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Repetitive common peroneal nerve stimulation increases ankle dorsiflexor motor evoked potentials in incomplete spinal cord lesions

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Abstract

Plasticity of corticospinal tract (CST) activity likely plays a key role in motor function recovery after central nervous system (CNS) lesions. In non-injured adults, 30 min of repetitive common peroneal nerve stimulation (rCPnS) increases CST excitability by 40–50% and the effect persists for at least 30 min. The present study evaluated with transcranial magnetic stimulation (TMS) the changes in CST excitability after 30 min of rCPnS in people with foot drop due to incomplete SCI. Suprathreshold rCPnS (25 Hz, alternating 1 s on 1 s off stimulation cycle) was given for two 15-min periods, while the subject sat at rest with ankle and knee joints fixed. Before, between, and after the periods of stimulation, the tibialis anterior (TA) motor evoked potentials (MEPs) to TMS were measured at a TMS intensity that originally produced a half-maximum MEP (typically 10–20% above threshold) while the sitting subject provided 25–30% maximum voluntary TA contraction. In 10 subjects with SCI, the peak-to-peak TA MEP increased by 14 ± 3% after rCPnS and the peak increase (+21 ± 7%) occurred 15 min after the cessation of rCPnS. The TA H-reflex, measured in separate experiments in 7 subjects, did not increase after rCPnS. The results indicate that rCPnS can increase CST excitability for the TA in people with incomplete SCI, although its effects appear smaller and shorter lasting than those found in non-injured control subjects. Such short-term plasticity in the CST excitability induced by rCPnS may contribute to long-term therapeutic effects of functional electrical stimulation previously reported in people with CNS lesions.

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References

  • Andersen JB, Sinkjaer T (1999) The stretch reflex and H-reflex of the human soleus muscle during walking. Mot Control 3:151–157

    CAS  Google Scholar 

  • Ashby P, Wiens M (1989) Reciprocal inhibition following lesions of the spinal cord in man. J Physiol 414:145–157

    PubMed  CAS  Google Scholar 

  • Bajd T, Gregoric M, Vodovnik L, Benko H (1985) Electrical stimulation in treating spasticity resulting from spinal cord injury. Arch Phys Med Rehabil 66:515–517

    PubMed  CAS  Google Scholar 

  • Barbeau H, Ladouceur M, Mirbagheri MM, Kearney RE (2002) The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies. Brain Res Rev 40:274–291

    Article  PubMed  Google Scholar 

  • Bennett DJ, Li Y, Harvey PJ, Gorassini M (2001) Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 86:1972–1982

    PubMed  CAS  Google Scholar 

  • Burridge J, Wood D, Taylor P, Swain I, Hagan S (1997) The effect of common peroneal nerve stimulation on quadriceps spasticity in hemiplegia. Physiotherapy 83:82–89

    Article  Google Scholar 

  • Burridge JH, Haugland M, Larsen B, Pickering RM, Svaneborg N, Iversen HK, Christensen PB, Haase J, Brennum J, Sinkjaer T (2007) Phase II trial to evaluate the ActiGait implanted drop-foot stimulator in established hemiplegia. J Rehabil Med 39:212–218

    Article  PubMed  Google Scholar 

  • Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661–3665

    Article  PubMed  CAS  Google Scholar 

  • Capaday C, Stein RB (1986) Amplitude modulation of the soleus H-reflex in the human during walking and standing. J Neurosci 6:1308–1313

    PubMed  CAS  Google Scholar 

  • Chen XY, Wolpaw JR (2002) Probable corticospinal tract control of spinal cord plasticity in the rat. J Neurophysiol 87:645–652

    PubMed  Google Scholar 

  • Chen XY, Wolpaw JR, Jakeman LB, Stokes BT (1996) Operant conditioning of H-reflex in spinal cord-injured rats. J Neurotrauma 13:755–766

    Article  PubMed  CAS  Google Scholar 

  • Chen R, Lozano AM, Ashby P (1999) Mechanism of the silent period following transcranial magnetic stimulation. Evidence from epidural recordings. Exp Brain Res 128:539–542

    Article  PubMed  CAS  Google Scholar 

  • Chen XY, Carp JS, Chen L, Wolpaw JR (2002) Corticospinal tract transection prevents operantly conditioned H-reflex increase in rats. Exp Brain Res 144:88–94

    Article  PubMed  Google Scholar 

  • Chen XY, Chen Y, Chen L, Tennissen AM, Wolpaw JR (2006) Corticospinal tract transection permanently abolishes H-reflex down-conditioning in rats. J Neurotrauma 23:1705–1712

    Article  PubMed  Google Scholar 

  • Crone C, Nielsen J, Petersen N, Ballegaard M, Hultborn H (1994) Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain 117:1161–1168

    Article  PubMed  Google Scholar 

  • Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB (2003) Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 126:495–507

    Article  PubMed  CAS  Google Scholar 

  • Delwaide PJ, Oliver E (1988) Short-latency autogenic inhibition (IB inhibition) in human spasticity. J Neurol Neurosurg Psychiatry 51:1546–1550

    Article  PubMed  CAS  Google Scholar 

  • Devanne H, Lavoie BA, Capaday C (1997) Input-output properties and gain changes in the human corticospinal pathway. Exp Brain Res 114:329–338

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Fuhr P, Agostino R, Hallett M (1991) Spinal motor neuron excitability during the silent period after cortical stimulation. Electroencephalogr Clin Neurophysiol 81:257–262

    Article  PubMed  CAS  Google Scholar 

  • Garvey MA, Ziemann U, Becker DA, Barker CA, Bartko JJ (2001) New graphical method to measure silent periods evoked by transcranial magnetic stimulation. Clin Neurophysiol 112:1451–1460

    Article  PubMed  CAS  Google Scholar 

  • Gorassini MA, Knash ME, Harvey PJ, Bennett DJ, Yang JF (2004) Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127:2247–2258

    Article  PubMed  Google Scholar 

  • Goulet C, Arsenault AB, Bourbonnais D, Laramee MT, Lepage Y (1996) Effects of transcutaneous electrical nerve stimulation on H-reflex and spinal spasticity. Scand J Rehabil Med 28:169–176

    PubMed  CAS  Google Scholar 

  • Granat MH, Ferguson AC, Andrews BJ, Delargy M (1993) The role of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injury—observed benefits during gait studies. Paraplegia 31:207–215

    PubMed  CAS  Google Scholar 

  • Grey MJ, Klinge K, Crone C, Lorentzen J, Biering-Sorensen F, Ravnborg M, Nielsen JB (2008) Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Exp Brain Res 185:189–197

    Article  PubMed  Google Scholar 

  • Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944–947

    Article  PubMed  CAS  Google Scholar 

  • Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633

    Article  PubMed  CAS  Google Scholar 

  • Katz R, Pierrot-Deseilligny E (1982) Recurrent inhibition of alpha-motoneurons in patients with upper motor neuron lesions. Brain 105:103–124

    Article  PubMed  CAS  Google Scholar 

  • 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 162:497–502

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 159:491–500

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kottink AI, Hermens HJ, Nene AV, Tenniglo MJ, Groothuis-Oudshoorn CG, IJzerman MJ (2008) Therapeutic effect of an implantable peroneal nerve stimulator in subjects with chronic stroke and footdrop: a randomized controlled trial. Phys Ther 88:437–448

    Google Scholar 

  • Krause P, Szecsi P, Straube A (2007) FES cycling reduces spastic muscle tone in a patient with multiple sclerosis. NeuroRehabilitation 22:335–337

    PubMed  Google Scholar 

  • Ladouceur M, Barbeau H (2000) Functional electrical stimulation-assisted walking for persons with incomplete spinal injuries: longitudinal changes in maximal overground walking speed. Scand J Rehabil Med 32:28–36

    Article  PubMed  CAS  Google Scholar 

  • Levin MF, Hui-Chan CW (1992) Relief of hemiparetic spasticity by TENS is associated with improvement in reflex and voluntary motor functions. Electroencephalogr Clin Neurophysiol 85:131–142

    Article  PubMed  CAS  Google Scholar 

  • Levy LM, Ziemann U, Chen R, Cohen LG (2002) Rapid modulation of GABA in sensorimotor cortex induced by acute deafferentation. Ann Neurol 52:755–761

    Article  PubMed  CAS  Google Scholar 

  • Li Y, Bennett DJ (2003) Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90:857–869

    Article  PubMed  CAS  Google Scholar 

  • Mirbagheri MM, Ladouceur M, Barbeau H, Kearney RE (2002) The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects. IEEE Trans Neural Syst Rehabil Eng 10:280–289

    Article  PubMed  Google Scholar 

  • Morita H, Crone C, Christenhuis D, Petersen NT, Nielsen JB (2001) Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain 124:826–837

    Article  PubMed  CAS  Google Scholar 

  • Morita H, Shindo M, Momoi H, Yanagawa S, Ikeda S, Yanagisawa N (2006) Lack of modulation of Ib inhibition during antagonist contraction in spasticity. Neurology 67:52–56

    Article  PubMed  CAS  Google Scholar 

  • Nielsen JB, Crone C, Hultborn H (2007) The spinal pathophysiology of spasticity–from a basic science point of view. Acta Physiol (Oxf) 189:171–180

    Article  CAS  Google Scholar 

  • Pierrot-Deseilligny E, Burke D (2005) The circuitry of the human spinal cord: its role in motor control and movement disorders. Cambridge University Press, Cambridge, UK

    Book  Google Scholar 

  • Potisk KP, Gregoric M, Vodovnik L (1995) Effects of transcutaneous electrical nerve stimulation (TENS) on spasticity in patients with hemiplegia. Scand J Rehabil Med 27:169–174

    PubMed  CAS  Google Scholar 

  • Roy FD, Yang JF, Gorassini MA (2010) Afferent regulation of leg motor cortex excitability after incomplete spinal cord injury. J Neurophysiol 103:2222–2233

    Article  PubMed  Google Scholar 

  • Schmit BD, Benz EN, Rymer WZ (2002) Reflex mechanisms for motor impairment in spinal cord injury. Adv Exp Med Biol 508:315–323

    PubMed  Google Scholar 

  • Seib TP, Price R, Reyes MR, Lehmann JF (1994) The quantitative measurement of spasticity: effect of cutaneous electrical stimulation. Arch Phys Med Rehabil 75:746–750

    PubMed  CAS  Google Scholar 

  • Shefner JM, Berman SA, Sarkarati M, Young RR (1992) Recurrent inhibition is increased in patients with spinal cord injury. Neurology 42:2162–2168

    PubMed  CAS  Google Scholar 

  • Sinkjaer T, Andersen JB, Larsen B (1996) Soleus stretch reflex modulation during gait in humans. J Neurophysiol 76:1112–1120

    PubMed  CAS  Google Scholar 

  • Sinkjaer T, Andersen JB, Nielsen JF, Hansen HJ (1999) Soleus long-latency stretch reflexes during walking in healthy and spastic humans. Clin Neurophysiol 110:951–959

    Article  PubMed  CAS  Google Scholar 

  • Solomonow M, Reisin E, Aguilar E, Baratta RV, Best R, D’Ambrosia R (1997) Reciprocating gait orthosis powered with electrical muscle stimulation (RGO II). Part II: Medical evaluation of 70 paraplegic patients. Orthopedics 20:411–418

    PubMed  CAS  Google Scholar 

  • Stein RB (1998) Assembly for functional electrical stimulation. In: Continuation in part US patent 5814093

  • Stein RB, Belanger M, Wheeler G, Wieler M, Popovic DB, Prochazka A, Davis LA (1993a) Electrical systems for improving locomotion after incomplete spinal cord injury: an assessment. Arch Phys Med Rehabil 74:954–959

    Article  PubMed  CAS  Google Scholar 

  • Stein RB, Yang JF, Belanger M, Pearson KG (1993b) Modification of reflexes in normal and abnormal movements. Prog Brain Res 97:189–196

    Article  PubMed  CAS  Google Scholar 

  • Stein RB, Chong S, Everaert DG, Rolf R, Thompson AK, Whittaker M, Robertson J, Fung J, Preuss R, Momose K, Ihashi K (2006) A multicenter trial of a footdrop stimulator controlled by a tilt sensor. Neurorehabil Neural Repair 20:371–379

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Taylor PN, Burridge JH, Dunkerley AL, Wood DE, Norton JA, Singleton C, Swain ID (1999a) Clinical use of the Odstock dropped foot stimulator: its effect on the speed and effort of walking. Arch Phys Med Rehabil 80:1577–1583

    Article  PubMed  CAS  Google Scholar 

  • Taylor PN, Burridge JH, Dunkerley AL, Wood DE, Norton JA, Singleton C, Swain ID (1999b) Clinical use of the Odstock dropped foot stimulator: its effect on the speed and effort of walking. Arch Phys Med Rehabil 80:1577–1583

    Article  PubMed  CAS  Google Scholar 

  • Thompson AK, Doran B, Stein RB (2006) Short-term effects of functional electrical stimulation on spinal excitatory and inhibitory reflexes in ankle extensor and flexor muscles. Exp Brain Res 170:216–226

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Uysal H, Larsson LE, Efendi H, Burke D, Ertekin C (2009) Medium-latency reflex response of soleus elicited by peroneal nerve stimulation. Exp Brain Res 193:275–286

    Article  PubMed  Google Scholar 

  • Wieler M, Stein RB, Ladouceur M, Whittaker M, Smith AW, Naaman S, Barbeau H, Bugaresti J, Aimone E (1999) Multicenter evaluation of electrical stimulation systems for walking. Arch Phys Med Rehabil 80:495–500

    Article  PubMed  CAS  Google Scholar 

  • Wu T, Sommer M, Tergau F, Paulus W (2000) Modification of the silent period by double transcranial magnetic stimulation. Clin Neurophysiol 111:1868–1872

    Article  PubMed  CAS  Google Scholar 

  • Yang JF, Fung J, Edamura M, Blunt R, Stein RB, Barbeau H (1991) H-reflex modulation during walking in spastic paretic subjects. Can J Neurol Sci 18:443–452

    PubMed  CAS  Google Scholar 

  • Ziemann U, Netz J, Szelenyi A, Homberg V (1993) Spinal and supraspinal mechanisms contribute to the silent period in the contracting soleus muscle after transcranial magnetic stimulation of human motor cortex. Neurosci Lett 156:167–171

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Corwell B, Cohen LG (1998a) Modulation of plasticity in human motor cortex after forearm ischemic nerve block. J Neurosci 18:1115–1123

    PubMed  CAS  Google Scholar 

  • Ziemann U, Hallett M, Cohen LG (1998b) Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18:7000–7007

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Drs. Richard B. Stein and Francois Roy for helpful comments on the manuscript. This work was supported by New York State Spinal Cord Injury Research Trust (C023685).

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Correspondence to Aiko K. Thompson.

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Thompson, A.K., Lapallo, B., Duffield, M. et al. Repetitive common peroneal nerve stimulation increases ankle dorsiflexor motor evoked potentials in incomplete spinal cord lesions. Exp Brain Res 210, 143–152 (2011). https://doi.org/10.1007/s00221-011-2607-1

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