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Limbic and motor circuits involved in symmetry behavior in Tourette's syndrome

  • Froukje E. de Vries (a1), Odile A. van den Heuvel (a1) (a2), Danielle C. Cath (a3), Henk J. Groenewegen (a2), Anton J. L. M. van Balkom (a1), Ronald Boellaard (a4), Adriaan A. Lammertsma (a4) and Dick J. Veltman (a1)...
Abstract
Objective

The need for symmetry and ordering objects related to a “just right”-feeling is a common symptom in Tourette's syndrome (TS) and resembles symmetry behavior in obsessive-compulsive disorder, but its pathophysiology is unknown. We used a symptom provocation paradigm to investigate the neural correlates of symmetry behavior in TS and hypothesized the involvement of frontal-striatal and limbic brain areas.

Methods

Pictures of asymmetrically and symmetrically arranged objects were presented in randomized blocks (4 blocks of each condition) to 14 patients with TS and 10 matched healthy controls (HC). A H215O positron emission tomography scan was acquired during each stimulus block, resulting in 8 scans per subject. After each scan, state anxiety and symmetry behavior (the urge to rearrange objects) were measured using a visual analogue scale.

Results

During the asymmetry condition, TS patients showed increased regional cerebral blood flow (rCBF) in the anterior cingulate cortex, supplementary motor area, and inferior frontal cortex, whereas HC showed increased rCBF in the visual cortex, primary motor cortex, and dorsal prefrontal cortex. Symmetry ratings during provocation correlated positively with orbitofrontal activation in the TS group and sensorimotor activation in the HC group, and negatively with dorsal prefrontal activity in HC.

Conclusions

Results suggest that both motor and limbic circuits are involved in symmetry behavior in TS. Motor activity may relate to an urge to move or perform tics, and limbic activation may indicate that asymmetry stimuli are salient for TS patients. In contrast, symmetry provocation in HC resulted in activation of brain regions implicated in sensorimotor function and cognitive control.

Copyright
Corresponding author
*Address for correspondence: Froukje E. de Vries, VU University Medical Center, Medical Faculty, Department of Anatomy and Neuroscience, Room G 102-b, Van der Boechorststraat 7, 1081 BT Amsterdam, the Netherlands. (Email fe.devries@vumc.nl)
References
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1.Cath DC, Hedderly T, Ludolph AG, etal. European clinical guidelines for Tourette syndrome and other tic disorders. Part I: assessment. Eur Child Adolesc Psychiatry. 2011; 20(4): 155171.
2.Worbe Y, Mallet L, Golmard JL, etal. Repetitive behaviours in patients with Gilles de la Tourette syndrome: tics, compulsions, or both? PLoS One. 2010; 5(9): e12959.
3.Pauls DL, Towbin KE, Leckman JF, Zahner GE, Cohen DJ. Gilles de la Tourette's syndrome and obsessive-compulsive disorder: evidence supporting a genetic relationship. Arch Gen Psychiatry. 1986; 43(12): 11801182.
4.Robertson MM. Tourette syndrome, associated conditions and the complexities of treatment. Brain. 2000; 123(Pt 3): 425462.
5.Cath DC, Spinhoven P, van Woerkom TC, etal. Gilles de la Tourette's syndrome with and without obsessive-compulsive disorder compared with obsessive-compulsive disorder without tics: which symptoms discriminate? J Nerv Ment Dis. 2001; 189(4): 219228.
6.Mataix-Cols D, van den Heuvel OA. Common and distinct neural correlates of obsessive-compulsive and related disorders. Psychiatr Clin North Am. 2006; 29(2): 391410.
7.Bloch MH, Leckman JF, Zhu H, Peterson BS. Caudate volumes in childhood predict symptom severity in adults with Tourette syndrome. Neurology. 2005; 65(8): 12531258.
8.Makki MI, Govindan RM, 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(6): 669678.
9.Pourfar M, Feigin A, Tang CC, etal. Abnormal metabolic brain networks in Tourette syndrome. Neurology. 2011; 76(11): 944952.
10.Braun AR, Randolph C, Stoetter B, etal. The functional neuroanatomy of Tourette's syndrome: an FDG-PET study. II: relationships between regional cerebral metabolism and associated behavioral and cognitive features of the illness. Neuropsychopharmacology. 1995; 13(2): 151168.
11.Mataix-Cols D, Wooderson S, Lawrence N, etal. Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry. 2004; 61(6): 564576.
12.van den Heuvel OA, Remijnse PL, Mataix-Cols D, etal. The major symptom dimensions of obsessive-compulsive disorder are mediated by partially distinct neural systems. Brain. 2009; 132(Pt 4): 853868.
13.van den Heuvel OA, Veltman DJ, Groenewegen HJ, etal. Amygdala activity in obsessive-compulsive disorder with contamination fear: a study with oxygen-15 water positron emission tomography. Psychiatry Res. 2004; 132(3): 225237.
14.Leckman JF, Riddle MA, Hardin MT, etal. The Yale Global Tic Severity Scale: initial testing of a clinician-rated scale of tic severity. J Am Acad Child Adolesc Psychiatry. 1989; 28(4): 566573.
15. First MB, Spitzer RL, Gibbon M, Williams JB. Structured Clinical Interview for DSM-IV Axis I Disorders–Patient Edition(SCID-I/P(version 2.0) edn); 1996. New York, Biomedics Research, New York State Psychiatric Institute, 2002.
16.Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961; 4: 561571.
17.van Oppen P, Hoekstra RJ, Emmelkamp PM. The structure of obsessive-compulsive symptoms. Behav Res Ther. 1995; 33(1): 1523.
18.van den Heuvel OA, Boellaard R, Veltman DJ, Mesina C, Lammertsma AA. Attenuation correction of PET activation studies in the presence of task-related motion. Neuroimage. 2003; 19(4): 15011509.
19.Mesina CT, Boellaard R, van den Heuvel OA, etal. Effects of attenuation correction and reconstruction method on PET activation studies. Neuroimage. 2003; 20(2): 898908.
20.Lieberman MD, Cunningham WA. Type I and type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci. 2009; 4(4): 423428.
21.Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986; 9: 357381.
22.Haber SN. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat. 2003; 26(4): 317330.
23.Mink JW. Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. Pediatr Neurol. 2001; 25(3): 190198.
24.Worbe Y, Gerardin E, Hartmann A, etal. Distinct structural changes underpin clinical phenotypes in patients with Gilles de la Tourette syndrome. Brain. 2010; 133(Pt. 12): 36493660.
25.Peterson BS, Skudlarski P, Anderson AW, etal. A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch Gen Psychiatry. 1998; 55(4): 326333.
26.Mazzone L, Yu S, Blair C, etal. An FMRI study of frontostriatal circuits during the inhibition of eye blinking in persons with Tourette syndrome. Am J Psychiatry. 2010; 167(3): 341349.
27.Bohlhalter S, Goldfine A, Matteson S, etal. Neural correlates of tic generation in Tourette syndrome: an event-related functional MRI study. Brain. 2006; 129(Pt. 8): 20292037.
28.Stern E, Silbersweig DA, Chee KY, etal. A functional neuroanatomy of tics in Tourette syndrome. Arch Gen Psychiatry. 2000; 57(8): 741748.
29.Kawohl W, Bruhl A, Krowatschek G, Ketteler D, Herwig U. Functional magnetic resonance imaging of tics and tic suppression in Gilles de la Tourette syndrome. World J Biol Psychiatry. 2009; 10(4 Pt. 2): 567570.
30.Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol Psychiatry. 2003; 54(5): 504514.
31.Elliott R, Dolan RJ, Frith CD. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb Cortex. 2000; 10(3): 308317.
32.Hampson M, Tokoglu F, King RA, Constable RT, Leckman JF. Brain areas coactivating with motor cortex during chronic motor tics and intentional movements. Biol Psychiatry. 2009; 65(7): 594599.
33.Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MF. Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc Natl Acad Sci U S A. 2010; 107(30): 1324013245.
34.Mantovani A, Lisanby SH, Pieraccini F, etal. Repetitive transcranial magnetic stimulation (rTMS) in the treatment of obsessive-compulsive disorder (OCD) and Tourette's syndrome (TS). Int J Neuropsychopharmacol. 2006; 9(1): 95100.
35.Fried I, Katz A, McCarthy G, etal. Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci. 1991; 11(11): 36563666.
36.Mars RB, Klein MC, Neubert FX, etal. Short-latency influence of medial frontal cortex on primary motor cortex during action selection under conflict. J Neurosci. 2009; 29(21): 69266931.
37.Jeffries KJ, Schooler C, Schoenbach C, etal. The functional neuroanatomy of Tourette's syndrome: an FDG PET study III: functional coupling of regional cerebral metabolic rates. Neuropsychopharmacology. 2002; 27(1): 92104.
38.Remijnse PL, van den Heuvel OA, Veltman DJ. Neuroimaging in obsessive-compulsive disorder. Current Medical Imaging Reviews. 2005; 1: 331335.
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CNS Spectrums
  • ISSN: 1092-8529
  • EISSN: 2165-6509
  • URL: /core/journals/cns-spectrums
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