Skip to main content
SpringerLink
Log in

Correlates and Clinical Implications of Tic Suppressibility

  • Tourette’s Syndrome (M Yadegar and E Ricketts, Section Editors)
  • Published:
Current Developmental Disorders Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Tic disorders are common in the pediatric population and are differentiated from other movement disorders by tic suppressibility. Understanding the mechanism of tic suppression may provide new insights to the pathophysiology of tic disorders. This article highlights clinical phenomenology and neuronal correlates of tic suppressibility.

Recent Findings

Recent studies suggest that tic suppressibility exists in children shortly after onset of their tics. Moreover, those who are better able to suppress their tics have better tic outcomes. Interoceptive awareness and automatic action inhibition may be involved in tic suppression.

Summary

We illustrate a possible underlying mechanism of tic suppressibility and its clinical correlations and implications. New concepts such as interoceptive awareness and action inhibition may help explain tic disorders. Further study will be useful to fill remaining knowledge gaps.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

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

  1. American Psychiatric Association. Diagnostic and statistical manual of mental disorders (DSM-5®): American Psychiatric Pub; 2013.

  2. Snider LA, Seligman LD, Ketchen BR, Levitt SJ, Bates LR, Garvey MA, et al. Tics and problem behaviors in schoolchildren: prevalence, characterization, and associations. Pediatrics. 2002;110:331–6. https://doi.org/10.1542/peds.110.2.331.

    Article  PubMed  Google Scholar 

  3. Kurlan R, McDermott MP, Deeley C, Como PG, Brower C, Eapen S, et al. Prevalence of tics in schoolchildren and association with placement in special education. Neurology. 2001;57:1383–8. https://doi.org/10.1212/wnl.57.8.1383.

    Article  CAS  PubMed  Google Scholar 

  4. Black KJ, Black ER, Greene DJ, Schlaggar BL. Provisional tic disorder: what to tell parents when their child first starts ticcing. F1000Res. 2016;5:696. https://doi.org/10.12688/f1000research.8428.1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Leckman JF, Zhang H, Vitale A, Lahnin F, Lynch K, Bondi C, et al. Course of tic severity in Tourette syndrome: the first two decades. Pediatrics. 1998;102:14–9. https://doi.org/10.1542/peds.102.1.14.

    Article  CAS  PubMed  Google Scholar 

  6. Mink JW. The basal ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arch Neurol. 2003;60:1365–8. https://doi.org/10.1001/archneur.60.10.1365.

    Article  PubMed  Google Scholar 

  7. Woods DW, Piacentini J, Himle MB, Chang S. Premonitory Urge for Tics Scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with tic disorders. J Dev Behav Pediatr. 2005;26:397–403. https://doi.org/10.1097/00004703-200512000-00001.

    Article  PubMed  Google Scholar 

  8. Bliss J, Cohen DJ, Freedman DX. Sensory experiences of Gilles de la Tourette syndrome. Arch Gen Psychiatry. 1980;37:1343–7. https://doi.org/10.1001/archpsyc.1980.01780250029002.

    Article  CAS  PubMed  Google Scholar 

  9. Leckman JF. Tourette’s syndrome. Lancet. 2002;360:1577–86. https://doi.org/10.1016/S0140-6736(02)11526-1.

    Article  PubMed  Google Scholar 

  10. Jankovic J. Tourette syndrome. Phenomenology and classification of tics. Neurol Clin. 1997;15:267–75. https://doi.org/10.1016/s0733-8619(05)70311-x.

    Article  CAS  PubMed  Google Scholar 

  11. Koller WC, Biary NM. Volitional control of involuntary movements. Mov Disord. 1989;4:153–6. https://doi.org/10.1002/mds.870040207.

    Article  CAS  PubMed  Google Scholar 

  12. Matsuda N, Kono T, Nonaka M, Fujio M, Kano Y. Self-initiated coping with Tourette’s syndrome: effect of tic suppression on QOL. Brain Dev. 2016;38:233–41. https://doi.org/10.1016/j.braindev.2015.08.006.

    Article  PubMed  Google Scholar 

  13. Wadman R, Glazebrook C, Beer C, Jackson GM. Difficulties experienced by young people with Tourette syndrome in secondary school: a mixed methods description of self, parent and staff perspectives. BMC Psychiatry. 2016;16:14. https://doi.org/10.1186/s12888-016-0717-9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Meidinger AL, Miltenberger RG, Himle M, Omvig M, Trainor C, Crosby R. An investigation of tic suppression and the rebound effect in Tourette’s disorder. Behav Modif. 2005;29:716–45. https://doi.org/10.1177/0145445505279262.

    Article  PubMed  Google Scholar 

  15. Himle MB, Woods DW. An experimental evaluation of tic suppression and the tic rebound effect. Behav Res Ther. 2005;43:1443–51. https://doi.org/10.1016/j.brat.2004.11.002.

    Article  PubMed  Google Scholar 

  16. Woods DW, Himle MB. Creating tic suppression: comparing the effects of verbal instruction to differential reinforcement. J Appl Behav Anal. 2004;37:417–20. https://doi.org/10.1901/jaba.2004.37-417.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Woods DW, Himle MB, Miltenberger RG, Carr JE, Osmon DC, Karsten AM, et al. Durability, negative impact, and neuropsychological predictors of tic suppression in children with chronic tic disorder. J Abnorm Child Psychol 2008;36:237–45. https://doi.org/10.1007/s10802-007-9173-9.

  18. Ganos C, Bongert J, Asmuss L, Martino D, Haggard P, Münchau A. The somatotopy of tic inhibition: Where and how much?. Mov Disord 2015;30:1184–9. https://doi.org/10.1002/mds.26188.

  19. Goetz CG, Leurgans S, Chmura TA. Home alone: methods to maximize tic expression for objective videotape assessments in Gilles de la Tourette syndrome. Mov Disord 2001;16:693–7. https://doi.org/10.1002/mds.1159.

  20. Brandt VC, Lynn MT, Obst M, Brass M, Münchau A. Visual feedback of own tics increases tic frequency in patients with Tourette’s syndrome. Cogn Neurosci 2015;6:1–7. https://doi.org/10.1080/17588928.2014.954990.

  21. Misirlisoy E, Brandt V, Ganos C, Tübing J, Münchau A, Haggard P. The relation between attention and tic generation in Tourette syndrome. Neuropsychology. 2015;29:658–65. https://doi.org/10.1037/neu0000161.

    Article  PubMed  Google Scholar 

  22. Specht MW, Woods DW, Nicotra CM, Kelly LM, Ricketts EJ, Conelea CA, et al. Effects of tic suppression: ability to suppress, rebound, negative reinforcement, and habituation to the premonitory urge. Behav Res Ther. 2013;51:24–30. https://doi.org/10.1016/j.brat.2012.09.009.

    Article  PubMed  Google Scholar 

  23. •• Conelea CA, Wellen B, Woods DW, Greene DJ, Black KJ, Specht M, et al. Patterns and predictors of tic suppressibility in youth with tic disorders. Front Psychiatry. 2018;9:188. https://doi.org/10.3389/fpsyt.2018.00188This study gathers results from the previous TST studies and discusses patterns and clinical correlates of reward-enhanced tic suppression.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Himle MB, Woods DW, Bunaciu L. Evaluating the role of contingency in differentially reinforced tic suppression. J Appl Behav Anal. 2008;41:285–9. https://doi.org/10.1901/jaba.2008.41-285.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Woods DW, Walther MR, Bauer CC, Kemp JJ, Conelea CA. The development of stimulus control over tics: a potential explanation for contextually-based variability in the symptoms of Tourette syndrome. Behav Res Ther. 2009;47:41–7. https://doi.org/10.1016/j.brat.2008.10.013.

    Article  PubMed  Google Scholar 

  26. 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. https://doi.org/10.1017/s0012162203001294.

    Article  PubMed  Google Scholar 

  27. Greene DJ, Koller JM, Robichaux-Viehoever A, Bihun EC, Schlaggar BL, Black KJ. Reward enhances tic suppression in children within months of tic disorder onset. Dev Cogn Neurosci. 2015;11:65–74. https://doi.org/10.1016/j.dcn.2014.08.005.

    Article  PubMed  Google Scholar 

  28. • Kim S, Greene DJ, Robichaux-Viehoever A, et al. Tic suppression in children with recent-onset tics predicts 1-year tic outcome. J Child Neurol. 2019;34:757–64. https://doi.org/10.1177/0883073819855531This study demonstrates prognostic value of tic suppression early after the onset of tics.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Robertson MM, Banerjee S, Kurlan R, Cohen DJ, Leckman JF, McMahon W, et al. The Tourette syndrome diagnostic confidence index: development and clinical associations. Neurology. 1999;53:2108–12. https://doi.org/10.1212/wnl.53.9.2108.

    Article  CAS  PubMed  Google Scholar 

  30. Marcks BA, Woods DW, Teng EJ, Twohig MP. What do those who know, know? Investigating providers’ knowledge about Tourette’s syndrome and its treatment. Cogn Behav Pract. 2004;11:298–305. https://doi.org/10.1016/S1077-7229(04)80044-0.

    Article  Google Scholar 

  31. Verdellen CW, Hoogduin CA, Keijsers GP. Tic suppression in the treatment of Tourette’s syndrome with exposure therapy: the rebound phenomenon reconsidered. Mov Disord. 2007;22:1601–6. https://doi.org/10.1002/mds.21577.

    Article  PubMed  Google Scholar 

  32. Franklin ME, Best SH, Wilson MA, Loew B, Compton SN. Habit reversal training and acceptance and commitment therapy for Tourette syndrome: a pilot project. J Dev Phys Disabil. 2011;23:49–60. https://doi.org/10.1007/s10882-010-9221-1.

    Article  Google Scholar 

  33. O’Connor K, St-Pierre-Delorme MÈ, Leclerc J, Lavoie M, Blais MT. Meta-cognitions in Tourette syndrome, tic disorders, and body-focused repetitive disorder. Can J Psychiatry. 2014;59:417–25. https://doi.org/10.1177/070674371405900804.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Himle MB, Capriotti MR, Hayes LP, Ramanujam K, Scahill L, Sukhodolsky DG, et al. Variables associated with tic exacerbation in children with chronic tic disorders. Behav Modif. 2014;38:163–83. https://doi.org/10.1177/0145445514531016.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Robinson S, Hedderly T. Novel psychological formulation and treatment of “tic attacks” in Tourette syndrome. Front Pediatr. 2016;4:46. https://doi.org/10.3389/fped.2016.00046.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Leclerc JB, O’Connor KP. J.-Nolin G, Valois P, Lavoie ME. The effect of a new therapy for children with tics targeting underlying cognitive, behavioral, and physiological processes. Front. Psychiatry. 2016;7:135. https://doi.org/10.3389/fpsyt.2016.00135.

    Article  Google Scholar 

  37. Specht MW, Nicotra CM, Kelly LM, Woods DW, Ricketts EJ, Perry-Parrish C, et al. A comparison of urge intensity and the probability of tic completion during tic freely and tic suppression conditions. Behav Modif. 2014;38:297–318. https://doi.org/10.1177/0145445514537059.

    Article  PubMed  Google Scholar 

  38. Piacentini J, Woods DW, Scahill L, Wilhelm S, Peterson AL, Chang S, et al. Behavior therapy for children with Tourette disorder: a randomized controlled trial. JAMA. 2010;303:1929–37. https://doi.org/10.1001/jama.2010.607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Verdellen CW, Keijsers GP, Cath DC, Hoogduin CA. Exposure with response prevention versus habit reversal in Tourettes’s syndrome: a controlled study. Behav Res Ther. 2004;42:501–11. https://doi.org/10.1016/S0005-7967(03)00154-2.

  40. Conelea CA, Wellen BCM. Tic treatment goes tech: a review of TicHelper.com. Cogn Behav Pract. 2017;24:374–81. https://doi.org/10.1016/j.cbpra.2017.01.003.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Black JK, Black KJ. Software for web-based tic suppression training. F1000Res. 2017;6:2150. https://doi.org/10.12688/f1000research.13460.2.

    Article  PubMed  Google Scholar 

  42. Curatolo P, D’Agati E, Moavero R. The neurobiological basis of ADHD. Italian Journal of Pediatrics. 2010;36:79. https://doi.org/10.1186/1824-7288-36-79.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Sambrani T, Jakubovski E, Müller-Vahl KR. New insights into clinical characteristics of Gilles de la Tourette syndrome: findings in 1032 patients from a single German center. Front Neurosci. 2016;10:415. https://doi.org/10.3389/fnins.2016.00415.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Morand-Beaulieu S, Grot S, Lavoie J, Leclerc JB, Luck D, Lavoie ME. The puzzling question of inhibitory control in Tourette syndrome: a meta-analysis. Neurosci Biobehav Rev. 2017;80:240–62. https://doi.org/10.1016/j.neubiorev.2017.05.006.

    Article  PubMed  Google Scholar 

  45. Deckersbach T, Rauch S, Buhlmann U, Wilhelm S. Habit reversal versus supportive psychotherapy in Tourette’s disorder: a randomized controlled trial and predictors of treatment response. Behav Res Ther. 2006;44:1079–90. https://doi.org/10.1016/j.brat.2005.08.007.

    Article  PubMed  Google Scholar 

  46. Challman TD, Lipsky JJ. Methylphenidate: its pharmacology and uses. Mayo Clin Proc. 2000;75:711–21. https://doi.org/10.4065/75.7.711.

    Article  CAS  PubMed  Google Scholar 

  47. Arnsten AF, Dudley AG. Methylphenidate improves prefrontal cortical cognitive function through alpha2 adrenoceptor and dopamine D1 receptor actions: relevance to therapeutic effects in attention deficit hyperactivity disorder. Behav Brain Funct. 2005;1:2. https://doi.org/10.1186/1744-9081-1-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Tourette's Syndrome Study Group. Treatment of ADHD in children with tics: a randomized controlled trial. Neurology. 2002;58:527–36. https://doi.org/10.1212/wnl.58.4.527.

    Article  Google Scholar 

  49. Lyon GJ, Samar SM, Conelea C, Trujillo MR, Lipinski CM, Bauer CC, et al. Testing tic suppression: comparing the effects of dexmethylphenidate to no medication in children and adolescents with attention-deficit/hyperactivity disorder and Tourette’s disorder. J Child Adolesc Psychopharmacol. 2010;20:283–9. https://doi.org/10.1089/cap.2010.0032.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Brandt VC, Beck C, Sajin V, Baaske MK, Bäumer T, Beste C, et al. Temporal relationship between premonitory urges and tics in Gilles de la Tourette syndrome. Cortex. 2016;77:24–37. https://doi.org/10.1016/j.cortex.2016.01.008.

    Article  PubMed  Google Scholar 

  51. Müller-Vahl KR, Riemann L, Bokemeyer S. Tourette patients’ misbelief of a tic rebound is due to overall difficulties in reliable tic rating. J Psychosom Res. 2014;76:472–6. https://doi.org/10.1016/j.jpsychores.2014.03.003.

    Article  PubMed  Google Scholar 

  52. Himle MB, Woods DW, Conelea CA, Bauer CC, Rice KA. Investigating the effects of tic suppression on premonitory urge ratings in children and adolescents with Tourette’s syndrome. Behav Res Ther. 2007;45:2964–76. https://doi.org/10.1016/j.brat.2007.08.007.

    Article  PubMed  Google Scholar 

  53. Capriotti MR, Brandt BC, Turkel JE, Lee HJ, Woods DW. Negative reinforcement and premonitory urges in youth with Tourette syndrome: an experimental evaluation. Behav Modif. 2014;38:276–96. https://doi.org/10.1177/0145445514531015.

    Article  PubMed  Google Scholar 

  54. Draper A, Jackson GM, Morgan PS, Jackson SR. Premonitory urges are associated with decreased grey matter thickness within the insula and sensorimotor cortex in young people with Tourette syndrome. J Neuropsychol. 2016;10:143–53. https://doi.org/10.1111/jnp.12089.

    Article  PubMed  Google Scholar 

  55. • Kyriazi M, Kalyva E, Vargiami E, Krikonis K, Zafeiriou D. Premonitory urges and their link with tic severity in children and adolescents with tic disorders. Front Psychiatry. 2019;10:569. https://doi.org/10.3389/fpsyt.2019.00569This study explored relationship between premonitory urge and tic severity.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Verdellen CW, Hoogduin CA, Kato BS, Keijsers GP, Cath DC, Hoijtink HB. Habituation of premonitory sensations during exposure and response prevention treatment in Tourette’s syndrome. Behav Modif. 2008;32:215–27. https://doi.org/10.1177/0145445507309020.

    Article  PubMed  Google Scholar 

  57. Houghton DC, Capriotti MR, Scahill LD, Wilhelm S, Peterson AL, Walkup JT, et al. Investigating habituation to premonitory urges in behavior therapy for tic disorders. Behav Ther. 2017;48:834–46. https://doi.org/10.1016/j.beth.2017.08.004.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Ganos C, Kahl U, Schunke O, Kühn S, Haggard P, Gerloff C, et al. Are premonitory urges a prerequisite of tic inhibition in Gilles de la Tourette syndrome? J Neurol Neurosurg Psychiatry. 2012;83:975–8. https://doi.org/10.1136/jnnp-2012-303033.

    Article  PubMed  Google Scholar 

  59. Conelea CA, Woods DW, Brandt BC. The impact of a stress induction task on tic frequencies in youth with Tourette syndrome. Behav Res Ther. 2011;49:492–7. https://doi.org/10.1016/j.brat.2011.05.006.

    Article  PubMed  Google Scholar 

  60. Craig AD. How do you feel--now? The anterior insula and human awareness. Nat Rev Neurosci. 2009;10:59–70. https://doi.org/10.1038/nrn2555.

    Article  CAS  PubMed  Google Scholar 

  61. Jackson SR, Parkinson A, Kim SY, Schüermann M, Eickhoff SB. On the functional anatomy of the urge-for-action. Cogn Neurosci. 2011;2:227–43. https://doi.org/10.1080/17588928.2011.604717.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ganos C, Garrido A, Navalpotro-Gómez I, Ricciardi L, Martino D, Edwards MJ, et al. Premonitory urge to tic in Tourette’s is associated with interoceptive awareness. Mov Disord. 2015;30:1198–202. https://doi.org/10.1002/mds.26228.

    Article  PubMed  Google Scholar 

  63. Ficarella SC, Battelli L. Motor preparation for action inhibition: a review of single pulse TMS studies using the Go/NoGo Paradigm. Front Psychol. 2019;10:340. https://doi.org/10.3389/fpsyg.2019.00340.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Stern ER, Blair C, Peterson BS. Inhibitory deficits in Tourette’s syndrome. Dev Psychobiol. 2008;50:9–18. https://doi.org/10.1002/dev.20266.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Serrien DJ, Orth M, Evans AH, Lees AJ, Brown P. Motor inhibition in patients with Gilles de la Tourette syndrome: functional activation patterns as revealed by EEG coherence. Brain. 2005;128:116–25. https://doi.org/10.1093/brain/awh318.

    Article  PubMed  Google Scholar 

  66. Ganos C, Kühn S, Kahl U, Schunke O, Feldheim J, Gerloff C, et al. Action inhibition in Tourette syndrome. Mov Disord. 2014;29:1532–8. https://doi.org/10.1002/mds.25944.

    Article  PubMed  Google Scholar 

  67. Jackson GM, Mueller SC, Hambleton K, Hollis CP. Enhanced cognitive control in Tourette syndrome during task uncertainty. Exp Brain Res. 2007;182:357–64. https://doi.org/10.1007/s00221-007-0999-8.

    Article  CAS  PubMed  Google Scholar 

  68. Mueller SC, Jackson GM, Dhalla R, Datsopoulos S, Hollis CP. Enhanced cognitive control in young people with Tourette’s syndrome. Curr Biol. 2006;16:570–3. https://doi.org/10.1016/j.cub.2006.01.064.

    Article  CAS  PubMed  Google Scholar 

  69. Jackson SR, Parkinson A, Jung J, Ryan SE, Morgan PS, Hollis C, et al. Compensatory neural reorganization in Tourette syndrome. Curr Biol. 2011;21:580–5. https://doi.org/10.1016/j.cub.2011.02.047.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. • Rawji V, Modi S, Latorre A, Rocchi L, Hockey L, Bhatia K, et al. Impaired automatic but intact volitional inhibition in primary tic disorders. Brain. 2020;143:906–19. https://doi.org/10.1093/brain/awaa024This paper looks at automatic inhibition in TS patients.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Stenner MP, Baumgaertel C, Heinze HJ, Ganos C, Müller-Vahl KR. Intact automatic motor inhibition in patients with Tourette syndrome. Mov Disord. 2018;33:1800–4. https://doi.org/10.1002/mds.27493.

    Article  PubMed  Google Scholar 

  72. • Botteron HE, Richards CA, Nishino T, Ueda K, Acevedo HK, Koller JM, et al. The urge to blink in Tourette syndrome. Cortex. 2019;120:556–66. https://doi.org/10.1016/j.cortex.2019.07.010This study proposes a novel event-related individualized model to explore BOLD activity specific to the urge to tic during tic suppression.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Peterson BS, Thomas P, Kane MJ, Scahill L, Zhang H, Bronen R, et al. Basal Ganglia volumes in patients with Gilles de la Tourette syndrome. Arch Gen Psychiatry. 2003;60:415–24. https://doi.org/10.1001/archpsyc.60.4.415.

    Article  PubMed  Google Scholar 

  74. •• Augustine F, Singer HS. Merging the pathophysiology and pharmacotherapy of tics. Tremor Other Hyperkinet Mov (N Y). 2019;8:595. https://doi.org/10.7916/D8H14JTXA useful review of the pathophysiology and current pharmacological treatment of tics.

    Article  Google Scholar 

  75. Church JA, Fair DA, Dosenbach NU, Cohen AL, Miezin FM, Petersen SE, et al. Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain. 2009;132:225–38. https://doi.org/10.1093/brain/awn223.

    Article  PubMed  Google Scholar 

  76. Yael D, Vinner E, Bar-Gad I. Pathophysiology of tic disorders. Mov Disord. 2015;30:1171–8. https://doi.org/10.1002/mds.26304.

    Article  PubMed  Google Scholar 

  77. Albin RL, Mink JW. Recent advances in Tourette syndrome research. Trends Neurosci. 2006;29:175–82. https://doi.org/10.1016/j.tins.2006.01.001.

    Article  CAS  PubMed  Google Scholar 

  78. Singer HS. Tourette’s syndrome: from behaviour to biology. Lancet Neurol. 2005;4:149–59. https://doi.org/10.1016/S1474-4422(05)01012-4.

    Article  PubMed  Google Scholar 

  79. • Nielsen AN, Gratton C, Church JA, Dosenbach NUF, Black KJ, Petersen SE, et al. Atypical functional connectivity in Tourette syndrome differs between children and adults. Biol Psychiatry. 2020;87:164–73. https://doi.org/10.1016/j.biopsych.2019.06.021This study demonstrates altered brain networks in patietns with tics.

    Article  PubMed  Google Scholar 

  80. Peterson BS, Skudlarski P, Andersen AW, Zhang H, Gatenby JC, Lacadie CM, et al. A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch Gen Psychiatry. 1998;55:326–33. https://doi.org/10.1001/archpsyc.55.4.326.

    Article  CAS  PubMed  Google Scholar 

  81. Alvarez JA, Emory E. Executive function and the frontal lobes: a meta-analytic review. Neuropsychol Rev. 2006;16:17–42. https://doi.org/10.1007/s11065-006-9002-x.

    Article  PubMed  Google Scholar 

  82. Aron AR. From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry. 2011;69:e55–68. https://doi.org/10.1016/j.biopsych.2010.07.024.

    Article  PubMed  Google Scholar 

  83. Swick D, Ashley V, Turken AU. Left inferior frontal gyrus is critical for response inhibition. BMC Neurosci. 2008;9:102. https://doi.org/10.1186/1471-2202-9-102.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Ganos C, Kahl U, Brandt V, Schunke O, Bäumer T, Thomalla G, et al. The neural correlates of tic inhibition in Gilles de la Tourette syndrome. Neuropsychologia. 2014;65:297–301. https://doi.org/10.1016/j.neuropsychologia.2014.08.007.

    Article  PubMed  Google Scholar 

  85. van der Salm SMA, van der Meer JN, Cath DC, Groot PFC, van der Werf YD, Brouwers E, et al. Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging. Neuroimage Clin. 2018;20:783–92. https://doi.org/10.1016/j.nicl.2018.09.014.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Hong HJ, Sohn H, Cha M, Kim S, Oh J, Chu MK, et al. Increased frontomotor oscillations during tic suppression in children with Tourette syndrome. J Child Neurol. 2013;28:615–24. https://doi.org/10.1177/0883073812450317.

    Article  PubMed  Google Scholar 

  87. • Zapparoli L, Macerollo A, Joyce EM, Martino D, Kilner JM. Voluntary tic suppression and the normalization of motor cortical beta power in Gilles de la Tourette syndrome: an EEG study. Eur J Neurosci. 2019;50:3944–57. https://doi.org/10.1111/ejn.14548This paper explores neuronal activity over the sensorimotor cortex during involuntary movements and tic suppression.

    Article  PubMed  Google Scholar 

  88. Wardak C. The role of the supplementary motor area in inhibitory control in monkeys and humans. J Neurosci. 2011;31:5181–3. https://doi.org/10.1523/JNEUROSCI.0006-11.2011.

    Article  CAS  PubMed Central  Google Scholar 

  89. Dinomais M, Minassian AT, Tuilier T, Delion M, Wilke M, N’Guyen S, et al. Functional MRI comparison of passive and active movement: possible inhibitory role of supplementary motor area. Neuroreport. 2009;20:1351–5. https://doi.org/10.1097/WNR.0b013e328330cd43.

    Article  PubMed  Google Scholar 

  90. Kasess CH, Windischberger C, Cunnington R, Lanzenberger R, Pezawas L, Moser E. The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling. Neuroimage. 2008;40:828–37. https://doi.org/10.1016/j.neuroimage.2007.11.040.

    Article  PubMed  Google Scholar 

  91. Scangos KW, Stuphorn V. Medial frontal cortex motivates but does not control movement initiation in the countermanding task. J Neurosci. 2010;30:1968–82. https://doi.org/10.1523/JNEUROSCI.4509-09.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Chen X, Scangos KW, Stuphorn V. Supplementary motor area exerts proactive and reactive control of arm movements. J Neurosci. 2010;30:14657–75. https://doi.org/10.1523/JNEUROSCI.2669-10.2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Duann JR, Ide JS, Luo X, Li CS. Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. J Neurosci. 2009;29:10171–9. https://doi.org/10.1523/JNEUROSCI.1300-09.2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Mantovani A, Lisanby SH, Pieraccini F, Ulivelli M, Castrogiovanni P, Rossi S. Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette’s syndrome (TS). Int J Neuropsychopharmacol. 2006;9:95–100. https://doi.org/10.1017/S1461145705005729.

    Article  PubMed  Google Scholar 

  95. Franzkowiak S, Pollok B, Biermann-Ruben K, Südmeyer M, Paszek J, Jonas M, et al. Altered pattern of motor cortical activation-inhibition during voluntary movements in Tourette syndrome. Mov Disord. 2010;25:1960–6. https://doi.org/10.1002/mds.23186.

    Article  PubMed  Google Scholar 

  96. Franzkowiak S, Pollok B, Biermann-Ruben K, Südmeyer M, Paszek J, Thomalla G, et al. Motor-cortical interaction in Gilles de la Tourette syndrome. PLoS One. 2012;7:e27850. https://doi.org/10.1371/journal.pone.0027850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Thomalla G, Jonas M, Bäumer T, Siebner HR, Biermann-Ruben K, Ganos C, et al. Costs of control: decreased motor cortex engagement during a Go/NoGo task in Tourette’s syndrome. Brain. 2014;137:122–36. https://doi.org/10.1093/brain/awt288.

    Article  PubMed  Google Scholar 

  98. Draper A, Stephenson MC, Jackson GM, Pépés S, Morgan PS, Morris PG, et al. Increased GABA contributes to enhanced control over motor excitability in Tourette syndrome. Curr Biol. 2014;24:2343–7. https://doi.org/10.1016/j.cub.2014.08.038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Eddy CM, Rickards HE, Cavanna AE. Treatment strategies for tics in Tourette syndrome. Ther Adv Neurol Disord. 2011;4:25–45. https://doi.org/10.1177/1756285610390261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

A draft of this article was archived on the Open Science Framework (https://osf.io/5sg2d).

Funding

Research reported in this publication was supported by the National Institute of Mental Health of the National Institutes of Health under award numbers R01MH104030 and R01MH118217.

Author information

Authors and Affiliations

  1. Department of Neurology, Washington University School of Medicine, 660 S Euclid Avenue, Campus Box 8111, St. Louis, MO, 63110-1093, USA

    Keisuke Ueda & Kevin J. Black

  2. Department of Psychiatry, Washington University School of Medicine, St Louis, MO, USA

    Soyoung Kim & Kevin J. Black

  3. Department of Cognitive Science, University of California San Diego, La Jolla, CA, USA

    Deanna J. Greene

  4. Department of Radiology, Washington University School of Medicine, St Louis, MO, USA

    Kevin J. Black

  5. Department of Neuroscience, Washington University School of Medicine, St Louis, MO, USA

    Kevin J. Black

Authors
  1. Keisuke Ueda
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Soyoung Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Deanna J. Greene
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kevin J. Black
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keisuke Ueda.

Ethics declarations

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.

Conflict of Interest

The authors declare no conflicts of interest relevant to this manuscript.

Disclaimer

The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Tourette’s Syndrome

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ueda, K., Kim, S., Greene, D.J. et al. Correlates and Clinical Implications of Tic Suppressibility. Curr Dev Disord Rep 8, 112–120 (2021). https://doi.org/10.1007/s40474-021-00230-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40474-021-00230-4

Keywords

Search

Navigation