A Review and Update on Tourette Syndrome: Where Is the Field Headed?

Movement Disorders (S Fox, Section Editor)
First Online:
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  1. This article is part of the Topical Collection on Movement Disorders

Abstract

Tourette syndrome (TS) is a childhood onset neurologic disorder with manifestations including multiple motor and phonic tics, and in most cases a variety of behavioral comorbidities such as attention deficit hyperactivity disorder, obsessive compulsive disorder, and other impulse control disorders. Although it is considered a hereditary disorder, likely modified by environmental factors, genetic studies have yet to uncover relevant causative genes and there is no animal model that mimics the broad clinical phenomenology of TS. There has been a marked increase in the number of neurophysiological, neuroimaging, and other studies on TS. The findings from these studies, however, have been difficult to interpret because of small sample sizes, variability of symptoms across patients, and comorbidities. Although anti-dopaminergic drugs are the most widely used medications in the treatment of TS, there has been increasing interest in other drugs, behavioral therapies, and surgical approaches including deep brain stimulation. Herein, we review the current literature and discuss the complexities of TS and the challenges in understanding its pathophysiology and in selecting the most appropriate treatment. We also offer an expert’s view of where the field of TS may be headed.

Keywords

Tourette syndrome Tic disorders Neurodevelopmental disorders Movement disorders 
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Notes

Acknowledgments

We would like to acknowledge the support of the TSA Center of Excellence located at the University of Florida Center for Movement Disorders and Neurorestoration. We would also like to acknowledge the following grant support NIH R34MH080764 (Okun), NIH R211NS072897 (Okun), and UF CTSI NIH KL2 Scholarship (Gunduz). The authors would also like to sincerely thank Drs. Don Gilbert, Tamara Hershey, Joseph Jankovic, Carol Mathews, Jon Mink, and Doug Woods for their insightful comments on this manuscript.

Authors’ contributions

Aysegul Gunduz planned the outline of the manuscript, performed the literature search, drafted the text, designed the tables and figures, and approved the manuscript. Michael S. Okun planned the outline of the manuscript, contributed to and edited the text, contributed to the tables and figures, and approved the manuscript.

Compliance with Ethical Standards

Funding Source

The authors were not paid to write this article by a pharmaceutical company or other agency.

Conflict of Interest

Aysegul Gunduz has received research grants from the Michael J. Fox Foundation, UF Clinical and Translational Sciences Institute, and DARPA. The institution and not Dr. Gunduz receives grants from Medtronic, and Dr. Gunduz has financial interest in these grants.

Michael S. Okun serves as a consultant for the National Parkinson Foundation and has received research grants from NIH, NPF, the Michael J. Fox Foundation, the Parkinson Alliance, Smallwood Foundation, the Bachmann-Strauss Foundation, the Tourette Syndrome Association, and the UF Foundation. Dr. Okun has previously received honoraria, but in the past >60 months has received no support from industry. Dr. Okun has received royalties for publications with Demos, Manson, Amazon, Smashwords, Books4Patients, and Cambridge (movement disorders books). Dr. Okun is an associate editor for New England Journal of Medicine Journal Watch Neurology. Dr. Okun has participated in CME and educational activities on movement disorders (in the last 36 months) sponsored by PeerView, Prime, Quantia, Henry Stewart, and by Vanderbilt University. The institution and not Dr. Okun receives grants from Medtronic, Abbvie, and ANS/St. Jude, and the PI has no financial interest in these grants. Dr. Okun has participated as a site PI and/or co-I for several NIH, foundation, and industry-sponsored trials over the years but has not received honoraria.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Trivet HA, Chien HF, Munhoz RP, Barbosa ER. Charcot’s contribution to the study of Tourette syndrome. Arq Neuropsiquiatr. 2008;66:918–21.CrossRefGoogle Scholar
  2. 2.
    Gilles de la Tourette G. Étude sur une affection nerveuse caractérisée par de l’incoordination motrice accompagnée d’écholalie et de coprolalie [French]. Arch Neurol. 1885;9:158–200.Google Scholar
  3. 3.
    Itard JM. Mémoire sur quelques functions involontaires des appareils de la locomotion, de la préhension et de la voix [French]. Arch Gen Med. 1825;8:385–407.Google Scholar
  4. 4.
    Trousseau A. Clinique Médicale de l’Hôtel Dieu de Paris Paris: J.-B. Bailliere; 1868.Google Scholar
  5. 5.
    Hughlings JJ. Clinical lectures and reports to the London Hospital. 1868;1.Google Scholar
  6. 6.
    McNaught KS, Mink JW. Advances in understanding and treatment of Tourette syndrome. Nat Rev Neurol. 2011;7:667–76.PubMedCrossRefGoogle Scholar
  7. 7.
    Kurlan R. Clinical practice. Tourette’s syndrome. N Engl J Med. 2010;363:2332–8.PubMedCrossRefGoogle Scholar
  8. 8.
    Singer HS. Tourette’s syndrome: from behaviour to biology. Lancet Neurol. 2005;4:149–59.PubMedCrossRefGoogle Scholar
  9. 9.
    Jankovic J. Phenomenology and classification of tics. Neurol Clin. 1997;15:267–75.PubMedCrossRefGoogle Scholar
  10. 10.
    Ganos C, Ogrzal T, Schnitzler A, Münchau A. The pathophysiology of echopraxia/echolalia: relevance to Gilles De La Tourette syndrome. Mov Disord. 2012;27:1222–9.PubMedCrossRefGoogle Scholar
  11. 11.
    Freeman RD, Zinner SH, Muller-Vahl KR, et al. Coprophenomena in Tourette syndrome. Dev Med Child Neurol. 2009;51:218–27.PubMedCrossRefGoogle Scholar
  12. 12.
    Hanna PA, Jankovic J. Sleep and tic disorders. Woburn: Butterworth-Heinemann; 2003.Google Scholar
  13. 13.
    Demirkiran M, Jankovic J. Paroxysmal dyskinesias—clinical-features and classification. Ann Neurol. 1995;38:571–9.PubMedCrossRefGoogle Scholar
  14. 14.
    Jankovic J. Tourette’s syndrome. N Engl J Med. 2001;345:1184–92.PubMedCrossRefGoogle Scholar
  15. 15.
    Leckman J, Walker D, Cohen D. Premonitory urges in Tourette’s syndrome. Am J Psychiatry 1993;150.Google Scholar
  16. 16.
    Kwak C, Vuong KD, Jankovic J. Premonitory sensory phenomenon in Tourette’s syndrome. Mov Disord. 2003;18:1530–3.PubMedCrossRefGoogle Scholar
  17. 17.
    Banaschewski T, Woerner W, Rothenberger A. Premonitory sensory phenomena and suppressibility of tics in Tourette syndrome: developmental aspects in children and adolescents. Dev Med Child Neurol. 2003;45:700–3.PubMedCrossRefGoogle Scholar
  18. 18.
    Rajagopal S, Cavanna AE. Premonitory urges and repetitive behaviours in adult patients with Tourette syndrome. Neurol Sci. 2014;35:969–71.PubMedCrossRefGoogle Scholar
  19. 19.
    Tallur K, Minns RA. Tourette’s syndrome. Paediatr Child Health. 2010;20:88–93.CrossRefGoogle Scholar
  20. 20.
    Hirschtritt ME, Lee PC, Pauls DL, et al. Lifetime prevalence, age of risk, and genetic relationships of comorbid psychiatric disorders in Tourette syndrome. JAMA Psychiatry. 2015;72:325–33.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Canitano R, Vivanti G. Tics and Tourette syndrome in autism spectrum disorders. Autism. 2007;11:19–28.PubMedCrossRefGoogle Scholar
  22. 22.
    Leckman JF. Tourette’s syndrome. Lancet. 2002;360:1577–86.PubMedCrossRefGoogle Scholar
  23. 23.
    Leckman JF, Zhang HP, Vitale A, et al. Course of tic severity in Tourette Syndrome: the first two decades. Pediatrics. 1998;102:14–9.PubMedCrossRefGoogle Scholar
  24. 24.
    Bloch MH, Peterson BS, Scahill L, et al. Adulthood outcome of tic and obsessive-compulsive symptom severity in children with Tourette syndrome. Arch Pediatr Adolesc Med. 2006;160:65–9.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.••
    Scharf JM, Miller LL, Gauvin CA, Alabiso J, Mathews CA, Ben-Shlomo Y. Population prevalence of Tourette syndrome: a systematic review and meta-analysis. Mov Disord. 2015;30(2):221–8. This study is a systematic review of published studies on TS prevalence. The authors performed random-effects meta-analysis weighted by sample size and meta-regressions to examine covariates that were potential sources of heterogeneity. This study refined the population prevalence estimate of TS in children to be 0.3 to 0.9 %.Google Scholar
  26. 26.
    Knight T, Steeves T, Day L, Lowerison M, Jette N, Pringsheim T. Prevalence of tic disorders: a systematic review and meta-analysis. Pediatr Neurol. 2012;47:77–90.PubMedCrossRefGoogle Scholar
  27. 27.
    Bitsko RH, Holbrook JR, Visser SN, et al. A national profile of Tourette syndrome. J Dev Behav Pediatr. 2014;35:317–22.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Cheung MY, Shahed J, Jankovic J. Malignant Tourette syndrome. Mov Disord. 2007;22(12):1743–50.PubMedCrossRefGoogle Scholar
  29. 29.
    Ganos C, Garrido A, Navalpotro-Gomez I, et al. Premonitory urge to tic in Tourette’s is associated with interoceptive awareness. Mov Disord 2015.Google Scholar
  30. 30.
    Grados MA, Mathews CA. Clinical phenomenology and phenotype variability in Tourette syndrome. J Psychosom Res. 2009;67:491–6.PubMedCrossRefGoogle Scholar
  31. 31.
    American Psychiatric Association. Diagnostic and Statistal Manual of Mental Disorders (DSM-V). Washington: American Psychiatric Association Press; 2012.Google Scholar
  32. 32.
    Jankovic J, Mejia N. Tics associated with other disorders. Philadelphia: Lippincott Williams & Wilkins; 2006.Google Scholar
  33. 33.
    Khalifa N, von Knorring A-L. Tourette syndrome and other tic disorders in a total population of children: clinical assessment and background. Acta Paediatr. 2007;94:1608–14.CrossRefGoogle Scholar
  34. 34.
    Hanna P, Janjua F, Contant C, Jankovic J. Bilineal transmission in Tourette syndrome. Neurology. 1999;53:813–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Pauls DL, Raymond CL, Stevenson JM, Leckman JF. A family study of Gilles de la Tourette syndrome. Am J Hum Genet 1991;48.Google Scholar
  36. 36.
    Hyde TM, Aaronson BA, Randolph C, Rickler KC, Weinberger DR. Relationship of birth weight to the phenotypic expression of Gilles de la Tourette’s syndrome in monozygotic twins. Neurology. 1992;42:652–8.PubMedCrossRefGoogle Scholar
  37. 37.
    Price RA, Kidd KK, Cohen DJ, Pauls DL, Leckman JF. A twin study of Tourette syndrome. Arch Gen Psychiatry. 1985;42:815–20.PubMedCrossRefGoogle Scholar
  38. 38.
    Davis LK, Yu D, Keenan CL, Gamazon ER, Konkashbaev AI, et al. Partitioning the heritability of Tourette syndrome and obsessive compulsive disorder reveals differences in genetic architecture. PLoS Genet 2013;9.Google Scholar
  39. 39.
    Deng H, Gao K, Jankovic J. The genetics of Tourette syndrome. Nat Rev Neurol. 2012;8:203–13.PubMedGoogle Scholar
  40. 40.
    Genetics TTSAICf. A complete genome screen in sib pairs affected by Gilles de la Tourette syndrome. Am J Hum Genet. 1999;65:1428–36.CrossRefGoogle Scholar
  41. 41.
    Genetics TTSAICf. Genome scan for Tourette disorder in affected-sibling-pair and multigenerational families. Am J Hum Genet. 2007;80:265–72.CrossRefGoogle Scholar
  42. 42.
    Roessner V, Plessen KJ, Rothenberger A, et al. European clinical guidelines for Tourette syndrome and other tic disorders. Part II: pharmacological treatment. Eur Child Adolesc Psychiatry. 2011;20:173–96.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Dietrich A, Fernandez TV, King RA, et al. The Tourette International collaborative genetics (TIC Genetics) study, finding the genes causing Tourette syndrome: objectives and methods. Eur Child Adolesc Psychiatry 2014.Google Scholar
  44. 44.
    Selling L. The role of infection in the etiology of tics. Arch Neurol Psychiatry. 1929;22:1163–71.CrossRefGoogle Scholar
  45. 45.
    Petek E, Windpassinger C, Vincent JB, et al. Disruption of a novel gene (IMMP2L) by a breakpoint in 7q31 associated with Tourette syndrome. Am J Hum Genet. 2001;68:848–58.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Patel C, Cooper-Charles L, McMullan DJ, Walker JM, Davison V, Morton J. Translocation breakpoint at 7q31 associated with tics: further evidence for IMMP2L as a candidate gene for Tourette syndrome. Eur J Hum Genet. 2011;19:634–9.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Bertelsen B, Melchior L, Jensen LR, et al. Intragenic deletions affecting two alternative transcripts of the IMMP2L gene in patients with Tourette syndrome. Eur J Hum Genet. 2014;22:1283–9.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Whatley SA, Curti D, Marchbanks RM. Mitochondrial involvement in schizophrenia and other functional psychoses. Neurochem Res. 1996;21:995–1004.PubMedCrossRefGoogle Scholar
  49. 49.
    Lin H, Williams KA, Katsovich L, et al. Streptococcal upper respiratory tract infections and psychosocial stress predict future tic and obsessive-compulsive symptom severity in children and adolescents with Tourette syndrome and obsessive-compulsive disorder. Biol Psychiatry. 2010;67:684–91.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Swedo SE, Leonard HL, Garvey MA, Mittleman B, Allen JP, Perlmutter JS. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases. Am J Psychiatry. 1998;155:264–71.PubMedGoogle Scholar
  51. 51.
    Mell LK, Davis RL, Owens D. Association between streptococcal infection and obsessive-compulsive disorder, Tourette’s syndrome, and tic disorder. Pediatrics. 2005;116:56–60.PubMedCrossRefGoogle Scholar
  52. 52.
    Kaplan EL. PANDAS? or PAND? Or Both? Or Neither? Assessing a possible temporal or pathogenetic relationship with the group A “strep- tococcal diseases complex”. Contemp Pediatr. 2000;8:81–96.Google Scholar
  53. 53.
    Kurlan R. Tourette’s syndrome and ‘PANDAS’: will the relationship bear out? Neurology. 1998;50:1530–4.PubMedCrossRefGoogle Scholar
  54. 54.
    Singer HS. PANDAS and immunomodulatory therapy: commentary. Lancet. 1999;354:1137–8.PubMedCrossRefGoogle Scholar
  55. 55.
    Kurlan R, Kaplan EL. The pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection (PANDAS) etiology for tics and obsessive-compulsive symptoms: hypothesis or entity? Practical considerations for the clinician. Pediatrics. 2004;113:883–6.PubMedCrossRefGoogle Scholar
  56. 56.
    Swedo SE, Leckman JF, Rose NR. From research subgroup to clinical syndrome: modifying the PANDAS criteria to describe PANS (Pediatric Acute-onset Neuropsychiatric Syndrome). Pediatrics & Therapeutics 2012;2.Google Scholar
  57. 57.
    Lerner A, Bagic A, Simmons JM, et al. Widespread abnormality of the γ-aminobutyric acid-ergic system in Tourette syndrome. Brain. 2012;135:1926–36.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    van der Salm S, Tijssen M, Koelman J, van Rootselaar A. The bereitschaftspotential in jerky movement disorders. J Neurol Neurosurg Psychiatry. 2012;83:1162–7.PubMedCrossRefGoogle Scholar
  59. 59.
    Patel N, Jankovic J, Hallett M. Sensory aspects of movement disorders. Lancet Neurol. 2014;13:100–12.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Albin RL, Young AB, Penney JB. The functional-anatomy of basal ganglia disorders. Trends Neurosci. 1989;12:366–75.PubMedCrossRefGoogle Scholar
  61. 61.
    Mink JW. The basal ganglia and involuntary movements—impaired inhibition of competing motor patterns. Arch Neurol. 2003;60:1365–8.PubMedCrossRefGoogle Scholar
  62. 62.
    Mink JW. Basal ganglia dysfunction in Tourette’s syndrome: a new hypothesis. Pediatr Neurol. 2001;25:190–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Albin RL, Mink JW. Recent advances in Tourette syndrome research. Trends Neurosci. 2006;29:175–82.PubMedCrossRefGoogle Scholar
  64. 64.
    Marceglia S, Servello D, Foffani G, et al. Thalamic single-unit and local field potential activity in Tourette syndrome. Mov Disord. 2010;25:300–8.PubMedCrossRefGoogle Scholar
  65. 65.•
    Maling N, Hashemiyoon R, Foote KD, Okun MS, Sanchez JC. Increased thalamic gamma band activity correlates with symptom relief following deep brain stimulation in humans with Tourette’s syndrome. PLoS One. 2012;7, e44215. This study presents the first chronic electrophysiological data in humans with TS, which shows correlation between increased gamma band activity and clinical improvement.Google Scholar
  66. 66.
    Shute J, Maling N, Rossi PJ, et al. Neural correlates of Tourette syndrome within the centromedian thalamus, premotor and primary motor cortices. Neuroscience Annual Meeting 2014; Washington, DC.Google Scholar
  67. 67.
    Franzkowiak S, Pollok B, Biermann-Ruben K, et al. Altered pattern of motor cortical activation-inhibition during voluntary movements in Tourette syndrome. Mov Disord. 2010;25:1960–6.PubMedCrossRefGoogle Scholar
  68. 68.
    Biermann-Ruben K, Miller A, Franzkowiak S, et al. Increased sensory feedback in Tourette syndrome. NeuroImage. 2012;63:119–25.PubMedCrossRefGoogle Scholar
  69. 69.
    Peterson BS, Thomas P, Kane MJ, et al. Basal ganglia volumes in patients with Gilles de la Tourette syndrome. Arch Gen Psychiatry. 2003;60:415–24.PubMedCrossRefGoogle Scholar
  70. 70.
    Bloch M, Leckman J, Zhu H, Peterson B. Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome. Neurology. 2005;65:1253–8.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Makki MI, Munian Govindan R, Wilson BJ, Behen ME, Chugani HT. Altered Fronto-Striato-Thalamic connectivity in children with tourette syndrome assessed with diffusion tensor MRI and probabilistic fiber tracking. J Child Neurol. 2009;24:669–78.PubMedCrossRefGoogle Scholar
  72. 72.
    Worbe Y, Gerardin E, Hartmann A, et al. Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain. 2010;133:3649–60.PubMedCrossRefGoogle Scholar
  73. 73.
    Thomalla G, Siebner HR, Jonas M, et al. Structural changes in the somatosensory system correlate with tic severity in Gilles de la Tourette syndrome. Brain. 2009;132:765–77.PubMedCrossRefGoogle Scholar
  74. 74.
    Cavanna AE, Stecco A, Rickards H, et al. Corpus callosum abnormalities in Tourette syndrome: an MRI-DTI study of monozygotic twins. J Neurol Neurosurg Psychiatry. 2010;81:533–5.PubMedCrossRefGoogle Scholar
  75. 75.
    Jackson SR, Parkinson A, Jung J, et al. Compensatory neural reorganization in Tourette syndrome. Curr Biol. 2011;21:580–5.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Bäumer T, Thomalla G, Kroeger J, et al. Interhemispheric motor networks are abnormal in patients with Gilles de la Tourette syndrome. Mov Disord. 2010;25:2828–37.PubMedCrossRefGoogle Scholar
  77. 77.•
    Muellner J, Delmaire C, Valabrégue R, et al. Altered structure of cortical sulci in Gilles de la Tourette syndrome: further support for abnormal brain development. Mov Disord. 2015;30:655–61. This comprehensive study with 52 adult patients with TS (and 52 matched controls) shows abnormal structural patterns of cortical sulci, which correlated with severity of clinical symptoms.Google Scholar
  78. 78.
    Bohlhalter S. Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain. 2006;129:2029–37.PubMedCrossRefGoogle Scholar
  79. 79.
    Debes N, Hansen A, Skov L, Larsson H. A functional magnetic resonance imaging study of a large clinical cohort of children with Tourette syndrome. J Child Neurol. 2011;26:560–9.PubMedCrossRefGoogle Scholar
  80. 80.
    Mazzone L, Yu S, Blair C, et al. An FMRI study of frontostriatal circuits during the inhibition of eye blinking in persons with Tourette syndrome. Am J Psychiat. 2010; 341–9.Google Scholar
  81. 81.
    Worbe Y, Malherbe C, Hartmann A, et al. Functional immaturity of cortico-basal ganglia networks in Gilles de la Tourette syndrome. Brain. 2012;135:1937–46.PubMedCrossRefGoogle Scholar
  82. 82.
    Singer HS, Gilbert DL, Wolf DS, Mink JW, Kurlan R. Moving from PANDAS to CANS. J Pediatr. 2012;160:725–31.PubMedCrossRefGoogle Scholar
  83. 83.
    Roessner V, Schoenefeld K, Buse J, Bender S, Ehrlich S, Munchau A. Pharmacological treatment of tic disorders and Tourette syndrome. Neuropharmacology. 2013;68:143–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Saporta ASD, Chugani HT, Juhász C, et al. Multimodality neuroimaging in Tourette syndrome: alpha-[11C] methyl-L-tryptophan positron emission tomography and diffusion tensor imaging studies. J Child Neurol. 2010;25:336–42.PubMedCrossRefGoogle Scholar
  85. 85.
    Wong DF, Brasic JR, Singer HS, et al. Mechanisms of dopaminergic and serotonergic neurotransmission in Tourette syndrome: clues from an in vivo neurochemistry study with PET. Neuropsychopharmacology. 2007;33(6):1239–51.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Singer HS. Neurochemical analysis of postmortem cortical and striatal brain tissue in patients with Tourette syndrome. Adv Neurol. 1992;58:135–44.PubMedGoogle Scholar
  87. 87.
    Swedo SE, Leonard HL, Kruesi MJP, et al. Cerebrospinal fluid neurochemistry in children and adolescents with obsessive-compulsive disorder. Arch Gen Psychiatry 1992;49.Google Scholar
  88. 88.
    Harris K, Singer HS. Tic disorders: neural circuits, neurochemistry, and neuroimmunology. J Child Neurol. 2006;21:678–89.PubMedCrossRefGoogle Scholar
  89. 89.
    Cheon KA, Ryu YH, Namkoong K, Kim CH, Kim JJ, Lee JD. Dopamine transporter density of the basal ganglia assessed with [123I]IPT SPECT in drug-naive children with Tourette’s disorder. Psychiatry Res. 2004;130:85–95.PubMedCrossRefGoogle Scholar
  90. 90.
    Serra-Mestres J, Ring H, Costa D. Dopamine transporter binding in Gilles de la Tourette syndrome: a [123I]FP-CIT/ SPECT study. Acta Psychiatr Scand. 2004;109:140–6.PubMedCrossRefGoogle Scholar
  91. 91.
    Minzer K, Lee O, Hong JJ, Singer HS. Increased prefrontal D2 protein in Tourette syndrome: a postmortem analysis of frontal cortex and striatum. J Neurol Sci. 2004;219:55–61.PubMedCrossRefGoogle Scholar
  92. 92.
    Wong DF, Singer HS, Brandt J, et al. D2-like dopamine receptor density in Tourette syndrome measured by PET. J Nucl Med. 1997;38:1243–7.PubMedGoogle Scholar
  93. 93.
    Albin RL, Koeppe RA, Wernette K, et al. Striatal [11C]dihydrotetrabenazine and [11C]methylphenidate binding in Tourette syndrome. Neurology. 2009;72:1390–6.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Müller-Vahl KR, Meyer GJ, Knapp WH, et al. Serotonin transporter binding in Tourette syndrome. Neurosci Lett. 2005;385:120–5.PubMedCrossRefGoogle Scholar
  95. 95.
    Steeves TDL, Ko JH, Kideckel DM, et al. Extrastriatal dopaminergic dysfunction in Tourette syndrome. Ann Neurol. 2010;67:170–81.PubMedCrossRefGoogle Scholar
  96. 96.••
    Xu M, Kobets AJ, Du J-C, et al. Targeted ablation of cholinergic interneurons in the dorsolateral striatum produces behavioral manifestations of Tourette syndrome. Proc Natl Acad Sci PNAS. 2015;112:893–8. The authors developed a strategy for targeted ablation of cholinergic interneurons in the mice dorsolateral striatum, which demonstrated for the first time that these interneurons can cause behavioral changes that resemble aspects of TS.Google Scholar
  97. 97.
    Castellan Baldan L, Williams KA, Gallezot J-D, et al. Histidine decarboxylase deficiency causes tourette syndrome: parallel findings in humans and mice. Neuron. 2014;81:77–90.PubMedCrossRefGoogle Scholar
  98. 98.
    Singer HS. Treatment of tics and tourette syndrome. Curr Treat Options Neurol. 2010;12:539–61.PubMedCrossRefGoogle Scholar
  99. 99.
    Jankovic J. Treatment of hyperkinetic movement disorders. Lancet Neurol. 2009;8:844–56.PubMedCrossRefGoogle Scholar
  100. 100.
    Conelea CA, Woods DW, Zinner SH, et al. Exploring the impact of chronic tic disorders on youth: results from the Tourette syndrome impact survey. Child Psychiatry Hum Dev. 2011;42:219–42.PubMedCrossRefGoogle Scholar
  101. 101.
    Leckman JF, Riddle MA, Hardin MT, et al. The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry. 1989;28:566–73.PubMedCrossRefGoogle Scholar
  102. 102.
    Goetz CG, Pappert EJ, Louis ED, Raman R, Leurgans S. Advantages of a modified scoring method for the Rush Video-Based Tic Rating Scale. Mov Disord. 1999;14:502–6.PubMedCrossRefGoogle Scholar
  103. 103.
    Ackermans L, Duits A, van der Linden C, et al. Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain 2011; 832–44.Google Scholar
  104. 104.
    Maciunas RJ, Maddux BN, Riley DE, et al. Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. J Neurosurg. 2007;107:1004–14.PubMedCrossRefGoogle Scholar
  105. 105.
    Wilhelm S, Deckersbach T, Coffey BJ, Bohne A, Peterson AL, Baer L. Habit reversal vs supportive psychotherapy for Tourette’s disorder: a randomized controlled trial. Am J Psychiatry. 2003;160:1175–6.PubMedCrossRefGoogle Scholar
  106. 106.
    Deckersbach T, Rauch S, Buhlmann U, Wilhelm S. Habit reversal vs supportive psychotherapy in Tourette’s disorder: a randomized controlled trial and predictors of treatment response. Behav Res Ther. 2006;44:1079–90.PubMedCrossRefGoogle Scholar
  107. 107.
    Piacentini J, Woods DW, Scahill L, et al. Behavior therapy for children with Tourette disorder a randomized controlled trial. JAMA J Am Med Assoc. 2010;303:1929–37.CrossRefGoogle Scholar
  108. 108.
    Wilhelm S, Peterson AL, Piacentini J, et al. Randomized trial of behavior therapy for adults with Tourette syndrome. Arch Gen Psychiatry. 2012;69:795–803.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    O’connor KP, Laverdure A, Taillon A, Stip E, Borgeat F, Lavoie M. Cognitive behavioral management of Tourette’s syndrome and chronic tic disorder in medicated and unmedicated samples. Behav Res Ther. 2009;47:1090–5.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Verdellen CWJ, Keijsers GPJ, Cath DC, Hoogduin CAL. Exposure with response prevention versus habit reversal in Tourettes’s syndrome: a controlled study. Behav Res Ther. 2004;42:501–11.PubMedCrossRefGoogle Scholar
  111. 111.
    Wile DJ, Pringsheim TM. Behavior therapy for Tourette syndrome: a systematic review and meta-analysis. Curr Treat Options Neurol. 2013;15:385–95.PubMedCrossRefGoogle Scholar
  112. 112.
    McGuire J, Piacentini J, Brennan E, et al. A meta-analysis of behavior therapy for Tourette syndrome. J Psychiatr Res. 2014;50:106–12.PubMedCrossRefGoogle Scholar
  113. 113.
    Weisman H, Qureshi IA, Leckman JF, Scahill L, Bloch MH. Systematic review: pharmacological treatment of tic disorders—efficacy of antipsychotic and alpha-2 adrenergic agonist agents. Neurosci Biobehav Rev. 2013;37:1162–71.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Scahill L, Chappell PB, Kim YS, et al. A placebo-controlled study of guanfacine in the treatment of children with tic disorders and attention deficit hyperactivity disorder. Am J Psychiatry. 2001;158:1067–74.PubMedCrossRefGoogle Scholar
  115. 115.
    Leckman JF, Cohen DJ, Detlor J, Young JG, Harcherik D, Shaywitz BA. Clonidine in the treatment of Tourette syndrome: a review of data. Adv Neurol. 1982;35:391–401.PubMedGoogle Scholar
  116. 116.
    Kushner HI. From Gilles de la Tourette’s disease to Tourette syndrome: a history. CNS Spectr. 1999;4:24–35.Google Scholar
  117. 117.
    Pena MS, Yaltho TC, Jankovic J. Tardive dyskinesia secondary to Aripiprazole. Ann Neurol. 2010;68:S21–S.Google Scholar
  118. 118.
    Wijemanne S, Wu L, Jankovic J. Long-term efficacy and safety of fluphenazine in patients with Tourette syndrome. Mov Disord. 2014;29:126–30.PubMedCrossRefGoogle Scholar
  119. 119.
    Ondo WG, Jong D, Davis A. Comparison of weight gain in treatments for Tourette syndrome: tetrabenazine versus neuroleptic drugs. J Child Neurol. 2008;23:435–7.PubMedCrossRefGoogle Scholar
  120. 120.
    Kenney C, Hunter C, Mejia N, Jankovic J. Tetrabenazine in the treatment of Tourette syndrome. J Pediatr Neurol. 2007;5:9–13.Google Scholar
  121. 121.
    Jimenez-Shahed J, Jankovic J. Tetrabenazine for treatment of chorea associated with Huntington’s disease. Expert Opin Orphan Drugs. 2013;1:423–36.CrossRefGoogle Scholar
  122. 122.
    Jankovic J, Jimenez-Shahed J, Brown LW. A randomised, double-blind, placebo-controlled study of topiramate in the treatment of Tourette syndrome. J Neurol Neurosurg Psychiatry. 2010;81:70–3.PubMedCrossRefGoogle Scholar
  123. 123.
    Marras C, Andrews D, Sime E, Lang A. Botulinum toxin for simple motor tics: a randomized, double-blind, controlled clinical trial. Neurology. 2001;56:605–10.PubMedCrossRefGoogle Scholar
  124. 124.
    Viswanathan A, Jimenez-Shahed J, Baizabal Carvallo J, Jankovic J. Deep brain stimulation for Tourette syndrome: target selection. Stereotact Funct Neurosurg. 2012;90:213–24.PubMedCrossRefGoogle Scholar
  125. 125.
    Hassler R, Dieckmann G. Traitement stéréotaxique des tics et cris inarticulés ou coprolaliques considérés comme phenomena d’obsession motrice au cours de la maladie de Gilles de la Tourette. Rev Neurol (Paris). 1970;123:89–100.Google Scholar
  126. 126.•
    Tourette Syndrome Association International Deep Brain Stimulation (DBS) Database and Registry Study Group. Tourette syndrome deep brain stimulation: a review and updated recommendations. Move Disord in press. This paper presents a review of all reported cases of TS DBS and provides updated recommendations for selection, assessment, and management of potential TS DBS cases based on the literature and implantation experience.Google Scholar
  127. 127.
    Shprecher DR, Schrock L, Himle M. Neurobehavioral aspects, pathophysiology, and management of Tourette syndrome. Curr Opin Neurol. 2014;27:484–92.PubMedCrossRefGoogle Scholar
  128. 128.
    Okun MS, Fernandez HH, Foote KD, Murphy TK, Goodman WK. Avoiding deep brain stimulation failures in Tourette syndrome. J Neurol Neurosurg Psychiatry. 2008;79:111–2.PubMedCrossRefGoogle Scholar
  129. 129.
    Le K, Liu L, Sun M, Hu L, Xiao N. Transcranial magnetic stimulation at 1 Hertz improves clinical symptoms in children with Tourette syndrome for at least 6 months. J Clin Neurosci. 2013;20:257–62.PubMedCrossRefGoogle Scholar
  130. 130.
    Kwon HJ, Lim WS, Lim MH, et al. 1-Hz low frequency repetitive transcranial magnetic stimulation in children with Tourette’s syndrome. Neurosci Lett. 2011;492:1–4.PubMedCrossRefGoogle Scholar
  131. 131.
    Ganos C, Roessner V, Münchau A. The functional anatomy of Gilles de la Tourette syndrome. Neurosci Biobehav Rev 2013; 1050–62.Google Scholar
  132. 132.
    Rossi PJ, Shute J, Gunduz A, Bowers D, Foote KD, Okun MS. Fewer than 2 hours of daily thalamic stimulation reduces tics in Tourette syndrome: two-year follow-up of scheduled deep brain stimulation. Brain 2014;submitted.Google Scholar
  133. 133.
    Almeida L, Martinez-Ramirez D, Rossi PJ, Peng Z, Gunduz A, Okun MS. Chasing tics in the Human brain: development of open, scheduled and closed loop responsive approaches to deep brain stimulation for Tourette syndrome. J Clin Neurol 2015;11.Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.J. Crayton Pruitt Family Department of Biomedical EngineeringGainesvilleUSA
  2. 2.UF Health Center for Movement Disorders and NeurorestorationGainesvilleUSA
  3. 3.Department of NeurologyUniversity of FloridaGainesvilleUSA
  4. 4.Department of NeurosurgeryUniversity of FloridaGainesvilleUSA

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