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Mini-review article: the role of spinal reciprocal inhibition and intracortical inhibition in functional recovery from stroke

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A Correction to this article was published on 28 July 2020

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Abstract

Spinal reciprocal inhibition (RI) and intracortical inhibition are important physiological mechanisms for voluntary movement control and functional recovery of voluntary movement in patients with stroke. Spasticity, which impairs motor performance, is one of the major manifestations of stroke. RI may be involved in reducing spasticity. This might allow finger extension, and, therefore, better hand function by reducing co-contraction with finger extensors. One potential mechanism of functional reorganization of the motor cortex is that pre-existing masking pathways are unmasked by decreased intracortical inhibition. The inhibitory neurotransmitter GABA plays an important role in this process. Changes in RI might be mediated through unmasking of cortical pathways through decreased inhibition, with the neurotransmitter GABA. These changes can be assessed using short-latency intracortical inhibition (SICI) and RI. Functional recovery in the chronic phase of stroke induced by rehabilitation was accompanied by SICI and spinal RI changes. Cortical reorganization and spinal plasticity might play important roles in functional recovery induced by rehabilitation, even in patients with chronic severe hemiparesis. This review aims to provide a focused overview of neuroplasticity of spinal RI and intracortical inhibition associated with functional motor recovery from stroke.

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Change history

  • 28 July 2020

    In the original publication of the article, it was published under the title ‘Mini-review article: the role of spinal reciprocal inhibition and intracortical inhibition in functional recovery from stroke’.

References

  • Berardelli A, Inghilleri M, Rothwell JC, Romeo S, Curra A, Gilio F, Modungo N, Manfredi M (1998) Facilitation of muscle evoked responses after repetitive cortical stimulation in man. Exp Brain Res 122:79–84

    Article  CAS  Google Scholar 

  • Bohannon RW, Smith MB (1987) Interrater reliability of modified Ashworth scale of muscle spasticity. Phys Ther 67:206–207

    Article  CAS  Google Scholar 

  • Chen Y, Chen XY, Jakeman LB, Schalk G, Stokes BT, Wolpaw JR (2005) The interaction of a new motor skill and an old one: H reflex conditioning and locomotion in rats. J Neurosci 25:6898–6906

    Article  CAS  Google Scholar 

  • Clarkson AN, Huang BS, MacIsaac SE, Mody I, Carmichael ST (2010) Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature 468:305–309

    Article  CAS  Google Scholar 

  • Day BL, Marsden CD, Rothwell OJA, JC. (1984) Reciprocal inhibition between the muscles of human forearm. J Physiol 349:519–534

    Article  CAS  Google Scholar 

  • Di Pino G, Pellegrino G, Assenza G, Capone F, Ferreri F, Formica D, Ranieri F, Tombini M, Ziemann U, Rothwell JC, Di Lazzaro V (2014) Modulation of brain plasticity in stroke: a novel model for neurorehabilitation. Nat Rev Neurol 10:597–608

    Article  Google Scholar 

  • Dobkin BH (2005) Rehabilitation after stroke. N Engl J Med 352:1677–1684

    Article  CAS  Google Scholar 

  • Edwards MJ, Huang YZ, Wood NW, Rothwell JC, Bhatia KP (2003) Different pattern of electrophysiological deficits in manifesting and non-manifesting carriers of the DYT1 gene mutation. Brain 126(9):2074–2080

    Article  Google Scholar 

  • Fujiwara T, Liu M, Hase K, Tanaka N, Hara Y (2004) Electrophysiological and clinical assessment of a simple wrist-hand splint for patients with chronic spastic hemiparesis secondary to stroke. Electromyogr Clin Neurophysiol 44:423–429

    CAS  PubMed  Google Scholar 

  • Fujiwara T, Kasashima Y, Honaga K, Muraoka Y, Tsuji T, Osu R, Hase K, Masakado Y, Liu M (2009) Motor improvement and corticospinal modulation induced by hybrid assistive neuromuscular dynamic stimulation (HANDS) therapy in patients with chronic stroke. Neurorehabil Neural Repair 23:125–132

    Article  Google Scholar 

  • Fujiwara T, Tsuji T, Honaga K, Hase K, Ushiba J, Liu M (2011) Transcranial direct current stimulation modulates the spinal plasticity induced with patterned electrical stimulation. Clin Neurophysiol 122:1834–1837

    Article  Google Scholar 

  • Fujiwara T, Honaga K, Kawakami M, Nishimoto A, Abe K, Mizuno K, Kodama M, Masakado Y, Tsuji T, Liu M (2015) Modulation of cortical and spinal inhibition with functional recovery of upper extremity motor function among patients with chronic stroke. Restor Neurol Neurosci 33:883–894

    CAS  PubMed  Google Scholar 

  • Honaga K, Fujiwara T, Tsuji T, Hase K, Ushiba J, Liu M (2013) State of intracortical inhibitory interneuron activity in patients with chronic stroke. Clin Neurophysiol 124:364–370

    Article  Google Scholar 

  • Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206

    Article  CAS  Google Scholar 

  • Huang YZ, Trender-Gerhard I, Edwards MJ, Mir P, Rothwell JC, Bhaita KP (2006) Motor system inhibition in dopa-responsive dystonia and its modulation by treatment. Neurology 66:1088–1090

    Article  Google Scholar 

  • Jackson A, Zimmermann JB (2012) Neural interfaces for the brain and spinal cord-restoring motor function. Nat Rev Neurol 8:690–699

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kheder A, Nair KPS (2012) Spasticity: Pathophysiology, evaluation and management. Pract Neurol 12:289–298

    Article  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    Article  CAS  Google Scholar 

  • Kumru H, Murillo N, Samso JV, Valls-Sole J, Edwards D, Pelayo R, Valero-Cabre A, Tormos JM, Pascual-Leone A (2010) Reduction of spasticity with repetitive transcranial magnetic stimulation in patients with spial cord injury. Neurorehabil Neural Repair 24:435–441

    Article  Google Scholar 

  • Liepert J, Storch P, Fritsch A, Weiller C (2000) Motor cortex disinhibition in acute stroke. Clin Neurophysiol 111:671–676

    Article  CAS  Google Scholar 

  • Masakado Y, Muraoka Y, Tomita Y, Chino N (2001) The effect of transcranial magnetic stimulation on reciprocal inhibition in the human leg. Electromyogr Clin Neurophysiol 41:429–432

    CAS  PubMed  Google Scholar 

  • Mizuno Y, Tanaka R, Yanagisawa N (1971) Reciprocal group I inhibition on triceps surae motoneurones in man. J Neurophysiol 34:1010–1017

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Nakashima K, Rothwell JC, Day BL, Thompson PD, Shannon K, Marsden CD (1989) Reciprocal inhibition between forearm muscles in patients with writer’s cramp and other occupational cramps, symptomatic hemidystonia and hemiparesis due to stroke. Brain 112:681–697

    Article  Google Scholar 

  • Nielsen JB (2004) Sensorimotor integration at spinal level as a basis for muscle coordination during voluntary movement in humans. J Appl Physiol 96:1961–1967

    Article  Google Scholar 

  • Nielsen JB (2016) Human spinal motor control. Annu Rev Neurosci 39:81–101

    Article  CAS  Google Scholar 

  • Nielsen J, Peterson N, Deuschi G, Ballegaard M (1993) Task-related changes in the effect of magnetic brain stimulation on spinal neurons in man. J Physiol 471:223–243

    Article  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 

  • Pandyan AD, Gregoric M, Barnes MP, Wood D, Van Wijck F, Burridge J, Hermens H, Johnson GR (2005) Spasticity: clinical perceptions, neurological realities and meaningful measurement. Disabil Rehabil 27:2–6

    Article  CAS  Google Scholar 

  • Perez MA, Field-Fote EC, Floeter MK (2003) Patterned sensory stimulation induced plasticity in reciprocal Ia inhibition in humans. J Neurosci 23:2014–2018

    Article  CAS  Google Scholar 

  • Perez MA, Lungholt BK, Nielsen JB (2005) Short-term adaptations in spinal cord circuits evoked by repetitive transcranial magnetic stimulation: possible underlying mechanisms. Exp Brain Res 162:202–212

    Article  Google Scholar 

  • Rothwell JC, Day BL, Berardelli A, Marsden CD (1984) Effects of motor cortex stimulation on spinal interneurons in intact man. Exp Brain Res 54:382–384

    Article  CAS  Google Scholar 

  • Sanger TD, Garg RR, Chen R (2001) Interactions between two different inhibitory systems in the human motor cortex. J Physiol 530:307–317

    Article  CAS  Google Scholar 

  • Sherrington CS (1906) The integrative action of the nervous system. Yale University Pres, New Haven

    Google Scholar 

  • Shimizu T, Hosaki A, Hino T, Sato M, Komori T, Hirai S, Rossini PM (2002) Motor cortical disinhibition in the unaffected hemisphere after unilateral cortical stroke. Brain 125:1896–1907

    Article  Google Scholar 

  • Swayne OB, Rothwell JC, Ward NS, Greenwood RJ (2008) Stages of motor output reorganization after hemispheric stroke suggested by longitudinal studies of cortical physiology. Cereb Cortex 18:1909–1922

    Article  Google Scholar 

  • Tanaka R (1974) Reciprocal Ia inhibition during voluntary movements in man. Exp Brain Res 21:529–540

    Article  CAS  Google Scholar 

  • Yamaguchi T, Fujiwara T, Tsai YA, Tang SC, Kawakami M, Mizuno K, Kodama M, Masakado Y, Liu M (2016) The effects of anodal transcranial direct current stimulation and patterned electrical stimulation on spinal inhibitory interneurons and motor function in patients with spinal cord injury. Exp Brain Res 234:1469–1478

    Article  Google Scholar 

  • Yamaguchi T, Fujiwara T, Lin SC, Takahashi Y, Hatori K, Liu M, Huang YZ (2018) Priming intermittent theta burst transcranial magnetic stimulation promotes spinal plasticity induced by peripheral patterned electrical stimulation. Front Neurosci 12:508. https://doi.org/10.3389/fnins.2018.00508

    Article  PubMed  PubMed Central  Google Scholar 

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Correspondence to Toshiyuki Fujiwara.

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Communicated by Sven Bestmann.

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Fujiwara, T. Mini-review article: the role of spinal reciprocal inhibition and intracortical inhibition in functional recovery from stroke. Exp Brain Res 238, 1701–1705 (2020). https://doi.org/10.1007/s00221-020-05849-0

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  • DOI: https://doi.org/10.1007/s00221-020-05849-0

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