Imaging the where and when of tic generation and resting state networks in adult Tourette patients

Frontiers in Human Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Neuner, Irene ^a,b,c   Werner, Cornelius J ^a,d   Arrubla, Jorge ^a,b   Stöcker, Tony ^a,c   Ehlen, Corinna ^b   Wegener, Hans P ^a   Schneider, Frank ^b,c   Jon Shah, N ^a,c,d  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c JARA TRANSLATIONAL BRAIN MEDICINE   (Germany)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

Author keywords

Basal ganglia; Cortico striato thalamo cortical circuit; Resting state networks; Tics; Tourette

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; DIAGNOSTIC IMAGING; DISEASE SEVERITY; ELECTROSTIMULATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GILLES DE LA TOURETTE SYNDROME; HUMAN; INSULA; MALE; OPERCULUM (BRAIN); PARIETAL OPERCULUM; POSITRON EMISSION TOMOGRAPHY; PRIMARY MOTOR CORTEX; PUTAMEN; RESTING STATE NETWORK; SCORING SYSTEM; SENSORIMOTOR CORTEX; SOMATOSENSORY CORTEX; SUPPLEMENTARY MOTOR AREA; THALAMUS; TIC; VISUAL CORTEX; YALE GLOBAL TIC SEVERITY SCALE;

EID: 84901605293     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00362     Document Type: Article

References (88)

1. Ackermans, L., Duits, A., van der Linden, C., Tijssen, M., Schruers, K., Temel, Y., et al. (2011). Double-blind clinical trial of thalamic stimulation in patients with Tourette syndrome. Brain 134, 832-844. doi: 10.1093/brain/awq380
2. Ackermans, L., Kuhn, J., Neuner, I., Temel, Y., and Visser-Vandewalle, V. (2013a). Surgery for Tourette Syndrome. World Neurosurg. 80, S29. e15-S29. e22. doi: 10.1016/j.wneu.2012.06.017
3. Ackermans, L., Neuner, I., Temel, Y., Duits, A., Kuhn, J., and Visser-Vandewalle, V. (2013b). Thalamic deep brain stimulation for Tourette syndrome. Behav. Neurol. 27, 133-138. doi: 10.3233/BEN-120301
4. Beckmann, C. F., and Smith, S. M. (2004). Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans. Med. Imaging 23, 137-152. doi: 10.1109/TMI.2003.822821
5. Benjamini, Y., and Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165-1188. doi: 10.1214/aos/1013699998
6. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541. doi: 10.1002/mrm.1910340409
7. Bluhm, R. L., Miller, J., Lanius, R. A., Osuch, E. A., Boksman, K., Neufeld, R. W. J., et al. (2007). Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophr. Bull. 33, 1004-1012. doi: 10.1093/schbul/sbm052
8. Bohlhalter, S., Goldfine, A., Matteson, S., Garraux, G., Hanakawa, T., Kansaku, K., et al. (2006). Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain 129, 2029-2037. doi: 10.1093/brain/awl050
9. Boly, M., Tshibanda, L., Vanhaudenhuyse, A., Noirhomme, Q., Schnakers, C., Ledoux, D., et al. (2009). Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient. Hum. Brain Mapp. 30, 2393-2400. doi: 10.1002/hbm.20672
10. Bonavita, S., Gallo, A., Sacco, R., Corte, M. D., Bisecco, A., Docimo, R., et al. (2011). Distributed changes in default-mode resting-state connectivity in multiple sclerosis. Mult. Scler. 17, 411-422. doi: 10.1177/1352458510394609
11. Braun, A. R., Stoetter, B., Randolph, C., Hsiao, J. K., Vladar, K., Gernert, J., et al. (1993). The functional neuroanatomy of Tourette's syndrome: an FDG-PET study. I. Regional changes in cerebral glucose metabolism differentiating patients and controls. Neuropsychopharmacology 9, 277-291. doi: 10.1038/npp.1993.64
12. Buckner, R. L., Andrews-Hanna, J. R., and Schacter, D. L. (2008). The brain's default network: anatomy, function, and relevance to disease. Ann. N.Y. Acad. Sci. 1124, 1-38. doi: 10.1196/annals.1440.011
13. Cannon, E., Silburn, P., Coyne, T., O'Maley, K., Crawford, J. D., and Sachdev, P. S. (2012). Deep brain stimulation of anteromedial globus pallidus interna for severe Tourette's syndrome. Am. J. Psychiatry 169, 860-866. doi: 10.1176/appi.ajp.2012.11101583
14. Cavanna, A. E., and Termine, C. (2012). Tourette syndrome. Adv. Exp. Med. Biol. 724, 375-383. doi: 10.1007/978-1-4614-0653-2_28
15. Church, J. A., Fair, D. A., Dosenbach, N. U. F., Cohen, A. L., Miezin, F. M., Petersen, S. E., et al. (2009). Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain 132, 225-238. doi: 10.1093/brain/awn223
16. Cohen, D. J., and Leckman, J. F. (1991). Tourette's syndrome. JAMA 265, 1738.
17. Craig, A. D. (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666. doi: 10.1038/nrn894
18. Craig, A. D. B. (2009). Emotional moments across time: a possible neural basis for time perception in the anterior insula. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1933-1942. doi: 10.1098/rstb.2009.0008
19. Cunnington, R., Windischberger, C., Deecke, L., and Moser, E. (2003). The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 20, 404-412. doi: 10.1016/S1053-8119(03)00291-X
20. Damoiseaux, J. S., and Greicius, M. D. (2009). Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct. Funct. 213, 525-533. doi: 10.1007/s00429-009-0208-6
21. Damoiseaux, J. S., Rombouts, S. A. R. B., Barkhof, F., Scheltens, P., Stam, C. J., Smith, S. M., et al. (2006). Consistent resting-state networks across healthy subjects. Proc. Natl. Acad. Sci. U.S.A. 103, 13848-13853. doi: 10.1073/pnas.0601417103
22. Delaveau, P., Salgado-Pineda, P., Fossati, P., Witjas, T., Azulay, J.-P., and Blin, O. (2010). Dopaminergic modulation of the default mode network in Parkinson's disease. Eur. Neuropsychopharmacol. 20, 784-792. doi: 10.1016/j.euroneuro.2010.07.001
23. Derbyshire, S. W. G., Whalley, M. G., Stenger, V. A., and Oakley, D. A. (2004). Cerebral activation during hypnotically induced and imagined pain. Neuroimage 23, 392-401. doi: 10.1016/j.neuroimage.2004.04.033
24. Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995a). REVIEW: Contributions of anterior cingulate cortex to behaviour. Brain 118, 279-306.
25. Devinsky, O., Morrell, M. J., and Vogt, B. A. (1995b). Contributions of anterior cingulate cortex to behaviour. Brain118(Pt 1), 279-306.
26. Disbrow, E., Litinas, E., Recanzone, G. H., Padberg, J., and Krubitzer, L. (2003). Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys. J. Comp. Neurol. 462, 382-399. doi: 10.1002/cne.10731
27. Draganski, B., Martino, D., Cavanna, A. E., Hutton, C., Orth, M., Robertson, M. M., et al. (2010). Multispectral brain morphometry in Tourette syndrome persisting into adulthood. Brain 133, 3661-3675. doi: 10.1093/brain/awq300
28. Eccles, J. C. (1982). The initiation of voluntary movements by the supplementary motor area. Arch. Psychiatr. Nervenkr. 231, 423-441. doi: 10.1007/BF00342722
29. Eickhoff, S. B., Jbabdi, S., Caspers, S., Laird, A. R., Fox, P. T., Zilles, K., et al. (2010). Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J. Neurosci. 30, 6409-6421. doi: 10.1523/JNEUROSCI.5664-09.2010
30. Esposito, F., Tessitore, A., Giordano, A., De Micco, R., Paccone, A., Conforti, R., et al. (2013). Rhythm-specific modulation of the sensorimotor network in drug-naive patients with Parkinson's disease by levodopa. Brain 136, 710-725. doi: 10.1093/brain/awt007
31. Felling, R. J., and Singer, H. S. (2011). Neurobiology of tourette syndrome: current status and need for further investigation. J. Neurosci. 31, 12387-12395. doi: 10.1523/JNEUROSCI.0150-11.2011
32. Filippini, N., MacIntosh, B. J., Hough, M. G., Goodwin, G. M., Frisoni, G. B., Smith, S. M., et al. (2009). Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc. Natl. Acad. Sci. U.S.A. 106, 7209-7214. doi: 10.1073/pnas.0811879106
33. Franzkowiak, S., Pollok, B., Biermann-Ruben, K., Südmeyer, M., Paszek, J., Thomalla, G., et al. (2012). Motor-cortical interaction in Gilles de la Tourette syndrome. PLoS ONE 7:e27850. doi: 10.1371/journal.pone.0027850
34. Fried, I., Katz, A., McCarthy, G., Sass, K. J., Williamson, P., Spencer, S. S., et al. (1991). Functional organization of human supplementary motor cortex studied by electrical stimulation. J. Neurosci. 11, 3656-3666.
35. Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253-258. doi: 10.1073/pnas.0135058100
36. Greicius, M. D., Srivastava, G., Reiss, A. L., and Menon, V. (2004). Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. U.S.A. 101, 4637-4642. doi: 10.1073/pnas.0308627101
37. Hampson, M., Tokoglu, F., King, R. A., Constable, R. T., and Leckman, J. F. (2009). Brain areas coactivating with motor cortex during chronic motor tics and intentional movements. Biol. Psychiatry 65, 594-599. doi: 10.1016/j.biopsych.2008.11.012
38. Heise, K.-F., Steven, B., Liuzzi, G., Thomalla, G., Jonas, M., Müller-Vahl, K., et al. (2010). Altered modulation of intracortical excitability during movement preparation in Gilles de la Tourette syndrome. Brain 133, 580-590. doi: 10.1093/brain/awp299
39. Hsieh, J. C., Hägermark, O., Ståhle-Bäckdahl, M., Ericson, K., Eriksson, L., Stone-Elander, S., et al. (1994). Urge to scratch represented in the human cerebral cortex during itch. J. Neurophysiol. 72, 3004-3008.
40. Isnard, J., Guénot, M., Sindou, M., and Mauguière, F. (2004). Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study. Epilepsia 45, 1079-1090. doi: 10.1111/j.0013-9580.2004.68903.x
41. Kawohl, W., Brühl, A., Krowatschek, G., Ketteler, D., and Herwig, U. (2009a). Functional magnetic resonance imaging of tics and tic suppression in Gilles de la Tourette syndrome. World J. Biol. Psychiatry 10, 567-570. doi: 10.1080/15622970802118356
42. Kawohl, W., Schneider, F., Vernaleken, I., and Neuner, I. (2009b). Aripiprazole in the pharmacotherapy of Gilles de la Tourette syndrome in adult patients. World J. Biol. Psychiatry 10, 827-831. doi: 10.1080/15622970701762544
43. Kawohl, W., Schneider, F., Vernaleken, I., and Neuner, I. (2009c). Chronic motor tic disorder and aripiprazole. J. Neuropsychiatry Clin. Neurosci. 21, 224. doi: 10.1176/appi.neuropsych.21.2.224
44. Khalifa, N., and von Knorring, A.-L. (2003). Prevalence of tic disorders and Tourette syndrome in a Swedish school population. Dev. Med. Child Neurol. 45, 315-319. doi: 10.1111/j.1469-8749.2003.tb00402.x
45. Kwan, C. L., Crawley, A. P., Mikulis, D. J., and Davis, K. D. (2000). An fMRI study of the anterior cingulate cortex and surrounding medial wall activations evoked by noxious cutaneous heat and cold stimuli. Pain 85, 359-374. doi: 10.1016/S0304-3959(99)00287-0
46. Leckman, J. F. (2002). Tourette's syndrome. Lancet 360, 1577-1586. doi: 10.1016/S0140-6736(02)11526-1
47. Leckman, J. F., Riddle, M. A., Hardin, M. T., Ort, S. I., Swartz, K. L., Stevenson, J., et al. (1989). The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J. Am. Acad. Child Adolesc. Psychiatry 28, 566-573. doi: 10.1097/00004583-198907000-00015
48. Lerner, A., Bagic, A., Boudreau, E. A., Hanakawa, T., Pagan, F., Mari, Z., et al. (2007). Neuroimaging of neuronal circuits involved in tic generation in patients with Tourette syndrome. Neurology 68, 1979-1987. doi: 10.1212/01.wnl.0000264417.18604.12
49. Lerner, A., Bagic, A., Simmons, J. M., Mari, Z., Bonne, O., Xu, B., et al. (2012). Widespread abnormality of the γ-aminobutyric acid-ergic system in Tourette syndrome. Brain 135, 1926-1936. doi: 10.1093/brain/aws104
50. Li, S.-J., Li, Z., Wu, G., Zhang, M.-J., Franczak, M., and Antuono, P. G. (2002). Alzheimer disease: evaluation of a functional MR imaging index as a marker. Radiology 225, 253-259. doi: 10.1148/radiol.2251011301
51. Luppino, G., Matelli, M., Camarda, R. M., Gallese, V., and Rizzolatti, G. (1991). Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: an intracortical microstimulation study in the macaque monkey. J. Comp. Neurol. 311, 463-482. doi: 10.1002/cne.903110403
52. Mesulam, M. M., and Mufson, E. J. (1982a). Insula of the old world monkey. I. Architectonics in the insulo-orbito-temporal component of the paralimbic brain. J. Comp. Neurol. 212, 1-22.
53. Mesulam, M. M., and Mufson, E. J. (1982b). Insula of the old world monkey. III: Efferent cortical output and comments on function. J. Comp. Neurol. 212, 38-52.
54. Mufson, E. J., and Mesulam, M. M. (1982). Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum. J. Comp. Neurol. 212, 23-37. doi: 10.1002/cne.902120103
55. Müller-Vahl, K. R., Cath, D. C., Cavanna, A. E., Dehning, S., Porta, M., Robertson, M. M., et al. (2011). European clinical guidelines for Tourette syndrome and other tic disorders. Part IV: deep brain stimulation. Eur. Child Adolesc. Psychiatry 20, 209-217. doi: 10.1007/s00787-011-0166-4
56. Neuner, I., Kellermann, T., Stöcker, T., Kircher, T., Habel, U., Shah, J. N., et al. (2010a). Amygdala hypersensitivity in response to emotional faces in Tourette's patients. World J. Biol. Psychiatry 11, 858-872. doi: 10.3109/15622975.2010.480984
57. Neuner, I., Kupriyanova, Y., Stöcker, T., Huang, R., Posnansky, O., Schneider, F., et al. (2010b). White-matter abnormalities in Tourette syndrome extend beyond motor pathways. Neuroimage 51, 1184-1193. doi: 10.1016/j.neuroimage.2010.02.049
58. Neuner, I., and Ludolph, A. G. (2011). [Neurobiology, clinical characteristics and therapy in Tourette's syndrome]. Fortschr. Neurol. Psychiatr. 79, 724-732. doi: 10.1055/s-0031-1281853
59. Neuner, I., Nordt, C., Schneider, F., and Kawohl, W. (2012). Effectiveness of aripiprazole in the treatment of adult Tourette patients up to 56 months. Hum. Psychopharmacol. 27, 364-369. doi: 10.1002/hup.2235
60. Neuner, I., Podoll, K., Janouschek, H., Michel, T. M., Sheldrick, A. J., and Schneider, F. (2009). From psychosurgery to neuromodulation: deep brain stimulation for intractable Tourette syndrome. World J. Biol. Psychiatry 10, 366-376. doi: 10.1080/15622970802513317
61. Neuner, I., Wegener, P., Stoecker, T., Kircher, T., Schneider, F., and Shah, N. J. (2007). Development and implementation of an MR-compatible whole body video system. Neurosci. Lett. 420, 122-127. doi: 10.1016/j.neulet.2007.03.063
62. Nichols, T. E., and Holmes, A. P. (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 15, 1-25. doi: 10.1002/hbm.1058
63. Oakes, T. R., Fox, A. S., Johnstone, T., Chung, M. K., Kalin, N., and Davidson, R. J. (2007). Integrating VBM into the General Linear Model with voxelwise anatomical covariates. Neuroimage 34, 500-508. doi: 10.1016/j.neuroimage.2006.10.007
64. Pearlson, G. D., and Calhoun, V. D. (2009). Convergent approaches for defining functional imaging endophenotypes in schizophrenia. Front. Hum. Neurosci. 3:37. doi: 10.3389/neuro.09.037.2009
65. Peterson, B. S., Skudlarski, P., Anderson, A. W., Zhang, H., Gatenby, J. C., Lacadie, C. M., et al. (1998). A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch. Gen. Psychiatry 55, 326-333. doi: 10.1001/archpsyc.55.4.326
66. Peterson, B. S., Thomas, P., Kane, M. J., Scahill, L., Zhang, H., Bronen, R., et al. (2003). Basal Ganglia volumes in patients with Gilles de la Tourette syndrome. Arch. Gen. Psychiatry 60, 415-424. doi: 10.1001/archpsyc.60.4.415
67. Plessen, K. J., Bansal, R., and Peterson, B. S. (2009). Imaging evidence for anatomical disturbances and neuroplastic compensation in persons with Tourette syndrome. J. Psychosom. Res. 67, 559-573. doi: 10.1016/j.jpsychores.2009.07.005
68. Qi, H.-X., Lyon, D. C., and Kaas, J. H. (2002). Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus). J. Comp. Neurol. 443, 168-182. doi: 10.1002/cne.10113
69. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G. L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682. doi: 10.1073/pnas.98.2.676
70. Robertson, M. M. (2012). The Gilles de la Tourette syndrome: the current status. Arch. Dis. Child. Educ. Pract. Ed. 97, 166-175. doi: 10.1136/archdischild-2011-300585
71. Roessner, V., Rothenberger, A., Rickards, H., and Hoekstra, P. J. (2011). European clinical guidelines for Tourette syndrome and other tic disorders. Eur. Child Adolesc. Psychiatry 20, 153-154. doi: 10.1007/s00787-011-0165-5
72. Roland, P. E., Larsen, B., Lassen, N. A., and Skinhøj, E. (1980). Supplementary motor area and other cortical areas in organization of voluntary movements in man. J. Neurophysiol. 43, 118-136.
73. Rosazza, C., and Minati, L. (2011). Resting-state brain networks: literature review and clinical applications. Neurol. Sci. 32, 773-785. doi: 10.1007/s10072-011-0636-y
74. Sadaghiani, S., Hesselmann, G., Friston, K. J., and Kleinschmidt, A. (2010). The relation of ongoing brain activity, evoked neural responses, and cognition. Front. Syst. Neurosci. 4:20. doi: 10.3389/fnsys.2010.00020
75. Singer, H. S. (2005). Tourette's syndrome: from behaviour to biology. Lancet Neurol. 4, 149-159. doi: 10.1016/S1474-4422(05)01012-4
76. Smith, S. M., Fox, P. T., Miller, K. L., Glahn, D. C., Fox, P. M., Mackay, C. E., et al. (2009). Correspondence of the brain's functional architecture during activation and rest. Proc. Natl. Acad. Sci. U.S.A. 106, 13040-13045. doi: 10.1073/pnas.0905267106
77. Stern, E., Silbersweig, D. A., Chee, K. Y., Holmes, A., Robertson, M. M., Trimble, M., et al. (2000). A functional neuroanatomy of tics in Tourette syndrome. Arch. Gen. Psychiatry 57, 741-748. doi: 10.1001/archpsyc.57.8.741
78. Tessitore, A., Esposito, F., Vitale, C., Santangelo, G., Amboni, M., Russo, A., et al. (2012). Default-mode network connectivity in cognitively unimpaired patients with Parkinson disease. Neurology 79, 2226-2232. doi: 10.1212/WNL.0b013e31827689d6
79. Thomalla, G., Siebner, H. R., Jonas, M., Bäumer, T., Biermann-Ruben, K., Hummel, F., et al. (2009). Structural changes in the somatosensory system correlate with tic severity in Gilles de la Tourette syndrome. Brain 132, 765-777. doi: 10.1093/brain/awn339
80. Van Eimeren, T., Monchi, O., Ballanger, B., and Strafella, A. P. (2009). Dysfunction of the default mode network in Parkinson disease: a functional magnetic resonance imaging study. Arch. Neurol. 66, 877-883.
81. Vandewalle, V., van der Linden, C., Groenewegen, H. J., and Caemaert, J. (1999). Stereotactic treatment of Gilles de la Tourette syndrome by high frequency stimulation of thalamus. Lancet 353, 724. doi: 10.1016/S0140-6736(98)05964-9
82. Wang, Z., Maia, T. V., Marsh, R., Colibazzi, T., Gerber, A., and Peterson, B. S. (2011). The neural circuits that generate tics in Tourette's syndrome. Am. J. Psychiatry 168, 1326-1337. doi: 10.1176/appi.ajp.2011.09111692
83. Werner, C. J., Dogan, I., Saß, C., Mirzazade, S., Schiefer, J., Shah, N. J., et al. (2014). Altered resting-state connectivity in Huntington's Disease. Hum. Brain Mapp. 35, 2582-2593. doi: 10.1002/hbm.22351
84. Werner, C. J., Stöcker, T., Kellermann, T., Wegener, H. P., Schneider, F., Shah, N. J., et al. (2010). Altered amygdala functional connectivity in adult Tourette's syndrome. Eur. Arch. Psychiatry Clin. Neurosci. 260(Suppl.), S95-S99. doi: 10.1007/s00406-010-0161-7
85. Wolf, R. C., Sambataro, F., Vasic, N., Wolf, N. D., Thomann, P. A., Saft, C., et al. (2012). Default-mode network changes in preclinical Huntington's disease. Exp. Neurol. 237, 191-198. doi: 10.1016/j.expneurol.2012.06.014
86. Worbe, Y., Gerardin, E., Hartmann, A., Valabrégue, R., Chupin, M., Tremblay, L., et al. (2010). Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain 133, 3649-3660. doi: 10.1093/brain/awq293
87. Ziemann, U., Paulus, W., and Rothenberger, A. (1997). Decreased motor inhibition in Tourette's disorder: evidence from transcranial magnetic stimulation. Am. J. Psychiatry 154, 1277-1284.
88. Zuo, X.-N., Kelly, C., Adelstein, J. S., Klein, D. F., Castellanos, F. X., and Milham, M. P. (2010). Reliable intrinsic connectivity networks: test-retest evaluation using ICA and dual regression approach. Neuroimage 49, 2163-2177. doi: 10.1016/j.neuroimage.2009.10.080