Changes in sensorimotor network activation after botulinum toxin type A injections in patients with cervical dystonia: a functional MRI study

. 2018 Oct ; 236 (10) : 2627-2637. [epub] 20180703

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid29971454

Grantová podpora
16-30210A AZV Ministry of Health Czech Republic, Czech Health Research Council

Odkazy

PubMed 29971454
PubMed Central PMC6153868
DOI 10.1007/s00221-018-5322-3
PII: 10.1007/s00221-018-5322-3
Knihovny.cz E-zdroje

Botulinum toxin type A (BoNT) is considered an effective therapeutic option in cervical dystonia (CD). The pathophysiology of CD and other focal dystonias has not yet been fully explained. Results from neurophysiological and imaging studies suggest a significant involvement of the basal ganglia and thalamus, and functional abnormalities in premotor and primary sensorimotor cortical areas are considered a crucial factor in the development of focal dystonias. Twelve BoNT-naïve patients with CD were examined with functional MRI during a skilled hand motor task; the examination was repeated 4 weeks after the first BoNT injection to the dystonic neck muscles. Twelve age- and gender-matched healthy controls were examined using the same functional MRI paradigm without BoNT injection. In BoNT-naïve patients with CD, BoNT treatment was associated with a significant increase of activation in finger movement-induced fMRI activation of several brain areas, especially in the bilateral primary and secondary somatosensory cortex, bilateral superior and inferior parietal lobule, bilateral SMA and premotor cortex, predominantly contralateral primary motor cortex, bilateral anterior cingulate cortex, ipsilateral thalamus, insula, putamen, and in the central part of cerebellum, close to the vermis. The results of the study support observations that the BoNT effect may have a correlate in the central nervous system level, and this effect may not be limited to cortical and subcortical representations of the treated muscles. The results show that abnormalities in sensorimotor activation extend beyond circuits controlling the affected body parts in CD even the first BoNT injection is associated with changes in sensorimotor activation. The differences in activation between patients with CD after treatment and healthy controls at baseline were no longer present.

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Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord. 2003;3:231–240. doi: 10.1002/mds.10327. PubMed DOI

Abbruzzese G, Berardelli A. Neurophysiological effects of botulinum toxin type A. Neurotox Res. 2006;9:109–114. doi: 10.1007/BF03033927. PubMed DOI

Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C. Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain. 2001;124(Pt 3):537–545. doi: 10.1093/brain/124.3.537. PubMed DOI

Antonucci F, Rossi C, Gianfranceschi L, Rossetto O, Caleo M. Long-distance retrograde effects of botulinum neurotoxin A. J Neurosci. 2008;28(14):3689–3696. doi: 10.1523/JNEUROSCI.0375-08.2008. PubMed DOI PMC

Avanzino L, Abbruzzese G. How does the cerebellum contribute to the pathophysiology of dystonia? Basal Ganglia. 2012;2(4):231–235. doi: 10.1016/j.baga.2012.05.003. DOI

Burciu RG, Hess CW, Coombes SA, Ofori E, Shukla P, Chung JW, McFarland NR, Wagle Shukla A, Okun MS, Vaillancourt DE. Functional activity of the sensorimotor cortex and cerebellum relates to cervical dystonia symptoms. Hum Brain Mapp. 2017;38(9):4563–4573. doi: 10.1002/hbm.23684. PubMed DOI PMC

Carbon M, Ghilardi MF, Argyelan M, Dhawan V, Bressman SB, Eidelberg D. Increased cerebellar activation during sequence learning in DYT1 carriers: an equiperformance study. Brain. 2008;131(1):146–154. doi: 10.1093/brain/awm243. PubMed DOI PMC

Castrop F, Dresel C, Hennenlotter A, Zimmer C, Haslinger B. Basal ganglia-premotor dysfunction during movement imagination in writer’s cramp. Mov Disord. 2012;27(11):1432–1439. doi: 10.1002/mds.24944. PubMed DOI

Chouinard PA, Paus T. What have we learned from “perturbing” the human cortical motor system with transcranial magnetic stimulation? Front Hum Neurosci. 2010;19(4):173. PubMed PMC

Consky E, Lang A. Clinical assessments of patients with cervical dystonia. In: Jankovic JHM, editor. Therapy with Botulinum Toxin. New York: Marcel Dekker Inc.; 1994.

Cuny E, Ghorayeb I, Guehl D, Escola L, Bioulac B, Burbaud P. Sensory motor mismatch within the supplementary motor area in the dystonic monkey. Neurobiol Dis. 2008;2:151–161. doi: 10.1016/j.nbd.2007.12.011. PubMed DOI

de Vries PM, Johnson KA, de Jong BM, Gieteling EW, Bohning DE, George MS, Leenders KL. Changed patterns of cerebral activation related to clinically normal hand movement in cervical dystonia. Clin Neurol Neurosurg. 2008;110(2):120–128. doi: 10.1016/j.clineuro.2007.09.020. PubMed DOI

de Vries PM, de Jong BM, Bohning DE, Hinson VK, George MS, Leenders KL. Reduced parietal activation in cervical dystonia after parietal TMS interleaved with fMRI. Clin Neurol Neurosurg. 2012;114(7):914–921. doi: 10.1016/j.clineuro.2012.02.006. PubMed DOI

Deuschl G, Heinen F, Kleedorfer B, Wagner M, Lücking CH, Poewe W. Clinical and polymyographic investigation of spasmodic torticollis. J Neurol. 1992;239(1):9–15. doi: 10.1007/BF00839204. PubMed DOI

Extremera VC, Alvarez-Coca J, Rodrıguez GA, Perez JM, de Villanueva JLR, Dıaz CP. Torticollis is a usual symptom in posterior fossa tumors. Eur J Pediatr. 2008;167(2):249–250. doi: 10.1007/s00431-007-0453-8. PubMed DOI

Filip P, Lungu OV, Bares M. Dystonia and the cerebellum: a new field of interest in movement disorders? Clin Neurophysiol. 2013;124(7):1269–1276. doi: 10.1016/j.clinph.2013.01.003. PubMed DOI

Filip P, Lungu OV, Shaw DJ, Kasparek T, Bareš M. The mechanisms of movement control and time estimation in cervical dystonia patients. Neural Plast. 2013;2013:908741. doi: 10.1155/2013/908741. PubMed DOI PMC

Filip P, Gallea C, Lehéricy S, Bertasi E, Popa T, Mareček R, Lungu OV, Kašpárek T, Vaníček J, Bareš M. Disruption in cerebellar and basal ganglia networks during a visuospatial task in cervical dystonia. Mov Disord. 2017;32(5):757–768. doi: 10.1002/mds.26930. PubMed DOI

Frasson E, Priori A, Bertolasi L, Mauguière F, Fiaschi A, Tinazzi M. Somatosensory disinhibition in dystonia. Mov Disord. 2001;16(4):674–682. doi: 10.1002/mds.1142. PubMed DOI

Gelb DJ, Yoshimura DM, Olney RK, Lowenstein DH, Aminoff MJ. Change in pattern of muscle activity following botulinum toxin injections for torticollis. Ann Neurol. 1991;29(4):370–376. doi: 10.1002/ana.410290407. PubMed DOI

Gilio F, Currà A, Lorenzano C, Modugno N, Manfredi M, Berardelli A. Effects of botulinum toxin type A on intracortical inhibition in patients with dystonia. Ann Neurol. 2000;48(1):20–26. doi: 10.1002/1531-8249(200007)48:1<20::AID-ANA5>3.0.CO;2-U. PubMed DOI

Hinkley LB, Webster RL, Byl NN, Nagarajan SS. Neuroimaging characteristics of patients with focal hand dystonia. J Hand Ther. 2009;2:125–134. doi: 10.1016/j.jht.2008.11.002. PubMed DOI PMC

Hok P, Opavský J, Kutín M, Tüdös Z, Kaňovský P, Hluštík P. Modulation of the sensorimotor system by sustained manual pressure stimulation. Neuroscience. 2017;21:11–22. doi: 10.1016/j.neuroscience.2017.02.005. PubMed DOI

Huynh W, Krishnan AV, Lin CS, Vucic S, Katrak P, Hornberger M, Kiernan MC. Botulinum toxin modulates cortical maladaptation in poststroke spasticity. Muscle Nerve. 2013;48(1):93–99. doi: 10.1002/mus.23719. PubMed DOI

Jankovic Joseph. Treatment of cervical dystonia with botulinum toxin. Movement Disorders. 2004;19(S8):S109–S115. doi: 10.1002/mds.20024. PubMed DOI

Jenkinson Mark, Beckmann Christian F., Behrens Timothy E.J., Woolrich Mark W., Smith Stephen M. FSL. NeuroImage. 2012;62(2):782–790. doi: 10.1016/j.neuroimage.2011.09.015. PubMed DOI

Jinnah HA, Hess EJ, LeDoux MS, Sharma N, Baxter MG, DeLong MR. Rodent models for dystonia research: characteristics, evaluation, and utility. Mov Disord. 2005;20(3):283–292. doi: 10.1002/mds.20364. PubMed DOI

Johansen-Berg H, Dawes H, Guy C, Smith SM, Wade DT, Matthews PM. Correlation between motor improvements and altered fMRI activity after rehabilitative therapy. Brain. 2002;125:2731–2742. doi: 10.1093/brain/awf282. PubMed DOI

Kaňovský P, Rosales RL. Debunking the pathophysiological puzzle of dystonia with special reference to botulinum toxin therapy. Parkinsonism Relat Disord. 2011;17(Suppl 1):S11–S14. doi: 10.1016/j.parkreldis.2011.06.018. PubMed DOI

Kaňovský P, Dufek J, Halačková H, Rektor I. Change in the pattern of cervical dystonia might be the cause of benefit loss during botulinum toxin treatment. Eur J Neurol. 1997;4(1):79–84. doi: 10.1111/j.1468-1331.1997.tb00303.x. PubMed DOI

Kaňovský P, Streitová H, Dufek J, Znojil V, Daniel P, Rektor I. Change in lateralization of the P22/N30 cortical component of median nerve somatosensory evoked potentials in patients with cervical dystonia after successful treatment with botulinum toxin A. Mov Disord. 1998;1:108–117. doi: 10.1002/mds.870130122. PubMed DOI

Kaňovský P, Bareš M, Streitová H, Klajblová H, Daniel P, Rektor I. Abnormalities of cortical excitability and cortical inhibition in cervical dystonia. Evidence from somatosensory evoked potentials and paired transcranial magnetic stimulation recordings. J Neurol. 2003;250:42–50. doi: 10.1007/s00415-003-0942-2. PubMed DOI

Kantak SS, Stinear JW, Buch ER, Cohen LG. Rewiring the brain: potential role of the premotor cortex in motor control, learning, and recovery of function following brain injury. Neurorehabil Neural Repair. 2012;26(3):282–292. doi: 10.1177/1545968311420845. PubMed DOI PMC

LeDoux MS, Brand KA. Secondary cervical dystonia associated with structural lesions of the central nervous system. Mov Disord. 2003;18(1):60–69. doi: 10.1002/mds.10301. PubMed DOI

Liepert J, Kucinski T, Tuscher O, Pawlas F, Baumer T, Weiller C. Motor cortex excitability after cerebellar infarction. Stroke. 2004;35(11):2484–2488. doi: 10.1161/01.STR.0000143152.45801.ca. PubMed DOI

Marchal-Crespo L, Michels L, Jaeger L, López-Olóriz J, Riener R. Effect of error augmentation on brain activation and motor learning of a complex locomotor task. Front Neurosci. 2017;11:526. doi: 10.3389/fnins.2017.00526. PubMed DOI PMC

Marchand-Pauvert V, Aymard C, Giboin LS, Dominici F, Rossi A, Mazzocchio R. Beyond muscular effects: depression of spinal recurrent inhibition after botulinum neurotoxin A. J Physiol. 2013;15(4):1017–1029. doi: 10.1113/jphysiol.2012.239178. PubMed DOI PMC

Marin C, Martí MJ, Tolosa E, Alvarez R, Montserrat LL, Santamaria J. Modification of muscle activity after BOTOX injections in spasmodic torticollis. Ann Neurol. 1992;32(3):411–412. doi: 10.1002/ana.410320323. PubMed DOI

Marin C, Martí MJ, Tolosa E, Alvarez R, Montserrat L, Santamaria J. Muscle activity changes in spasmodic torticollis after botulinum toxin treatment. Eur J Neurol. 1995;1(3):243–247. doi: 10.1111/j.1468-1331.1995.tb00078.x. PubMed DOI

Obermann M, Yaldizli O, de Greiff A, Konczak J, Lachenmayer ML, Tumczak F, et al. Increased basal-ganglia activation performing a non-dystonia-related task in focal dystonia. Eur J Neurol. 2008;8:831–838. doi: 10.1111/j.1468-1331.2008.02196.x. PubMed DOI

Obermann M, Vollrath C, de Greiff A, Gizewski ER, Diener HC, Hallett M, Maschke M. Sensory disinhibition on passive movement in cervical dystonia. Mov Disord. 2010;25(15):2627–2633. doi: 10.1002/mds.23321. PubMed DOI

Oliveri M, Babiloni C, Filippi MM, Caltagirone C, Babiloni F, Cicinelli P, Traversa R, Palmieri MG, Rossini PM. Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues. Exp Brain Res. 2003;149(2):214–221. doi: 10.1007/s00221-002-1346-8. PubMed DOI

Opavský R, Hluštík P, Otruba P, Kaňovský P. Sensorimotor network in cervical dystonia and the effect of botulinum toxin treatment: a functional MRI study. J Neur Sci. 2011;306(1–2):71–75. doi: 10.1016/j.jns.2011.03.040. PubMed DOI

Opavský R, Hluštík P, Otruba P, Kaňovský P. Somatosensory cortical activation in cervical dystonia and its modulation with botulinum toxin: an FMRI study. Int J Neurosci. 2012;122(1):45–52. doi: 10.3109/00207454.2011.623807. PubMed DOI

Palomar FJ, Mir P. Neurophysiological changes after intramuscular injection of botulinum toxin. Clin Neurophysiol. 2012;123(1):54–60. doi: 10.1016/j.clinph.2011.05.032. PubMed DOI

Peterson DA, Sejnowski TJ, Poizner H. Convergent evidence for abnormal striatal synaptic plasticity in dystonia. Neurobiol Dis. 2010;3:558–573. doi: 10.1016/j.nbd.2009.12.003. PubMed DOI PMC

Prudente CN, Stilla R, Singh S, Buetefisch C, Evatt M, Factor SA, Freeman A, Hu XP, Hess EJ, Sathian K, Jinnah HA. A functional magnetic resonance imaging study of head movements in cervical dystonia. Front Neurol. 2016;7:201. doi: 10.3389/fneur.2016.00201. PubMed DOI PMC

Raike RS, Jinnah HA, Hess EJ. Animal models of generalized dystonia. NeuroRx. 2005;2(3):504–512. doi: 10.1602/neurorx.2.3.504. PubMed DOI PMC

Rosales RL, Dressler D. On muscle spindles, dystonia and botulinum toxin. Eur J Neurol. 2010;17(Suppl 1):71–80. doi: 10.1111/j.1468-1331.2010.03056.x. PubMed DOI

Sadnicka A, Hoffland BS, Bhatia KP, van de Warrenburg BP, Edwards MJ. The cerebellum in dystonia help or hindrance? Clin Neurophysiol. 2012;123(1):65–70. doi: 10.1016/j.clinph.2011.04.027. PubMed DOI

Šenkárová Z, Hlustík P, Otruba P, Herzig R, Kanovský P. Modulation of cortical activity in patients suffering from upper arm spasticity following stroke and treated with botulinum toxin A: an fMRI study. J Neuroimaging. 2010;20(1):9–15. doi: 10.1111/j.1552-6569.2009.00375.x. PubMed DOI

Siggelkow S, Kossev A, Moll C, Däuper J, Dengler R, Rollnik JD. Impaired sensorimotor integration in cervical dystonia: a study using transcranial magnetic stimulation and muscle vibration. J Clin Neurophysiol. 2002;3:232–239. doi: 10.1097/00004691-200206000-00006. PubMed DOI

Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):208–219. doi: 10.1016/j.neuroimage.2004.07.051. PubMed DOI

Stacy M. Idiopathic cervical dystonia: an overview. Neurology. 2000;12(Suppl 5):2–8. PubMed

Tanji J. New concepts of the supplementary motor area. Curr Opin Neurobiol. 1996;6:782–787. doi: 10.1016/S0959-4388(96)80028-6. PubMed DOI

Thickbroom GW, Byrnes ML, Stell R, Mastaglia FL. Reversible reorganisation of the motor cortical representation of the hand in cervical dystonia. Mov Disord. 2003;18(4):395–402. doi: 10.1002/mds.10383. PubMed DOI

Tinazzi M, Fiorio M, Fiaschi A, Rothwell JC, Bhatia KP. Sensory functions indystonia: insights from behavioral studies. Mov Disord. 2009;10:1427–1436. doi: 10.1002/mds.22490. PubMed DOI

Tinazzi M, Squintani G, Berardelli A. Does neurophysiological testing provide the information we need to improve the clinical management of primary dystonia? Clin Neurophysiol. 2009;8:1424–1432. doi: 10.1016/j.clinph.2009.06.015. PubMed DOI

Tomášová Z, Hluštík P, Král M, Otruba P, Herzig R, Krobot A, Kaňovský P. Cortical activation changes in patients suffering from post-stroke arm spasticity and treated with botulinum toxin a. J Neuroimaging. 2013;23(3):337–344. doi: 10.1111/j.1552-6569.2011.00682.x. PubMed DOI

Torta DM, Cauda F. Different functions in the cingulate cortex, a meta-analytic connectivity modeling study. Neuroimage. 2011;56(4):2157–2172. doi: 10.1016/j.neuroimage.2011.03.066. PubMed DOI

Veverka T, Hluštík P, Tomášová Z, Hok P, Otruba P, Král M, Tüdös Z, Zapletalová J, Herzig R, Krobot A, Kaňovský P. BoNT-A related changes of cortical activity in patients suffering from severe hand paralysis with arm spasticity following ischemic stroke. J Neurol Sci. 2012;319(1–2):89–95. doi: 10.1016/j.jns.2012.05.008. PubMed DOI

Veverka Tomáš, Nevrly Martin, Otruba Pavel, Hluštík Petr, Kanovsky Petr. Botulinum Toxin Therapy Manual for Dystonia and Spasticity. 2016. How Much Evidence do we have on the Central Effects of Botulinum Toxin in Spasticity and Dystonia?

Vidailhet M, Grabli D, Roze E. Pathophysiology of dystonia. Curr Opin Neurol. 2009;22(4):406–413. doi: 10.1097/WCO.0b013e32832d9ef3. PubMed DOI

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