motor unit number estimation techniques. J Neural Eng 2:17–34
Mang CS, Lagerquist O, Collins DF (2010) Changes in corticospinal excitability evoked by common peroneal nerve stimulation depend on stimulation frequency. Exp Brain Res 203:11–20
Mang CS, Clair JM, Collins DF (2011) Neuromuscular electrical stimulation has a global effect on corticospinal excitability for leg muscles and a focused effect for hand muscles. Exp Brain Res 209:355–363
McKay D, Brooker R, Giacomin P, Ridding M, Miles T (2002a) Time course of induction of increased human motor cortex excitability by nerve stimulation. NeuroReport 13:1271–1273
McKay DR, Ridding MC, Thompson PD, Miles TS (2002b) Induction of persistent changes in the organisation of the human motor cortex. Exp Brain Res 143:342–349
Mesin L, Merlo E, Merletti R, Orizio C (2010) Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle. J Electromyogr Kinesiol 20:580–589
Milner-Brown HS, Stein RB, Yemm R (1973) The orderly recruitment of human motor units during voluntary isometric contractions. J Physiol 230:359–370
Mogyoros I, Kiernan MC, Burke D (1996) Strength-duration properties of human peripheral nerve. Brain 119:439–447
Nielsen J, Kagamihara Y, Crone C, Hultborn H (1992) Central facilitation of Ia inhibition during tonic ankle dorsiflexion revealed after blockade of peripheral feedback. Exp Brain Res 88:651–656
Panizza M, Nilsson J, Hallett M (1989) Optimal stimulus duration for the H reflex. Muscle Nerve 12:576–579
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. Electroencephalogr Clin Neurophysiol 85:22–29
Perez MA, Field-Fote EC, Floeter MK (2003) Patterned sensory stimulation induces plasticity in reciprocal Ia inhibition in humans. J Neurosci 23:2014–2018
Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 30:67–80
Pitcher JB, Ridding MC, Miles TS (2003) Frequency-dependent, bi-directional plasticity in motor cortex of human adults. Clin Neurophysiol 114:1265–1271
Place N, Casartelli N, Glatthorn JF, Maffiuletti NA (2010) Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve 42:894–900
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
Round JM, Barr FM, Moffat B, Jones DA (1993) Fibre areas and histochemical fibre types in the quadriceps muscle of paraplegic subjects. J Neurol Sci 116:207–211
Roy FD, Gorassini MA (2008) Peripheral sensory activation of cortical circuits in the leg motor cortex of man. J Physiol 17:4091–4105
Schindler-Ivens S, Shields RK (2000) Low frequency depression of H-reflexes in humans with acute and chronic spinal-cord injury. Exp Brain Res 133:233–241
Selkowitz DM (1985) Improvement in isometric strength of the quadriceps femoris muscle after training with electrical stimulation. Phys Ther 65:186–196
Sheffler LR, Chae J (2007) Neuromuscular electrical stimulation in neurorehabilitation. Muscle Nerve 35:562–590
Shields RK (1995) Fatigability, relaxation properties, and electromyographic responses of the human paralyzed soleus muscle. J Neurophysiol 73:2195–2206
Shields RK (2002) Muscular, skeletal, and neural adaptations following spinal cord injury. J Orthop Sports Phys Ther 32:65–74
Solomonow M (1984) External control of the neuromuscular system. IEEE Trans Biomed Eng 31:752–763
Spiegel J, Tintera J, Gawehn J, Stoeter P, Treede RD (1999) Functional MRI of human primary somatosensory and motor cortex during median nerve stimulation. Clin Neurophysiol 110:47–52
Stein RB, Gordon T, Jefferson J, Sharfenberger A, Yang JF, de Zepetnek JT, Belanger M (1992) Optimal stimulation of paralyzed muscle after human spinal cord injury. J Appl Physiol 72:1393–1400
Stein RB, Everaert DG, Thompson AK, Chong SL, Whittaker M, Robertson J, Kuether G (2010) Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabil Neural Repair 24:152–167
Stevens JE, Mizner RL, Snyder-Mackler L (2004) Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series. J Ortho Sports Phys Ther 34:21–29
Stotz PJ, Bawa P (2001) Motor unit recruitment during lengthening contractions of human wrist flexors. Muscle Nerve 24:1535–1541
Theurel J, Lepers R, Pardon L, Maffiuletti NA (2007) Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol 157:341–347
Thomas CK, Nelson G, Than L, Zijdewind I (2002) Motor unit activation order during electrically evoked contractions of paralyzed or partially paralyzed muscles. Muscle Nerve 25:797–804
Thompson AK, Estabrooks KL, Chong S, Stein RB (2009) Spinal reflexes in ankle flexor and extensor muscles after chronic central nervous system lesions and functional electrical stimulation. Neurorehabil Neural Repair 23:133–142
Trimble MH, Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273–280
van Boxtel A (1986) Differential effects of low-frequency depression, vibration-induced inhibition, and posttetanic potentiation on H-reflexes and tendon jerks in the human soleus muscle. J Neurophysiol 55:551–568
Vanderthommen M, Depresseux JC, Dauchat L, Degueldre C, Croisier JL, Crielaard JM (2000) Spatial distribution of blood flow in electrically stimulated human muscle: a positron emission tomography study. Muscle Nerve 23:482–489
Vanderthommen M, Duteil S, Wary C, Raynaud JS, Leroy-Willig A, Crielaard JM, Carlier PG (2003) A comparision of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans. J Appl Physiol 94:1012–1024
Veale JL, Mark RF, Rees S (1973) Differential sensitivity of motor and sensory fibres in human ulnar nerve. J Neurol Neurosurg Psychiatry 36:75–86
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Roberto Bottinelli.
This article is published as part of the Special Issue Cluster on the XVIII Congress of the International Society of Electrophysiology and Kinesiology (ISEK 2010) that took place in Aalborg, Denmark on 16–19 June 2010.
Rights and permissions
About this article
Cite this article
Bergquist, A.J., Clair, J.M., Lagerquist, O. et al. Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111, 2409–2426 (2011). https://doi.org/10.1007/s00421-011-2087-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-011-2087-9