Alteration of cortical but not spinal inhibitory circuits in idiopathic scoliosis

. 2022 Mar ; 45 (2) : 186-193. [epub] 20200323

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32202478

Background: The pathogenesis of adolescent idiopathic scoliosis (AIS), including the role of brain and spinal inhibitory circuits, is still poorly elucidated. The aim of this study was to identify which central inhibitory mechanisms are involved in the pathogenesis of AIS.Design: A prospective neurophysiological study, using a battery of neurophysiological tests, such as cutaneous (CuSP) and cortical (CoSP) silent periods, motor evoked potentials (MEP) and paired-pulse transcranial magnetic stimulation (ppTMS).Settings: Neurophysiological laboratory.Participants: Sixteen patients with AIS (14 females, median age 14.4) and healthy controls.Outcome measures: MEPs were obtained after transcranial magnetic stimulation (TMS) and recorded from the abductor pollicis muscle (APB). ppTMS was obtained at interval ratios (ISI) of 1, 2, 3, 6, 10, 15 and 20 ms. The cortical silent period (CoSP) was recorded from the APB. The cutaneous silent period (CuSP) was measured after painful stimuli delivered to the thumb while the subjects maintained voluntary contraction of the intrinsic hand muscles. The data were analyzed and compared with those from healthy subjects.Results: The CoSP duration was significantly prolonged in AIS patients. A significantly higher amplitude of ppTMS for ISI was found in all AIS patients, without remarkable left-right side differences. No significant difference in MEP latency or amplitude nor in the CuSP duration was obtained.Conclusion: Our observation demonstrates evidence of central nervous system involvement in adolescent idiopathic scoliosis (AIS). Lower intracortical inhibition, higher motor cortex excitability, and preserved spinal inhibitory circuits are the main findings of this study. A possible explanation of these changes could be attributed to impaired sensorimotor integration predominantly at the cortical level.

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Kouwenhoven JW, Castelein RM.. The pathogenesis of adolescent idiopathic scoliosis: review of the literature. Spine (Phila Pa 1976). 2008;33(26):2898–908. doi: 10.1097/BRS.0b013e3181891751 PubMed DOI

Fidler MW, Jowett RL.. Muscle imbalance in the aetiology of scoliosis. J Bone Joint Surg Br. 1976;58(2):200–1. doi: 10.1302/0301-620X.58B2.932082 PubMed DOI

Mannion AF, Meier M, Grob D, Muntener M.. Paraspinal muscle fibre type alterations associated with scoliosis: an old problem revisited with new evidence. Eur Spine J. 1998;7(4):289–93. doi: 10.1007/s005860050077 PubMed DOI PMC

Burwell RG, Aujla RK, Grevitt MP, Dangerfield PH, Moulton A, Randell TL, et al. . Pathogenesis of adolescent idiopathic scoliosis in girls - a double neuro-osseous theory involving disharmony between two nervous systems, somatic and autonomic expressed in the spine and trunk: possible dependency on sympathetic nervous system and hormones with implications for medical therapy. Scoliosis. 2009;4:24. doi: 10.1186/1748-7161-4-24 PubMed DOI PMC

Girardo M, Bettini N, Dema E, Cervellati S.. The role of melatonin in the pathogenesis of adolescent idiopathic scoliosis (AIS). Eur Spine J. 2011;20(Suppl 1):S68–74. doi: 10.1007/s00586-011-1750-5 PubMed DOI PMC

Chu WC, Lam WM, Ng BK, Tze-Ping L, Lee KM, Guo X, et al. . Relative shortening and functional tethering of spinal cord in adolescent scoliosis - result of asynchronous neuro-osseous growth, summary of an electronic focus group debate of the IBSE. Scoliosis. 2008;3:8. doi: 10.1186/1748-7161-3-8 PubMed DOI PMC

Chu WC, Man GC, Lam WW, Yeung BH, Chau WW, Ng BK, et al. . Morphological and functional electrophysiological evidence of relative spinal cord tethering in adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 2008;33(6):673–80. doi: 10.1097/BRS.0b013e318166aa58 PubMed DOI

Domenech J, Garcia-Marti G, Marti-Bonmati L, Barrios C, Tormos JM, Pascual-Leone A.. Abnormal activation of the motor cortical network in idiopathic scoliosis demonstrated by functional MRI. Eur Spine J. 2011;20(7):1069–78. doi: 10.1007/s00586-011-1776-8 PubMed DOI PMC

Domenech J, Tormos JM, Barrios C, Pascual-Leone A.. Motor cortical hyperexcitability in idiopathic scoliosis: could focal dystonia be a subclinical etiological factor? Eur Spine J. 2010;19(2):223–30. doi: 10.1007/s00586-009-1243-y PubMed DOI PMC

Stetkarova I, Zamecnik J, Bocek V, Vasko P, Brabec K, Krbec M.. Electrophysiological and histological changes of paraspinal muscles in adolescent idiopathic scoliosis. Eur Spine J. 2016;25(10):3146–53. doi: 10.1007/s00586-016-4628-8 PubMed DOI

Chau WW, Chu WC, Lam TP, Ng BK, Fu LL, Cheng JC.. Anatomical origin of abnormal somatosensory-evoked potential (SEP) in adolescent idiopathic scoliosis with different curve severity and correlation with cerebellar tonsillar level determined by MRI. Spine (Phila Pa 1976). 2016;41(10):E598–604. doi: 10.1097/BRS.0000000000001345 PubMed DOI

Chen Z, Qiu Y, Ma W, Qian B, Zhu Z.. Comparison of somatosensory evoked potentials between adolescent idiopathic scoliosis and congenital scoliosis without neural axis abnormalities. Spine J. 2014;14(7):1095–8. doi: 10.1016/j.spinee.2013.07.465 PubMed DOI

Lee RK, Griffith JF, Leung JH, Chu WC, Lam TP, Ng BK, et al. . Effect of upright position on tonsillar level in adolescent idiopathic scoliosis. Eur Radiol. 2015;25(8):2397–402. doi: 10.1007/s00330-015-3597-3 PubMed DOI

Sun X, Qiu Y, Zhu Z, Zhu F, Wang B, Yu Y, et al. . Variations of the position of the cerebellar tonsil in idiopathic scoliotic adolescents with a cobb angle >40 degrees: a magnetic resonance imaging study. Spine (Phila Pa 1976). 2007;32(15):1680–6. doi: 10.1097/BRS.0b013e318074d3f5 PubMed DOI

Wang D, Shi L, Liu S, Hui SC, Wang Y, Cheng JC, et al. . Altered topological organization of cortical network in adolescent girls with idiopathic scoliosis. PLoS One. 2013;8(12):e83767. doi: 10.1371/journal.pone.0083767 PubMed DOI PMC

Wang D, Shi L, Chu WC, Burwell RG, Cheng JC, Ahuja AT.. Abnormal cerebral cortical thinning pattern in adolescent girls with idiopathic scoliosis. Neuroimage. 2012;59(2):935–42. doi: 10.1016/j.neuroimage.2011.07.097 PubMed DOI

Beck S, Richardson SP, Shamim EA, Dang N, Schubert M, Hallett M.. Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia. J Neurosci. 2008;28(41):10363–9. doi: 10.1523/JNEUROSCI.3564-08.2008 PubMed DOI PMC

Beck S, Hallett M.. Surround inhibition in the motor system. Exp Brain Res. 2011;210(2):165–72. doi: 10.1007/s00221-011-2610-6 PubMed DOI PMC

Clarkson AN, Huang BS, Macisaac SE, Mody I, Carmichael ST.. Reducing excessive GABA-mediated tonic inhibition promotes functional recovery after stroke. Nature. 2010;468(7321):305–9. doi: 10.1038/nature09511 PubMed DOI PMC

Berardelli A, Abbruzzese G, Chen R, Orth M, Ridding MC, Stinear C, et al. . Consensus paper on short-interval intracortical inhibition and other transcranial magnetic stimulation intracortical paradigms in movement disorders. Brain Stimul. 2008;1(3):183–91. doi: 10.1016/j.brs.2008.06.005 PubMed DOI

Chen R. Interactions between inhibitory and excitatory circuits in the human motor cortex. Exp Brain Res. 2004;154(1):1–10. doi: 10.1007/s00221-003-1684-1 PubMed DOI

Di Lazzaro V, Ziemann U.. The contribution of transcranial magnetic stimulation in the functional evaluation of microcircuits in human motor cortex. Front Neural Circuits. 2013;7:18. doi: 10.3389/fncir.2013.00018 PubMed DOI PMC

Chong BW, Stinear CM.. Modulation of motor cortex inhibition during motor imagery. J Neurophysiol. 2017;117(4):1776–84. doi: 10.1152/jn.00549.2016 PubMed DOI PMC

Curra A, Modugno N, Inghilleri M, Manfredi M, Hallett M, Berardelli A.. Transcranial magnetic stimulation techniques in clinical investigation. Neurology. 2002;59(12):1851–9. doi: 10.1212/01.WNL.0000038744.30298.D4 PubMed DOI

Poston B, Kukke SN, Paine RW, Francis S, Hallett M.. Cortical silent period duration and its implications for surround inhibition of a hand muscle. Eur J Neurosci. 2012;36(7):2964–71. doi: 10.1111/j.1460-9568.2012.08212.x PubMed DOI PMC

Ni Z, Gunraj C, Chen R.. Short interval intracortical inhibition and facilitation during the silent period in human. J Physiol. 2007;583(Pt 3):971–82. doi: 10.1113/jphysiol.2007.135749 PubMed DOI PMC

Kofler M. Functional organization of exteroceptive inhibition following nociceptive electrical fingertip stimulation in humans. Clin Neurophysiol. 2003;114(6):973–80. doi: 10.1016/S1388-2457(03)00060-9 PubMed DOI

Floeter MK. Cutaneous silent periods. Muscle Nerve. 2003;28(4):391–401. doi: 10.1002/mus.10447 PubMed DOI

Vasko P, Bocek V, Mencl L, Haninec P, Stetkarova I.. Preserved cutaneous silent period in cervical root avulsion. J Spinal Cord Med. 2017;40(2):175–80. doi: 10.1179/2045772315Y.0000000053 PubMed DOI PMC

Kimberley TJ, Borich MR, Prochaska KD, Mundfrom SL, Perkins AE, Poepping JM.. Establishing the definition and inter-rater reliability of cortical silent period calculation in subjects with focal hand dystonia and healthy controls. Neurosci Lett. 2009;464(2):84–7. doi: 10.1016/j.neulet.2009.08.029 PubMed DOI PMC

Kofler M, Kumru H, Stetkarova I, Schindler C, Fuhr P.. Muscle force up to 50% of maximum does not affect cutaneous silent periods in thenar muscles. Clin Neurophysiol. 2007;118(9):2025–30. doi: 10.1016/j.clinph.2007.06.005 PubMed DOI

Weinstein SL, Dolan LA, Cheng JC, Danielsson A, Morcuende JA.. Adolescent idiopathic scoliosis. Lancet. 2008;371(9623):1527–37. doi: 10.1016/S0140-6736(08)60658-3 PubMed DOI

Cohen LG, Roth BJ, Nilsson J, Dang N, Panizza M, Bandinelli S, et al. . Effects of coil design on delivery of focal magnetic stimulation. Technical considerations. Electroencephalogr Clin Neurophysiol. 1990;75(4):350–7. doi: 10.1016/0013-4694(90)90113-X PubMed DOI

Kimiskidis VK, Potoupnis M, Papagiannopoulos SK, Dimopoulos G, Kazis DA, Markou K, et al. . Idiopathic scoliosis: a transcranial magnetic stimulation study. J Musculoskelet Neuronal Interact. 2007;7(2):155–60. PubMed

Sainburg RL. Convergent models of handedness and brain lateralization. Front Psychol. 2014;5:1092. doi: 10.3389/fpsyg.2014.01092 PubMed DOI PMC

Greenhouse I, Sias A, Labruna L, Ivry RB.. Nonspecific inhibition of the motor system during response preparation. J Neurosci. 2015;35(30):10675–84. doi: 10.1523/JNEUROSCI.1436-15.2015 PubMed DOI PMC

Farahpour N, Younesian H, Bahrpeyma F.. Electromyographic activity of erector spinae and external oblique muscles during trunk lateral bending and axial rotation in patients with adolescent idiopathic scoliosis and healthy subjects. Clin Biomech (Bristol, Avon). 2015;30(5):411–7. doi: 10.1016/j.clinbiomech.2015.03.018 PubMed DOI

Cheng JC, Guo X, Sher AH, Chan YL, Metreweli C.. Correlation between curve severity, somatosensory evoked potentials, and magnetic resonance imaging in adolescent idiopathic scoliosis. Spine (Phila Pa 1976). 1999;24(16):1679–84. doi: 10.1097/00007632-199908150-00009 PubMed DOI

Maruyama A, Matsunaga K, Tanaka N, Rothwell JC.. Muscle fatigue decreases short-interval intracortical inhibition after exhaustive intermittent tasks. Clin Neurophysiol. 2006;117(4):864–70. doi: 10.1016/j.clinph.2005.12.019 PubMed DOI

Arias P, Robles-Garcia V, Corral-Bergantinos Y, Madrid A, Espinosa N, Valls-Sole J, et al. . Central fatigue induced by short-lasting finger tapping and isometric tasks: a study of silent periods evoked at spinal and supraspinal levels. Neuroscience. 2015;305:316–27. doi: 10.1016/j.neuroscience.2015.07.081 PubMed DOI

Garvey MA, Gilbert DL.. Transcranial magnetic stimulation in children. Eur J Paediatr Neurol. 2004;8(1):7–19. doi: 10.1016/j.ejpn.2003.11.002 PubMed DOI

Garvey MA, Ziemann U, Bartko JJ, Denckla MB, Barker CA, Wassermann EM.. Cortical correlates of neuromotor development in healthy children. Clin Neurophysiol. 2003;114(9):1662–70. doi: 10.1016/S1388-2457(03)00130-5 PubMed DOI

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