Abstract
Study design:
Randomized, double-blind, crossover, sham-controlled trial.
Objectives:
Repetitive transcranial magnetic stimulation (rTMS) over the primary motor cortex (M1) leads to a significant reduction of spasticity in subjects with spinal cord injury (SCI), but the physiological basis of this effect is still not well understood. The purpose of this study was to evaluate the disynaptic reciprocal Ia inhibition of soleus motoneurons in SCI patients.
Setting:
Department of Neurology, Merano, Italy and TMS Laboratory, Paracelsus Medical University, Salzburg, Austria.
Methods:
Nine subjects with incomplete cervical or thoracic SCI received 5 days of daily sessions of real or sham rTMS applied over the contralateral M1. We compared the reciprocal inhibition, the Modified Ashworth Scale and the Spinal Cord Injury Assessment Tool for Spasticity at baseline, after the last session and 1 week later in the real rTMS and sham stimulation groups.
Results:
We found that real rTMS significantly reduced lower limb spasticity and restored the impaired excitability in the disynaptic reciprocal inhibitory pathway.
Conclusions:
In a small proof-of-concept study, rTMS strengthened descending projections between the motor cortex and inhibitory spinal interneuronal circuits. This reversed a defect in reciprocal inhibition after SCI, and reduced leg spasticity.
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References
Valero-Cabre A, Oliveri M, Gangitano M, Pascual-Leone A . Modulation of spinal cord excitability by subthreshold repetitive transcranial magnetic stimulation of the primary motor cortex in humans. Neuroreport 2001; 12: 3845–3848.
Centonze D, Koch G, Versace V, Mori F, Rossi S, Brusa L et al. Repetitive transcranial magnetic stimulation of the motor cortex ameliorates spasticity in multiple sclerosis. Neurology 2007; 68: 1045–1050.
Valle AC, Dionisio K, Pitskel NB, Pascual-Leone A, Orsati F, Ferreira MJ et al. Low and high frequency repetitive transcranial magnetic stimulation for the treatment of spasticity. Dev Med Child Neurol 2007; 49: 534–538.
Kumru H, Murillo N, Samso JV, Valls-Sole J, Edwards D, Pelayo R et al. Reduction of spasticity with repetitive transcranial magnetic stimulation in patients with spinal cord injury. Neurorehabil Neural Repair 2010; 24: 435–441.
Crone C, Hultborn H, Jespersen B, Nielsen J . Reciprocal Ia inhibition between ankle flexors and extensors in man. J Physiol 1987; 389: 163–185.
Crone C, Nielsen J . Central control of disynaptic reciprocal inhibition in humans. Acta Physiol Scand 1994; 152: 351–363.
Marino RJ, Barros T, Biering-Sorensen F, Burns SP, Donovan WH, Graves DE et alASIA Neurological Standards Committee. International standards for neurological classification of spinal cord injury. J Spinal Cord Med 2002; 26: S50–S56.
Bohannon RW, Smith MB . Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys Ther 1987; 67: 206–207.
Benz EN, Hornby TG, Bode RK, Scheidt RA, Schmit BD . A physiologically based clinical measure for spastic reflexes in spinal cord injury. Arch Phys Med Rehabil 2005; 86: 52–59.
Wellek S, Blettner M . On the proper use of the crossover design in clinical trials: Part 18 of a series on evaluation of scientific publications. Dtsch Arztebl Int 2012; 109: 276–281.
Cardillo G MyFriedman: Friedman test for non parametric two way analysis of variance. Matlab Central File exchange. Accessed online on 18 September 2013.
Benjamini Y, Hochberg Y . Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 1995; 57: 289–300.
Peinemann A, Reimer B, Löer C, Quartarone A, Münchau A, Conrad B et al. Long-lasting increase in corticospinal excitability after 1800 pulses of subtheshold 5 Hz repetitive TMS to the primary motor cortex. Clin Neurophysiol 2004; 115: 1519–1526.
Yanagisawa N, Tanaka R, Ito Z . Reciprocal Ia inhibition in spastic hemiplegia of man. Brain 1976; 99: 555–574.
Nakashima K, Rothwell JC, Day BL, Thompson PD, Shannon K, Marsden CD . Reciprocal inhibition between forearm muscles in patients with writer’s cramp and other occupational cramps, symptomatic hemidystonia and hemiparesis due to stroke. Brain 1989; 112: 681–697.
Crone C, Nielsen J, Petersen N, Ballegaard M, Hultborn H . Disynaptic reciprocal inhibition of ankle extensors in spastic patients. Brain 1994; 117: 1161–1168.
Morita H, Crone C, Christenhuis D, Petersen NT, Nielsen JB . Modulation of presynaptic inhibition and disynaptic reciprocal Ia inhibition during voluntary movement in spasticity. Brain 2001; 124: 826–837.
Crone C, Johnsen LL, Biering-Sorensen F, Nielsen JB . Appearance of reciprocal facilitation of ankle extensors from ankle flexors in patients with stroke or spinal cord injury. Brain 2003; 126: 495–507.
Cowan JMA, Day BL, Marsden C, Rothwell JC . The effect of percutaneous motor cortex stimulation on H reflexes in muscles of the arm and leg in intact man. J Physiol 1986; 377: 333–347.
Iles JF, Pisini JV . Cortical modulation of transmission in spinal reflex pathways of man. J Physiol 1992; 455: 425–446.
Nielsen J, Petersen N . Evidence favouring different descending pathways to soleus motoneurones activated by magnetic brain stimulation in man. J Physiol 1995; 486: 779–788.
Petersen N, Christensen LOD, Morita H, Sinkjær T, Nielsen J . Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man. J Physiol 1998; 512: 267–276.
Jankowska E, Tanaka R . Neuronal mechanism of the disynaptic inhibition evoked in primate spinal motoneurones from the corticospinal tract. Brain Res 1974; 751: 163–166.
Jankowska E, Padel Y, Tanaka R . Disynaptic inhibition of spinal motoneurones from the motor cortex in the monkey. J Physiol 1976; 258: 467–487.
Matsuyama K, Mori F, Nakajima K, Drew T, Aoki M, Mori S . Locomotor role of the corticoreticular-spinal interneuronal system. Prog Brain Res 2004; 143: 239–249.
Zaaimi B, Edgley SA, Soteropoulos DS, Baker SN . Changes in descending motor pathway connectivity after corticospinal tract lesion in macaque monkey. Brain 2012; 135: 2277–2289.
Eccles JC, Fatt P, Landgren S . The inhibitory pathway to motoneurones. Prog Neurobiol 1956; 2: 72–82.
Hultborn H, Illert M, Santini M . Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways. Acta Physiol Scand 1976; 96: 368–391.
Lundgren A, Voorhoeve P . Effects from the pyramidal tract on spinal reflex arcs. Acta Physiol Scand 1962; 56: 201–219.
Lundberg A . Supraspinal control of transmission in reflex paths to motoneurones and primary afferents. Prog Brain Res 1964; 12 (C): 197–221.
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Nardone, R., Höller, Y., Thomschewski, A. et al. rTMS modulates reciprocal inhibition in patients with traumatic spinal cord injury. Spinal Cord 52, 831–835 (2014). https://doi.org/10.1038/sc.2014.136
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DOI: https://doi.org/10.1038/sc.2014.136
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