1932

Abstract

Dystonia is a collection of symptoms with involuntary muscle activation causing hypertonia, hyperkinetic movements, and overflow. In children, dystonia can have numerous etiologies with varying neuroanatomic distribution. The semiology of dystonia can be explained by gain-of-function failure of a feedback controller that is responsible for stabilizing posture and movement. Because postural control is maintained by a widely distributed network, many different anatomic regions may be responsible for symptoms of dystonia, although all features of dystonia can be explained by uncontrolled activation or hypersensitivity of motor cortical regions that can cause increased reflex gain, inserted postures, or sensitivity to irrelevant sensory variables. Effective treatment of dystonia in children requires an understanding of the relationship between etiology, anatomy, and the specific mechanism of failure of postural stabilization.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-080317-061504
2018-07-08
2024-06-21
Loading full text...

Full text loading...

/deliver/fulltext/neuro/41/1/annurev-neuro-080317-061504.html?itemId=/content/journals/10.1146/annurev-neuro-080317-061504&mimeType=html&fmt=ahah

Literature Cited

  1. Alam M, Schwabe K, Lutjens G, Capelle HH, Manu M et al. 2015. Comparative characterization of single cell activity in the globus pallidus internus of patients with dystonia or Tourette syndrome. J. Neural. Transm. 122:687–99
    [Google Scholar]
  2. Albanese A, Bhatia K, Bressman S, Delong M, Fahn S et al. 2013. Phenomenology and classification of dystonia: a consensus update. Mov. Disord. 28:863–73
    [Google Scholar]
  3. Avanzino L, Fiorio M 2014. Proprioceptive dysfunction in focal dystonia: from experimental evidence to rehabilitation strategies. Front. Hum. Neurosci. 8:1000
    [Google Scholar]
  4. Bara-Jimenez W, Catalan MJ, Hallett M, Gerloff C 1998. Abnormal somatosensory homunculus in dystonia of the hand. Ann. Neurol. 44:828–31
    [Google Scholar]
  5. Bara-Jimenez W, Shelton P, Sanger TD, Hallett M 2000. Sensory discrimination capabilities in patients with focal hand dystonia. Ann. Neurol. 47:377–80
    [Google Scholar]
  6. Barow E, Neumann WJ, Brucke C, Huebl J, Horn A et al. 2014. Deep brain stimulation suppresses pallidal low frequency activity in patients with phasic dystonic movements. Brain 137:3012–24
    [Google Scholar]
  7. Bertucco M, Sanger TD 2014. Speed-accuracy testing on the Apple iPad® provides a quantitative test of upper extremity motor performance in children with dystonia. J. Child Neurol. 29:1460–66
    [Google Scholar]
  8. Bonsi P, Cuomo D, Martella G, Madeo G, Schirinzi T et al. 2011. Centrality of striatal cholinergic transmission in basal ganglia function. Front. Neuroanat. 5:6
    [Google Scholar]
  9. Byl NN, Archer ES, McKenzie A 2009. Focal hand dystonia: effectiveness of a home program of fitness and learning-based sensorimotor and memory training. J. Hand Ther. 22:183–98
    [Google Scholar]
  10. Byl NN, Merzenich MM, Jenkins WM 1996. A primate genesis model of focal dystonia and repetitive strain injury: I. Learning-induced dedifferentiation of the representation of the hand in the primary somatosensory cortex in adult monkeys. Neurology 47:508–20
    [Google Scholar]
  11. Byl NN, Nagajaran S, McKenzie AL 2003. Effect of sensory discrimination training on structure and function in patients with focal hand dystonia: a case series. Arch. Phys. Med. Rehabil. 84:1505–14
    [Google Scholar]
  12. Chang EF, Turner RS, Ostrem JL, Davis VR, Starr PA 2007. Neuronal responses to passive movement in the globus pallidus internus in primary dystonia. J. Neurophysiol. 98:3696–707
    [Google Scholar]
  13. Chen R, Hallett M 1998. Focal dystonia and repetitive motion disorders. Clin. Orthop. Relat. Res.351102–6
    [Google Scholar]
  14. Chu VWT, Sternad D, Sanger TD 2013. Healthy and dystonic children compensate for changes in motor variability. J. Neurophysiol. 109:2169–78
    [Google Scholar]
  15. Cif L, Coubes P 2017. Historical developments in children's deep brain stimulation. Eur. J. Paediatr. Neurol. 21:109–17
    [Google Scholar]
  16. Cisek P, Kalaska JF 2005. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45:801–14
    [Google Scholar]
  17. Cohen LG, Hallett M 1988. Hand cramps: clinical features and electromyographic patterns in a focal dystonia. Neurology 38:1005–12
    [Google Scholar]
  18. Cramer SC, Sampat A, Haske-Palomino M, Nguyen S, Procaccio V, Hermanowicz N 2010. Increased prevalence of val66 met BDNF genotype among subjects with cervical dystonia. Neurosci. Lett. 468:42–45
    [Google Scholar]
  19. Crittenden JR, Graybiel AM 2011. Basal ganglia disorders associated with imbalances in the striatal striosome and matrix compartments. Front. Neuroanat. 5:59
    [Google Scholar]
  20. Eltahawy HA, Saint-Cyr J, Giladi N, Lang AE, Lozano AM 2004. Primary dystonia is more responsive than secondary dystonia to pallidal interventions: outcome after pallidotomy or pallidal deep brain stimulation. Neurosurgery 54:613–21
    [Google Scholar]
  21. Filip P, Lungu OV, Bares M 2013. Dystonia and the cerebellum: a new field of interest in movement disorders. Clin. Neurophysiol. 124:1269–76
    [Google Scholar]
  22. Fitts PM 1954. The information capacity of the human motor system in controlling the amplitude of movement. J. Exp. Psychol. 47:381–91
    [Google Scholar]
  23. Frucht SJ 2009. Focal task-specific dystonia of the musicians’ hand—a practical approach for the clinician. J. Hand Ther. 22:136–43
    [Google Scholar]
  24. Graziano MS 2016. Ethological action maps: a paradigm shift for the motor cortex. Trends Cogn. Sci. 20:121–32
    [Google Scholar]
  25. Graziano MS, Aflalo TN, Cooke DF 2005. Arm movements evoked by electrical stimulation in the motor cortex of monkeys. J. Neurophysiol. 94:4209–23
    [Google Scholar]
  26. Griffin DM, Hudson HM, Belhaj-Saïf A, Cheney PD 2014. EMG activation patterns associated with high frequency, long-duration intracortical microstimulation of primary motor cortex. J. Neurosci. 34:1647–56
    [Google Scholar]
  27. Hallett M 1998. The neurophysiology of dystonia. Arch. Neurol. 55:601–3
    [Google Scholar]
  28. Hoon AH Jr., Stashinko EE, Nagae LM, Lin DD, Keller J et al. 2009. Sensory and motor deficits in children with cerebral palsy born preterm correlate with diffusion tensor imaging abnormalities in thalamocortical pathways. Dev. Med. Child Neurol. 51:697–704
    [Google Scholar]
  29. Huang XJ, Wang T, Wang JL, Liu XL, Che XQ et al. 2015. Paroxysmal kinesigenic dyskinesia: clinical and genetic analyses of 110 patients. Neurology 85:1546–53
    [Google Scholar]
  30. Hutchison WD, Lang AE, Dostrovsky JO, Lozano AM 2003. Pallidal neuronal activity: implications for models of dystonia. Ann. Neurol. 53:480–88
    [Google Scholar]
  31. Hutchison WD, Lozano A, Davis K, Saint-Cyr J, Lang A, Dostrovsky J 1994. Differential neuronal activity in segments of globus pallidus in Parkinson's disease patients. Neuroreport 5:1533–37
    [Google Scholar]
  32. Kansagra S, Mikati MA, Vigevano F 2013. Alternating hemiplegia of childhood. Handb. Clin. Neurol. 112:821–26
    [Google Scholar]
  33. Kilgard MP, Merzenich MM 1998. Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–18
    [Google Scholar]
  34. Koy A, Timmermann L 2017. Deep brain stimulation in cerebral palsy: challenges and opportunities. Eur. J. Paediatr. Neurol. 21:118–21
    [Google Scholar]
  35. Kukke SN, Sanger TD 2011. Contributors to excess antagonist activity during movement in children with secondary dystonia due to cerebral palsy. J. Neurophysiol. 105:2100–7
    [Google Scholar]
  36. Kupsch A, Benecke R, Müller J, Trottenberg T, Schneider G-H et al. 2006. Pallidal deep-brain stimulation in primary generalized or segmental dystonia. N. Engl. J. Med. 355:1978–90
    [Google Scholar]
  37. Lenz FA, Byl NN 1999. Reorganization in the cutaneous core of the human thalamic principal somatic sensory nucleus (ventral caudal) in patients with dystonia. J. Neurophysiol. 82:3204–12
    [Google Scholar]
  38. Lenz FA, Jaeger CJ, Seike MS, Lin YC, Reich SG et al. 1999. Thalamic single neuron activity in patients with dystonia: dystonia-related activity and somatic sensory reorganization. J. Neurophysiol. 82:2372–92
    [Google Scholar]
  39. Lenz FA, Suarez JI, Metman LV, Reich SG, Karp BI et al. 1998. Pallidal activity during dystonia: somatosensory reorganisation and changes with severity. J. Neurol. Neurosurg. Psychiatry 65:767–70
    [Google Scholar]
  40. Lin JP, Lumsden DE, Gimeno H, Kaminska M 2014. The impact and prognosis for dystonia in childhood including dystonic cerebral palsy: a clinical and demographic tertiary cohort study. J. Neurol. Neurosurg. Psychiatry 85:1239–44
    [Google Scholar]
  41. Lin JP, Nardocci N 2016. Recognizing the common origins of dystonia and the development of human movement: a manifesto of unmet needs in isolated childhood dystonias. Front. Neurol. 7:226
    [Google Scholar]
  42. Lumsden DE, Gimeno H, Lin JP 2016. Classification of dystonia in childhood. Parkinsonism Relat. Disord. 33:138–41
    [Google Scholar]
  43. Lumsden DE, Kaminska M, Ashkan K, Selway R, Lin JP 2017. Deep brain stimulation for childhood dystonia: Is ‘where’ as important as in ‘whom’. Eur. J. Paediatr. Neurol. 21:176–84
    [Google Scholar]
  44. Lunardini F, Bertucco M, Casellato C, Bhanpuri N, Pedrocchi A, Sanger TD 2015a. Speed-accuracy trade-off in a trajectory-constrained self-feeding task: a quantitative index of unsuppressed motor noise in children with dystonia. J. Child Neurol. 30:1676–85
    [Google Scholar]
  45. Lunardini F, Maggioni S, Casellato C, Bertucco M, Pedrocchi AL, Sanger TD 2015b. Increased task-uncorrelated muscle activity in childhood dystonia. J. Neuroeng. Rehabil. 12:52
    [Google Scholar]
  46. Malfait N, Sanger TD 2007. Does dystonia always include co-contraction? A study of unconstrained reaching in children with primary and secondary dystonia. Exp. Brain Res. 176:206–16
    [Google Scholar]
  47. Matsumoto RR, Pouw B 2000. Correlation between neuroleptic binding to σ1 and σ2 receptors and acute dystonic reactions. Eur. J. Pharmacol. 401:155–60
    [Google Scholar]
  48. McClelland VM, Valentin A, Rey HG, Lumsden DE, Elze MC et al. 2016. Differences in globus pallidus neuronal firing rates and patterns relate to different disease biology in children with dystonia. J. Neurol. Neurosurg. Psychiatry 87:958–67
    [Google Scholar]
  49. McMahon TA 1984. Muscles, Reflexes, and Locomotion Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  50. Milardi D, Arrigo A, Anastasi G, Cacciola A, Marino S et al. 2016. Extensive direct subcortical cerebellum-basal ganglia connections in human brain as revealed by constrained spherical deconvolution tractography. Front. Neuroanat. 10:29
    [Google Scholar]
  51. Mink JW 1996. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50:381–425
    [Google Scholar]
  52. Molloy F, Carr T, Zeuner K, Dambrosia J, Hallett M 2003. Abnormalities of spatial discrimination in focal and generalized dystonia. Brain 126:2175–82
    [Google Scholar]
  53. Nashed JY, Crevecoeur F, Scott SH 2014. Rapid online selection between multiple motor plans. J. Neurosci. 34:1769–80
    [Google Scholar]
  54. Neychev VK, Gross RE, Lehéricy S, Hess EJ, Jinnah H 2011. The functional neuroanatomy of dystonia. Neurobiol. Dis. 42:185–201
    [Google Scholar]
  55. Patel N, Jankovic J, Hallett M 2014. Sensory aspects of movement disorders. Lancet Neurol 13:100–12
    [Google Scholar]
  56. Perlmutter J, Tempel L, Black K, Parkinson D, Todd R 1997. MPTP induces dystonia and Parkinsonism. Clues to the pathophysiology of dystonia. Neurology 49:1432–38
    [Google Scholar]
  57. Pizoli CE, Jinnah HA, Billingsley ML, Hess EJ 2002. Abnormal cerebellar signaling induces dystonia in mice. J. Neurosci. 22:7825–33
    [Google Scholar]
  58. Quartarone A, Hallett M 2013. Emerging concepts in the physiological basis of dystonia. Mov. Disord. 28:958–67
    [Google Scholar]
  59. Quartarone A, Siebner HR, Rothwell J 2006. Task-specific hand dystonia: Can too much plasticity be bad for you. Trends Neurosci 29:192–99
    [Google Scholar]
  60. Raymond JL, Lisberger SG, Mauk MD 1996. The cerebellum: a neuronal learning machine. Science 272:1126–31
    [Google Scholar]
  61. Romo R, Schultz W 1990. Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J. Neurophysiol. 63:592–606
    [Google Scholar]
  62. Ruge D, Tisch S, Hariz MI, Zrinzo L, Bhatia KP et al. 2011. Deep brain stimulation effects in dystonia: time course of electrophysiological changes in early treatment. Mov. Disord. 26:1913–21
    [Google Scholar]
  63. Saint Hilaire M, Burke R, Bressman S, Brin M, Fahn S 1991. Delayed-onset dystonia due to perinatal or early childhood asphyxia. Neurology 41:216–22
    [Google Scholar]
  64. Sako W, Murakami N, Izumi Y, Kaji R 2015. Val66Met polymorphism of brain-derived neurotrophic factor is associated with idiopathic dystonia. J. Clin. Neurosci. 22:575–77
    [Google Scholar]
  65. Sanger TD 2003a. Childhood onset generalised dystonia can be modelled by increased gain in the indirect basal ganglia pathway. J. Neurol. Neurosurg. Psychiatry 74:1509–15
    [Google Scholar]
  66. Sanger TD 2003b. Pathophysiology of pediatric movement disorders. J. Child Neurol. 18:Suppl. 1S9–24
    [Google Scholar]
  67. Sanger TD 2003c. Pediatric movement disorders. Curr. Opin. Neurol. 16:529–35
    [Google Scholar]
  68. Sanger TD 2004. Failure of motor learning for large initial errors. Neural. Comput. 16:1873–86
    [Google Scholar]
  69. Sanger TD 2012. Hyperkinetic disorders in childhood. Hyperkinetic Movement Disorders O Suchowersky, C Comella 965–99 New York: Humana Press
    [Google Scholar]
  70. Sanger TD 2014. Risk-aware control. Neural Comput 26:2669–91
    [Google Scholar]
  71. Sanger TD, Chen D, Delgado MR, Gaebler-Spira D, Hallett M, Mink JW 2006. Definition and classification of negative motor signs in childhood. Pediatrics 118:2159–67
    [Google Scholar]
  72. Sanger TD, Chen D, Fehlings DL, Hallett M, Lang AE et al. 2010. Definition and classification of hyperkinetic movements in childhood. Mov. Disord. 25:1538–49
    [Google Scholar]
  73. Sanger TD, Delgado MR, Gaebler-Spira D, Hallett M, Mink JW 2003. Classification and definition of disorders causing hypertonia in childhood. Pediatrics 111:e89–97
    [Google Scholar]
  74. Sanger TD, Ferman D 2017. Similarity of involuntary postures between different children with dystonia. Mov. Disord. Clin. Pract. 4:870–74
    [Google Scholar]
  75. Sanger TD, Henderson J, Lerner-Durham J 2007. Optimizing assisted communication devices for children with motor impairment using a model of information rate and channel capacity. IEEE Trans. Neural. Syst. Rehab. Eng. 15:458–68
    [Google Scholar]
  76. Sanger TD, Kaiser J, Placek B 2005. Reaching movements in childhood dystonia contain signal-dependent noise. J. Child Neurol. 20:489–96
    [Google Scholar]
  77. Sanger TD, Kukke SN 2007. Abnormalities of tactile sensory function in children with dystonic and diplegic cerebral palsy. J. Child Neurol. 22:289–93
    [Google Scholar]
  78. Sanger TD, Merzenich MM 2000. Computational model of the role of sensory disorganization in focal task-specific dystonia. J. Neurophysiol. 84:2458–64
    [Google Scholar]
  79. Sanger TD, Pascual-Leone A, Tarsy D, Schlaug G 2002. Nonlinear sensory cortex response to simultaneous tactile stimuli in writer's cramp. Mov. Disord. 17:105–11
    [Google Scholar]
  80. Sanger TD, Tarsy D, Pascual-Leone A 2001. Abnormalities of spatial and temporal sensory discrimination in writer's cramp. Mov. Disord. 16:94–99
    [Google Scholar]
  81. Scholz JP, Schöner G 1999. The uncontrolled manifold concept: identifying control variables for a functional task. Exp. Brain Res. 126:289–306
    [Google Scholar]
  82. Schultz W 1997. Dopamine neurons and their role in reward mechanisms. Curr. Opin. Neurobiol. 7:191–97
    [Google Scholar]
  83. Schultz W 1998. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80:1–27
    [Google Scholar]
  84. Scott BL, Jankovic J 1996. Delayed-onset progressive movement disorders after static brain lesions. Neurology 46:68–74
    [Google Scholar]
  85. Scott SH, Cluff T, Lowrey CR, Takei T 2015. Feedback control during voluntary motor actions. Curr. Opin. Neurobiol. 33:85–94
    [Google Scholar]
  86. Shadlen MN, Newsome WT 1994. Noise, neural codes and cortical organization. Curr. Opin. Neurobiol. 4:569–79
    [Google Scholar]
  87. Shadlen MN, Newsome WT 1998. The variable discharge of cortical neurons: implications for connectivity, computation, and information coding. J. Neurosci. 18:3870–96
    [Google Scholar]
  88. Shakkottai VG, Batla A, Bhatia K, Dauer WT, Dresel C et al. 2017. Current opinions and areas of consensus on the role of the cerebellum in dystonia. Cerebellum 16:577–94
    [Google Scholar]
  89. Sitburana O, Jankovic J 2008. Focal hand dystonia, mirror dystonia and motor overflow. J. Neurol. Sci. 266:31–33
    [Google Scholar]
  90. Sohn W-J, Niu C, Sanger T 2016. A neuromorphic model of motor overflow in focal hand dystonia due to correlated sensory input. J. Neural. Eng. 13:1741–51
    [Google Scholar]
  91. Svetel MV, Djuric G, Novakovic I, Dobricic V, Stefanova E et al. 2013. A common polymorphism in the brain-derived neurotrophic factor gene in patients with adult-onset primary focal and segmental dystonia. Acta Neurol. Belg. 113:243–45
    [Google Scholar]
  92. Tinazzi M, Priori A, Bertolasi L, Frasson E, Mauguiere F, Fiaschi A 2000. Abnormal central integration of a dual somatosensory input in dystonia. Evidence for sensory overflow. Brain 123:Pt. 142–50
    [Google Scholar]
  93. Todorov E, Jordan MI 2002. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5:1226–35
    [Google Scholar]
  94. Torres-Russotto D, Perlmutter JS 2008. Task-specific dystonias. Ann. N. Y. Acad. Sci. 1142:179–99
    [Google Scholar]
  95. Van Doornik J, Kukke S, Sanger TD 2009. Hypertonia in childhood secondary dystonia due to cerebral palsy is associated with reflex muscle activation. Mov. Disord. 24:965–71
    [Google Scholar]
  96. Van Vreeswijk C, Sompolinsky H 1996. Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724–26
    [Google Scholar]
  97. Vitek JL 2002. Pathophysiology of dystonia: a neuronal model. Mov. Disord. 17:S49–62
    [Google Scholar]
  98. Wichmann T, Delong MR 2016. Deep brain stimulation for movement disorders of basal ganglia origin: restoring function or functionality. Neurotherapeutics 13:264–83
    [Google Scholar]
  99. Young SJ, Bertucco M, Sanger TD 2014. Cathodal transcranial direct current stimulation in children with dystonia: a sham-controlled study. J. Child Neurol. 29:232–39
    [Google Scholar]
  100. Young SJ, Bertucco M, Sheehan-Stross R, Sanger TD 2013. Cathodal transcranial direct current stimulation in children with dystonia: a pilot open-label trial. J. Child Neurol. 28:1238–44
    [Google Scholar]
  101. Young SJ, van Doornik J, Sanger TD 2011. Visual feedback reduces co-contraction in children with dystonia. J. Child Neurol. 26:37–43
    [Google Scholar]
  102. Zeuner KE, Bara-Jimenez W, Noguchi PS, Goldstein SR, Dambrosia JM, Hallett M 2002. Sensory training for patients with focal hand dystonia. Ann. Neurol. 51:593–98
    [Google Scholar]
  103. Zeuner KE, Hallett M 2003. Sensory training as treatment for focal hand dystonia: a 1-year follow-up. Mov. Disord. 18:1044–47
    [Google Scholar]
  104. Zeuner KE, Molloy FM 2008. Abnormal reorganization in focal hand dystonia–sensory and motor training programs to retrain cortical function. NeuroRehabilitation 23:43–53
    [Google Scholar]
  105. Zhuang P, Li Y, Hallett M 2004. Neuronal activity in the basal ganglia and thalamus in patients with dystonia. Clin. Neurophysiol. 115:2542–57
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-080317-061504
Loading
/content/journals/10.1146/annurev-neuro-080317-061504
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error