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Research Article| Volume 306, ISSUE 1-2, P71-75, July 15, 2011

Sensorimotor network in cervical dystonia and the effect of botulinum toxin treatment: A functional MRI study

  • Robert Opavský
    Correspondence
    Corresponding author at: Dept. of Neurology, Faculty of Medicine and Dentistry, Palacký University and University Hospital, I.P. Pavlova 6, 775 20 Olomouc, Czech Republic. Tel.: +420 588443401; fax: +420 585428201.
    Affiliations
    Department of Neurology, Faculty of Medicine and Dentistry, Palacký University and University Hospital, Olomouc, Czech Republic
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  • Petr Hluštík
    Affiliations
    Department of Neurology, Faculty of Medicine and Dentistry, Palacký University and University Hospital, Olomouc, Czech Republic
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  • Pavel Otruba
    Affiliations
    Department of Neurology, Faculty of Medicine and Dentistry, Palacký University and University Hospital, Olomouc, Czech Republic
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  • Petr Kaňovský
    Affiliations
    Department of Neurology, Faculty of Medicine and Dentistry, Palacký University and University Hospital, Olomouc, Czech Republic
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Published:April 14, 2011DOI:https://doi.org/10.1016/j.jns.2011.03.040

      Abstract

      Background

      The evidence suggests that the origin of primary dystonia is at least partly associated with widespread dysfunction of the basal ganglia and cortico–striato–thalamo–cortical circuits. The aim of the study was to assess the sensorimotor activation pattern outside the circuits controlling the affected body part in cervical dystonia, as well as to determine task-related activation changes induced by botulinum toxin type A (BoNT-A) treatment.

      Methods

      Seven patients suffering from cervical dystonia and nine healthy controls were examined with functional MRI during skilled hand motor task; the examination was repeated 4 weeks after BoNT-A application to dystonic neck muscles.

      Results

      Functional MRI data demonstrated overall reduced extent of hand movement-related cortical activation but greater magnitude of blood oxygenation level dependent signal change in the contralateral secondary somatosensory cortex in patients compared to controls. Effective BoNT-A treatment led to reduced activation of the ipsilateral supplementary motor area and dorsal premotor cortex in patients. The patients' post-treatment sensorimotor maps showed significantly smaller basal ganglia activation compared to controls.

      Conclusions

      These results provide imaging evidence that abnormalities in sensorimotor activation extend beyond circuits controlling the affected body parts in cervical dystonia. The study also supports observations that BoNT-A effect has a correlate at central nervous system level, and such effect may not be limited to cortical and subcortical representations of the treated muscles.

      Keywords

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      References

        • Stacy M.
        Idiopathic cervical dystonia: an overview.
        Neurology. 2000; 12: S2-S8
        • Peterson D.A.
        • Sejnowski T.J.
        • Poizner H.
        Convergent evidence for abnormal striatal synaptic plasticity in dystonia.
        Neurobiol Dis. 2010; 3: 558-573
        • Tinazzi M.
        • Fiorio M.
        • Fiaschi A.
        • Rothwell J.C.
        • Bhatia K.P.
        Sensory functions in dystonia: insights from behavioral studies.
        Mov Disord. 2009; 10: 1427-1436
        • 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
        • Hinkley L.B.
        • Webster R.L.
        • Byl N.N.
        • Nagarajan S.S.
        Neuroimaging characteristics of patients with focal hand dystonia.
        J Hand Ther. 2009; 2: 125-134
        • Dresel C.
        • Haslinger B.
        • Castrop F.
        • Wohlschlaeger A.M.
        • Ceballos-Baumann A.O.
        Silent event-related fMRI reveals deficient motor and enhanced somatosensory activation in orofacial dystonia.
        Brain. 2006; 1: 36-46
        • Walsh R.
        • Hutchinson M.
        Molding the sensory cortex: spatial acuity improves after botulinum toxin treatment for cervical dystonia.
        Mov Disord. 2007; 16: 2443-2446
        • 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
        • Pelosin E.
        • Bove M.
        • Marinelli L.
        • Abbruzzese G.
        • Ghilardi M.F.
        Cervical dystonia affects aimed movements of nondystonic segments.
        Mov Disord. 2009; 13: 1955-1961
        • Jankovic J.
        Treatment of cervical dystonia with botulinum toxin.
        Mov Disord. 2004; : S109-S115
        • Abbruzzese G.
        • Berardelli A.
        Neurophysiological effects of botulinum toxin type A.
        Neurotox Res. 2006; 9: 109-114
      1. Tsui JK, Eisen A, Stoessl AJ, Calne S, Calne DB. Double-blind study of botulinum toxin in spasmodic torticollis. Lancet 1986;8501:245–247.

        • Roland P.E.
        • Larsen B.
        • Lassen N.A.
        • Skinhøj E.
        Supplementary motor area and other cortical areas in organization of voluntary movements in man.
        J Neurophysiol. 1980; 1: 118-136
        • Brashear A.
        The botulinum toxins in the treatment of cervical dystonia.
        Semin Neurol. 2001; 1: 85-90
        • Johansen-Berg H.
        • Dawes H.
        • Guy C.
        • Smith S.M.
        • Wade D.T.
        • Matthews P.M.
        Correlation between motor improvements and altered fMRI activity after rehabilitative therapy.
        Brain. 2002; 125: 2731-2742
        • Smith S.M.
        • Jenkinson M.
        • Woolrich M.W.
        • Beckmann C.F.
        • Behrens T.E.
        • Johansen-Berg H.
        • et al.
        Advances in functional and structural MR image analysis and implementation as FSL.
        Neuroimage. 2004; 23: S208-S219
        • Benecke R.
        • Meyer B.U.
        • Schönle P.
        • Conrad B.
        Transcranial magnetic stimulation of the human brain: responses in muscles supplied by cranial nerves.
        Exp Brain Res. 1988; 3: 623-632
        • Thompson M.L.
        • Thickbroom G.W.
        • Mastaglia F.L.
        Corticomotor representation of the sternocleidomastoid muscle.
        Brain. 1997; 2: 245-255
        • Mazzini L.
        • Zaccala M.
        • Balzarini C.
        Abnormalities of somatosensory evoked potentials in spasmodic torticollis.
        Mov Disord. 1994; 9: 426-430
        • Tamburin S.
        • Manganotti P.
        • Marzi C.A.
        • Fiaschi A.
        • Zanette G.
        Abnormal somatotopic arrangement of sensorimotor interactions in dystonic patients.
        Brain. 2002; 12: 2719-2730
        • Siggelkow S.
        • Kossev A.
        • Moll C.
        • Däuper J.
        • Dengler R.
        • Rollnik J.D.
        Impaired sensorimotor integration in cervical dystonia: a study using transcranial magnetic stimulation and muscle vibration.
        J Clin Neurophysiol. 2002; 3: 232-239
        • Quartarone A.
        • Bagnato S.
        • Rizzo V.
        • Siebner H.R.
        • Dattola V.
        • Scalfari A.
        • et al.
        Abnormal associative plasticity of the human motor cortex in writer's cramp.
        Brain. 2003; 12: 2586-2596
        • De Vries P.M.
        • Johnson K.A.
        • de Jong B.M.
        • Gieteling E.W.
        • Bohning D.E.
        • George M.S.
        • et al.
        Changed patterns of cerebral activation related to clinically normal hand movement in cervical dystonia.
        Clin Neurol Neurosurg. 2008; 12: 120-128
        • Solodkin A.
        • Hlustik P.
        • Chen E.E.
        • Small S.L.
        Modulation in network activation during motor execution and motor imagery.
        Cereb Cortex. 2004; 14: 1246-1255
        • Kakigi R.
        • Shimojo M.
        • Hoshiyama M.
        • Koyama S.
        • Watanabe S.
        • Naka D.
        • et al.
        Effects of movement and movement imagery on somatosensory evoked magnetic fields following posterior tibial nerve stimulation.
        Brain Res Cogn Brain Res. 1997; 3: 241-253
        • Abbruzzese G.
        • Berardelli A.
        Sensorimotor integration in movement disorders.
        Mov Disord. 2003; 3: 231-240
        • Obermann M.
        • Vollrath C.
        • de Greiff A.
        • Gizewski E.R.
        • Diener H.C.
        • Hallett M.
        • et al.
        Sensory disinhibition on passive movement in cervical dystonia.
        Mov Disord. 2010; 25: 2627-2633
        • Quartarone A.
        • Rizzo V.
        • Terranova C.
        • Morgante F.
        • Schneider S.
        • Ibrahim N.
        • et al.
        Abnormal sensorimotor plasticity in organic but not in psychogenic dystonia.
        Brain. 2009; 10: 2871-2877
        • Tanji J.
        New concepts of the supplementary motor area.
        Curr Opin Neurobiol. 1996; 6: 782-787
        • 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
        • Chouinard P.A.
        • Paus T.
        The primary motor and premotor areas of the human cerebral cortex.
        Neuroscientist. 2006; 2: 143-152
        • Ceballos-Baumann A.O.
        • Passingham R.E.
        • Warner T.
        • Playford E.D.
        • Marsden C.D.
        • Brooks D.J.
        Overactive prefrontal and underactive motor cortical areas in idiopathic dystonia.
        Ann Neurol. 1995; 3: 363-372
        • Murase N.
        • Rothwell J.C.
        • Kaji R.
        • Urushihara R.
        • Nakamura K.
        • Murayama N.
        • et al.
        Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp.
        Brain. 2005; 1: 104-115
        • Obermann M.
        • Yaldizli O.
        • de Greiff A.
        • Konczak J.
        • Lachenmayer M.L.
        • Tumczak F.
        • et al.
        Increased basal-ganglia activation performing a non-dystonia-related task in focal dystonia.
        Eur J Neurol. 2008; 8: 831-838