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Neuroimaging of Dystonia

  • Silvina G. HorovitzEmail author
  • Mark Hallett
Chapter
Part of the Current Clinical Neurology book series (CCNEU, volume 44)

Abstract

The primary dystonias are movement disorders characterized by involuntary muscle contractions that produce abnormal postures of different parts of the body. Named for the body part affected, the common adult onset focal dystonias are blepharospasm, cervical dystonia, spasmodic dysphonia, and focal hand dystonia. Their pathophysiology and even underlying anatomy remain largely unknown. Neuroimaging does not presently have a clinical role except to rule out secondary dystonias, in which dystonia is a result of defined central nervous system lesions. However, neuroimaging plays a role in trying to define where pathology might be, although till date, the findings have not been robust. In this chapter, we review studies using different imaging modalities, aiming to understand the structural and functional deficits the patients might have. Gray matter studies, based on T1-weighted magnetic resonance imaging (MRI) images and morphometric techniques, suggest the presence of structural changes in basal ganglia and sensorimotor cortices of dystonia patients. White matter integrity, measured with diffusion tensor imaging (DTI) and modeled using tractography methods, indicate deficits in different aspects of the cerebellar-thalamo-cortical and basal ganglia-thalamo-cortical pathways. Changes in blood flow, function, and metabolism, measured with positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) also support widespread deficits within the basal ganglia and beyond. Involvement of the cerebral cortex, in particular sensorimotor, supplementary motor area, and parietal association areas, are consistent in all the primary dystonias. The cerebellum is also affected in all the dystonias discussed here.

Keywords

Basal Ganglion Fractional Anisotropy Diffusion Tensor Imaging Mean Diffusivity Supplementary Motor Area 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Muller U, Kupke KG. The genetics of primary torsion dystonia. Hum Genet. 1990;84:107–15.PubMedGoogle Scholar
  2. 2.
    Muller J, Kiechl S, Wenning GK, et al. The prevalence of primary dystonia in the general community. Neurology. 2002;59:941–3.PubMedCrossRefGoogle Scholar
  3. 3.
    Muller U. The monogenic primary dystonias. Brain. 2009;132:2005–25.PubMedCrossRefGoogle Scholar
  4. 4.
    Hallett M. Blepharospasm: recent advances. Neurology. 2002;59:1306–12.PubMedCrossRefGoogle Scholar
  5. 5.
    Hallett M, Evinger C, Jankovic J, Stacy M. Update on blepharospasm: report from the BEBRF International Workshop. Neurology. 2008;71:1275–82.PubMedCrossRefGoogle Scholar
  6. 6.
    Peckham EL, Lopez G, Shamim EA, et al. Clinical features of patients with blepharospasm: a report of 240 patients. Eur J Neurol. 2011;18:382–6.PubMedCrossRefGoogle Scholar
  7. 7.
    Jankovic J, Tsui J, Bergeron C. Prevalence of cervical dystonia and spasmodic torticollis in the United States general population. Parkinsonism Relat Disord. 2007;13:411–6.PubMedCrossRefGoogle Scholar
  8. 8.
    Ludlow CL. Spasmodic dysphonia: a laryngeal control disorder specific to speech. J Neurosci. 2011;31:793–7.PubMedCrossRefGoogle Scholar
  9. 9.
    Adler CH, Edwards BW, Bansberg SF. Female predominance in spasmodic dysphonia. J Neurol Neurosurg Psychiatry. 1997;63:688.PubMedCrossRefGoogle Scholar
  10. 10.
    Cohen SM, Kim J, Roy N, Asche C, Courey M. Prevalence and causes of dysphonia in a large treatment-seeking population. Laryngoscope. 2012;122:343–8.PubMedCrossRefGoogle Scholar
  11. 11.
    Bartolome FM, Fanjul S, Cantarero S, Hernandez J, Garcia Ruiz PJ. Primary focal dystonia: descriptive study of 205 patients. Neurologia. 2003;18:59–65.PubMedGoogle Scholar
  12. 12.
    Ashburner J, Friston KJ. Voxel-based morphometry-the methods. Neuroimage. 2000;11:805–21.PubMedCrossRefGoogle Scholar
  13. 13.
    Pierpaoli C, Basser PJ. Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med. 1996;36:893–906.PubMedCrossRefGoogle Scholar
  14. 14.
    Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage. 2007;34:144–55.PubMedCrossRefGoogle Scholar
  15. 15.
    Behrens TE, Woolrich MW, Jenkinson M, et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med. 2003;50:1077–88.PubMedCrossRefGoogle Scholar
  16. 16.
    Fox PT, Mintun MA, Raichle ME, Herscovitch P. A noninvasive approach to quantitative functional brain mapping with H2 (15)O and positron emission tomography. J Cereb Blood Flow Metab. 1984;4:329–33.PubMedCrossRefGoogle Scholar
  17. 17.
    De Graaf RA. In vivo NMR spectroscopy: principles and techniques. Chichester: Wiley; 1998.Google Scholar
  18. 18.
    Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS. Time course EPI of human brain function during task activation. Magn Reson Med. 1992;25:390–7.PubMedCrossRefGoogle Scholar
  19. 19.
    Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med. 1995;34:537–41.PubMedCrossRefGoogle Scholar
  20. 20.
    Draganski B, Schneider SA, Fiorio M, et al. Genotype-phenotype interactions in primary dystonias revealed by differential changes in brain structure. Neuroimage. 2009;47:1141–7.PubMedCrossRefGoogle Scholar
  21. 21.
    Carbon M, Su S, Dhawan V, Raymond D, Bressman S, Eidelberg D. Regional metabolism in primary torsion dystonia: effects of penetrance and genotype. Neurology. 2004;62:1384–90.PubMedCrossRefGoogle Scholar
  22. 22.
    Carbon M, Argyelan M, Eidelberg D. Functional imaging in hereditary dystonia. Eur J Neurol. 2010;17(Suppl 1):58–64.PubMedCrossRefGoogle Scholar
  23. 23.
    Argyelan M, Carbon M, Niethammer M, et al. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci. 2009;29:9740–7.PubMedCrossRefGoogle Scholar
  24. 24.
    Eidelberg D. Abnormal brain networks in DYT1 dystonia. Adv Neurol. 1998;78:127–33.PubMedGoogle Scholar
  25. 25.
    Trost M, Carbon M, Edwards C, et al. Primary dystonia: is abnormal functional brain architecture linked to genotype? Ann Neurol. 2002;52:853–6.PubMedCrossRefGoogle Scholar
  26. 26.
    Garibotto V, Romito LM, Elia AE, et al. In vivo evidence for GABA(A) receptor changes in the sensorimotor system in primary dystonia. Mov Disord. 2011;26:852–7.PubMedCrossRefGoogle Scholar
  27. 27.
    Hallett M. Pathophysiology of dystonia. J Neural Transm Suppl. 2006;70:485–8.PubMedCrossRefGoogle Scholar
  28. 28.
    Asanuma K, Ma Y, Okulski J, et al. Decreased striatal D2 receptor binding in non-manifesting carriers of the DYT1 dystonia mutation. Neurology. 2005;64:347–9.PubMedCrossRefGoogle Scholar
  29. 29.
    Carbon M, Niethammer M, Peng S, et al. Abnormal striatal and thalamic dopamine neurotransmission: genotype-related features of dystonia. Neurology. 2009;72:2097–103.PubMedCrossRefGoogle Scholar
  30. 30.
    Hallett M. The neurophysiology of dystonia. Arch Neurol. 1998;55:601–3.PubMedCrossRefGoogle Scholar
  31. 31.
    Ghilardi MF, Carbon M, Silvestri G, et al. Impaired sequence learning in carriers of the DYT1 dystonia mutation. Ann Neurol. 2003;54:102–9.PubMedCrossRefGoogle Scholar
  32. 32.
    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;131:146–54.PubMedCrossRefGoogle Scholar
  33. 33.
    Etgen T, Muhlau M, Gaser C, Sander D. Bilateral grey-matter increase in the putamen in primary blepharospasm. J Neurol Neurosurg Psychiatry. 2006;77:1017–20.PubMedCrossRefGoogle Scholar
  34. 34.
    Obermann M, Yaldizli O, De Greiff A, et al. Morphometric changes of sensorimotor structures in focal dystonia. Mov Disord. 2007;22:1117–23.PubMedCrossRefGoogle Scholar
  35. 35.
    Martino D, Di Giorgio A, D’Ambrosio E, et al. Cortical gray matter changes in primary blepharospasm: a voxel-based morphometry study. Mov Disord. 2011;26:1907–12.PubMedCrossRefGoogle Scholar
  36. 36.
    Murai H, Suzuki Y, Kiyosawa M, et al. Positive correlation between severity of blepharospasm and thalamic glucose metabolism. Case Report Ophthalmol. 2011;2:50–4.CrossRefGoogle Scholar
  37. 37.
    Horovitz SG, Ford A, Najee-ullah MA, Ostuni JL, Hallett M. Anatomical correlates of blepharospasm. Transl Neurodegener. 2012;1:12.PubMedCrossRefGoogle Scholar
  38. 38.
    Suzuki Y, Kiyosawa M, Wakakura M, Mochizuki M, Ishii K. Gray matter density increase in the primary sensorimotor cortex in long-term essential blepharospasm. Neuroimage. 2011;56:1–7.PubMedCrossRefGoogle Scholar
  39. 39.
    Fabbrini G, Pantano P, Totaro P, et al. Diffusion tensor imaging in patients with primary cervical dystonia and in patients with blepharospasm. Eur J Neurol. 2008;15:185–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Kerrison JB, Lancaster JL, Zamarripa FE, et al. Positron emission tomography scanning in essential blepharospasm. Am J Ophthalmol. 2003;136:846–52.PubMedCrossRefGoogle Scholar
  41. 41.
    Suzuki Y, Mizoguchi S, Kiyosawa M, et al. Glucose hypermetabolism in the thalamus of patients with essential blepharospasm. J Neurol. 2007;254:890–6.PubMedCrossRefGoogle Scholar
  42. 42.
    Emoto H, Suzuki Y, Wakakura M, et al. Photophobia in essential blepharospasm-a positron emission tomographic study. Mov Disord. 2010;25:433–9.PubMedCrossRefGoogle Scholar
  43. 43.
    Feiwell RJ, Black KJ, McGee-Minnich LA, Snyder AZ, MacLeod AM, Perlmutter JS. Diminished regional cerebral blood flow response to vibration in patients with blepharospasm. Neurology. 1999;52:291–7.PubMedCrossRefGoogle Scholar
  44. 44.
    Hutchinson M, Nakamura T, Moeller JR, et al. The metabolic topography of essential blepharospasm: a focal dystonia with general implications. Neurology. 2000;55:673–7.PubMedCrossRefGoogle Scholar
  45. 45.
    Obermann M, Yaldizli O, de Greiff A, et al. Increased basal-ganglia activation performing a non-dystonia-related task in focal dystonia. Eur J Neurol. 2008;15:831–8.PubMedCrossRefGoogle Scholar
  46. 46.
    Dresel C, Haslinger B, Castrop F, Wohlschlaeger AM, Ceballos-Baumann AO. Silent event-related fMRI reveals deficient motor and enhanced somatosensory activation in orofacial dystonia. Brain. 2006;129:36–46.PubMedCrossRefGoogle Scholar
  47. 47.
    Schmidt KE, Linden DE, Goebel R, Zanella FE, Lanfermann H, Zubcov AA. Striatal activation during blepharospasm revealed by fMRI. Neurology. 2003;60:1738–43.PubMedCrossRefGoogle Scholar
  48. 48.
    Baker RS, Andersen AH, Morecraft RJ, Smith CD. A functional magnetic resonance imaging study in patients with benign essential blepharospasm. J Neuroophthalmol. 2003;23:11–5.PubMedCrossRefGoogle Scholar
  49. 49.
    Dresel C, Bayer F, Castrop F, Rimpau C, Zimmer C, Haslinger B. Botulinum toxin modulates basal ganglia but not deficient somatosensory activation in orofacial dystonia. Mov Disord. 2011;26:1496–502.PubMedCrossRefGoogle Scholar
  50. 50.
    Lee MS, Marsden CD. Movement disorders following lesions of the thalamus or subthalamic region. Mov Disord. 1994;9:493–507.PubMedCrossRefGoogle Scholar
  51. 51.
    Larumbe R, Vaamonde J, Artieda J, Zubieta JL, Obeso JA. Reflex blepharospasm associated with bilateral basal ganglia lesion. Mov Disord. 1993;8:198–200.PubMedCrossRefGoogle Scholar
  52. 52.
    Sadnicka A, Hoffland BS, Bhatia KP, van de Warrenburg BP, Edwards MJ. The cerebellum in dystonia—help or hindrance? Clin Neurophysiol. 2012;123:65–70.PubMedCrossRefGoogle Scholar
  53. 53.
    Zerrate MC, Pardo CA, Jinnah HA. Neuropathology in idiopatic cervical dystonia. Mov Disord. 2007;22:1.CrossRefGoogle Scholar
  54. 54.
    Becker G, Berg D, Rausch WD, Lange HK, Riederer P, Reiners K. Increased tissue copper and manganese content in the lentiform nucleus in primary adult-onset dystonia. Ann Neurol. 1999;46:260–3.PubMedCrossRefGoogle Scholar
  55. 55.
    Becker G, Naumann M, Scheubeck M, et al. Comparison of transcranial sonography, magnetic resonance imaging, and single photon emission computed tomography findings in idiopathic spasmodic torticollis. Mov Disord. 1997;12:79–88.PubMedCrossRefGoogle Scholar
  56. 56.
    Egger K, Mueller J, Schocke M, et al. Voxel based morphometry reveals specific gray matter changes in primary dystonia. Mov Disord. 2007;22:1538–42.PubMedCrossRefGoogle Scholar
  57. 57.
    Pantano P, Totaro P, Fabbrini G, et al. A transverse and longitudinal MR imaging voxel-based morphometry study in patients with primary cervical dystonia. AJNR Am J Neuroradiol. 2011;32:81–4.PubMedGoogle Scholar
  58. 58.
    Blood AJ, Tuch DS, Makris N, Makhlouf ML, Sudarsky LR, Sharma N. White matter abnormalities in dystonia normalize after botulinum toxin treatment. Neuroreport. 2006;17:1251–5.PubMedCrossRefGoogle Scholar
  59. 59.
    Bonilha L, de Vries PM, Vincent DJ, et al. Structural white matter abnormalities in patients with idiopathic dystonia. Mov Disord. 2007;22:1110–6.PubMedCrossRefGoogle Scholar
  60. 60.
    Blood AJ, Kuster JK, Woodman SC, et al. Evidence for altered basal ganglia-brainstem connections in cervical dystonia. PLoS One. 2012;7:e31654.PubMedCrossRefGoogle Scholar
  61. 61.
    Federico F, Lucivero V, Simone IL, et al. Proton MR spectroscopy in idiopathic spasmodic torticollis. Neuroradiology. 2001;43:532–6.PubMedCrossRefGoogle Scholar
  62. 62.
    Leenders K, Hartvig P, Forsgren L, et al. Striatal [11C]-N-methyl-spiperone binding in patients with focal dystonia (torticollis) using positron emission tomography. J Neural Transm Park Dis Dement Sect. 1993;5:79–87.PubMedCrossRefGoogle Scholar
  63. 63.
    Hierholzer J, Cordes M, Schelosky L, et al. Dopamine D2 receptor imaging with iodine-123-iodobenzamide SPECT in idiopathic rotational torticollis. J Nucl Med. 1994;35:1921–7.PubMedGoogle Scholar
  64. 64.
    Naumann M, Pirker W, Reiners K, Lange KW, Becker G, Brucke T. Imaging the pre- and postsynaptic side of striatal dopaminergic synapses in idiopathic cervical dystonia: a SPECT study using [123I] epidepride and [123I] beta-CIT. Mov Disord. 1998;13:319–23.PubMedCrossRefGoogle Scholar
  65. 65.
    Galardi G, Perani D, Grassi F, et al. Basal ganglia and thalamo-cortical hypermetabolism in patients with spasmodic torticollis. Acta Neurol Scand. 1996;94:172–6.PubMedCrossRefGoogle Scholar
  66. 66.
    Lalli S, Piacentini S, Franzini A, et al. Epidural premotor cortical stimulation in primary focal dystonia: clinical and (18) F-fluoro deoxyglucose positron emission tomography open study. Mov Disord. 2012;27:533–8.PubMedCrossRefGoogle Scholar
  67. 67.
    de Vries PM, Johnson KA, de Jong BM, et al. Changed patterns of cerebral activation related to clinically normal hand movement in cervical dystonia. Clin Neurol Neurosurg. 2008;110:120–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Obermann M, Vollrath C, de Greiff A, et al. Sensory disinhibition on passive movement in cervical dystonia. Mov Disord. 2010;25:2627–33.PubMedCrossRefGoogle Scholar
  69. 69.
    Opavsky R, Hlustik P, Otruba P, Kanovsky P. Sensorimotor network in cervical dystonia and the effect of botulinum toxin treatment: a functional MRI study. J Neurol Sci. 2011;306:71–5.PubMedCrossRefGoogle Scholar
  70. 70.
    Opavsky R, Hlustik P, Otruba P, Kanovsky P. Somatosensory cortical activation in cervical dystonia and its modulation with botulinum toxin: an FMRI study. Int J Neurosci. 2012;122:45–52.PubMedCrossRefGoogle Scholar
  71. 71.
    Schaefer S, Freeman F, Finitzo T, et al. Magnetic resonance imaging findings and correlations in spasmodic dysphonia patients. Ann Otol Rhinol Laryngol. 1985;94:595–601.PubMedGoogle Scholar
  72. 72.
    Simonyan K, Ludlow CL. Abnormal structure-function relationship in spasmodic dysphonia. Cereb Cortex. 2012;22:417–25.PubMedCrossRefGoogle Scholar
  73. 73.
    Simonyan K, Tovar-Moll F, Ostuni J, et al. Focal white matter changes in spasmodic dysphonia: a combined diffusion tensor imaging and neuropathological study. Brain. 2008;131:447–59.PubMedCrossRefGoogle Scholar
  74. 74.
    Hirano S, Kojima H, Naito Y, et al. Cortical dysfunction of the supplementary motor area in a spasmodic dysphonia patient. Am J Otolaryngol. 2001;22:219–22.PubMedCrossRefGoogle Scholar
  75. 75.
    Ali SO, Thomassen M, Schulz GM, et al. Alterations in CNS activity induced by botulinum toxin treatment in spasmodic dysphonia: an H2 15O PET study. J Speech Lang Hear Res. 2006;49:1127–46.PubMedCrossRefGoogle Scholar
  76. 76.
    Simonyan K, Ludlow CL. Abnormal activation of the primary somatosensory cortex in spasmodic dysphonia: an fMRI study. Cereb Cortex. 2010;20:2749–59.PubMedCrossRefGoogle Scholar
  77. 77.
    Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007;8:393–402.PubMedCrossRefGoogle Scholar
  78. 78.
    Black KJ, Ongur D, Perlmutter JS. Putamen volume in idiopathic focal dystonia. Neurology. 1998;51:819–24.PubMedCrossRefGoogle Scholar
  79. 79.
    Garraux G, Bauer A, Hanakawa T, Wu T, Kansaku K, Hallett M. Changes in brain anatomy in focal hand dystonia. Ann Neurol. 2004;55:736–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Granert O, Peller M, Jabusch HC, Altenmuller E, Siebner HR. Sensorimotor skills and focal dystonia are linked to putaminal grey-matter volume in pianists. J Neurol Neurosurg Psychiatry. 2011;82:1225–31.PubMedCrossRefGoogle Scholar
  81. 81.
    Imfeld A, Oechslin MS, Meyer M, Loenneker T, Jancke L. White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage. 2009;46:600–7.PubMedCrossRefGoogle Scholar
  82. 82.
    Delmaire C, Vidailhet M, Wassermann D, et al. Diffusion abnormalities in the primary sensorimotor pathways in writer’s cramp. Arch Neurol. 2009;66:502–8.PubMedCrossRefGoogle Scholar
  83. 83.
    Levy LM, Hallett M. Impaired brain GABA in focal dystonia. Ann Neurol. 2002;51:93–101.PubMedCrossRefGoogle Scholar
  84. 84.
    Hallett M. Pathophysiology of writer’s cramp. Hum Mov Sci. 2006;25:454–63.PubMedCrossRefGoogle Scholar
  85. 85.
    Herath P, Gallea C, van der Veen JW, Horovitz SG, Hallett M. In vivo neurochemistry of primary focal hand dystonia: a magnetic resonance spectroscopic neurometabolite profiling study at 3 T. Mov Disord. 2010;25:2800–8.PubMedCrossRefGoogle Scholar
  86. 86.
    Naumann M, Warmuth-Metz M, Hillerer C, Solymosi L, Reiners K. 1H magnetic resonance spectroscopy of the lentiform nucleus in primary focal hand dystonia. Mov Disord. 1998;13:929–33.PubMedCrossRefGoogle Scholar
  87. 87.
    Ceballos-Baumann AO, Sheean G, Passingham RE, Marsden CD, Brooks DJ. Botulinum toxin does not reverse the cortical dysfunction associated with writer’s cramp. A PET study. Brain. 1997;120(Pt 4):571–82.PubMedCrossRefGoogle Scholar
  88. 88.
    Lerner A, Shill H, Hanakawa T, Bushara K, Goldfine A, Hallett M. Regional cerebral blood flow correlates of the severity of writer’s cramp symptoms. Neuroimage. 2004;21:904–13.PubMedCrossRefGoogle Scholar
  89. 89.
    Tempel LW, Perlmutter JS. Abnormal vibration-induced cerebral blood flow responses in idiopathic dystonia. Brain. 1990;113(Pt 3):691–707.PubMedCrossRefGoogle Scholar
  90. 90.
    Tempel LW, Perlmutter JS. Abnormal cortical responses in patients with writer’s cramp. Neurology. 1993;43:2252–7.PubMedCrossRefGoogle Scholar
  91. 91.
    Perlmutter JS, Stambuk MK, Markham J, et al. Decreased [18F] spiperone binding in putamen in idiopathic focal dystonia. J Neurosci. 1997;17:843–50.PubMedGoogle Scholar
  92. 92.
    Karimi M, Moerlein SM, Videen TO, et al. Decreased striatal dopamine receptor binding in primary focal dystonia: a D2 or D3 defect? Mov Disord. 2011;26:100–6.PubMedCrossRefGoogle Scholar
  93. 93.
    Moore RD, Gallea C, Horovitz SG, Hallett M. Individuated finger control in focal hand dystonia: an fMRI study. Neuroimage. 2012;61:823–31.PubMedCrossRefGoogle Scholar
  94. 94.
    Pujol J, Roset-Llobet J, Rosines-Cubells D, et al. Brain cortical activation during guitar-induced hand dystonia studied by functional MRI. Neuroimage. 2000;12:257–67.PubMedCrossRefGoogle Scholar
  95. 95.
    Oga T, Honda M, Toma K, et al. Abnormal cortical mechanisms of voluntary muscle relaxation in patients with writer’s cramp: an fMRI study. Brain. 2002;125:895–903.PubMedCrossRefGoogle Scholar
  96. 96.
    Elbert T, Candia V, Altenmuller E, et al. Alteration of digital representations in somatosensory cortex in focal hand dystonia. Neuroreport. 1998;9:3571–5.PubMedCrossRefGoogle Scholar
  97. 97.
    Butterworth S, Francis S, Kelly E, McGlone F, Bowtell R, Sawle GV. Abnormal cortical sensory activation in dystonia: an fMRI study. Mov Disord. 2003;18:673–82.PubMedCrossRefGoogle Scholar
  98. 98.
    Nelson AJ, Blake DT, Chen R. Digit-specific aberrations in the primary somatosensory cortex in writer’s cramp. Ann Neurol. 2009;66:146–54.PubMedCrossRefGoogle Scholar
  99. 99.
    Delmaire C, Krainik A, Tezenas du Montcel S, et al. Disorganized somatotopy in the putamen of patients with focal hand dystonia. Neurology. 2005;64:1391–6.PubMedCrossRefGoogle Scholar
  100. 100.
    Sanger TD, Pascual-Leone A, Tarsy D, Schlaug G. Nonlinear sensory cortex response to simultaneous tactile stimuli in writer’s cramp. Mov Disord. 2002;17:105–11.PubMedCrossRefGoogle Scholar
  101. 101.
    Havrankova P, Jech R, Walker ND, et al. Repetitive TMS of the somatosensory cortex improves writer’s cramp and enhances cortical activity. Neuro Endocrinol Lett. 2010;31:73–86.PubMedGoogle Scholar
  102. 102.
    Blood AJ, Flaherty AW, Choi JK, et al. Basal ganglia activity remains elevated after movement in focal hand dystonia. Ann Neurol. 2004;55:744–8.PubMedCrossRefGoogle Scholar
  103. 103.
    Kadota H, Nakajima Y, Miyazaki M, et al. An fMRI study of musicians with focal dystonia during tapping tasks. J Neurol. 2010;257:1092–8.PubMedCrossRefGoogle Scholar
  104. 104.
    Peller M, Zeuner KE, Munchau A, et al. The basal ganglia are hyperactive during the discrimination of tactile stimuli in writer’s cramp. Brain. 2006;129:2697–708.PubMedCrossRefGoogle Scholar
  105. 105.
    Wu CC, Fairhall SL, McNair NA, et al. Impaired sensorimotor integration in focal hand dystonia patients in the absence of symptoms. J Neurol Neurosurg Psychiatry. 2010;81:659–65.PubMedCrossRefGoogle Scholar
  106. 106.
    Delnooz CC, Helmich RC, Medendorp WP, Van de Warrenburg BP, Toni I. Writer’s cramp: increased dorsal premotor activity during intended writing. Hum Brain Mapp. 2013;34:613–25.PubMedGoogle Scholar
  107. 107.
    Castrop F, Dresel C, Hennenlotter A, Zimmer C, Haslinger B. Basal ganglia-premotor dysfunction during movement imagination in writer’s cramp. Mov Disord. 2012;27:1432–9.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Human Motor Control Section, Medical Neurology Branch, National Institute of Neurological Disorders and StrokeNational Institute of HealthBethesdaUSA

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