Skip to main content Accessibility help
×
Home
Hostname: page-component-cf9d5c678-5tm97 Total loading time: 0.429 Render date: 2021-08-03T17:16:13.417Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

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

Published online by Cambridge University Press:  03 December 2012

Froukje E. de Vries
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, the Netherlands
Odile A. van den Heuvel
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, the Netherlands Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, the Netherlands
Danielle C. Cath
Affiliation:
Department of Clinical Psychology, University of Utrecht & Academic Anxiety Center Altrecht, Utrecht, the Netherlands
Henk J. Groenewegen
Affiliation:
Department of Anatomy and Neurosciences, VU University Medical Center, Amsterdam, the Netherlands
Anton J. L. M. van Balkom
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, the Netherlands
Ronald Boellaard
Affiliation:
Department of Nuclear Medicine & PET Research, VU University Medical Center, Amsterdam, the Netherlands
Adriaan A. Lammertsma
Affiliation:
Department of Nuclear Medicine & PET Research, VU University Medical Center, Amsterdam, the Netherlands
Dick J. Veltman
Affiliation:
Department of Psychiatry, VU University Medical Center, Amsterdam, the Netherlands
Corresponding
E-mail address:

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.

Type
Original Research
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
4.Robertson, MM. Tourette syndrome, associated conditions and the complexities of treatment. Brain. 2000; 123(Pt 3): 425462.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
9.Pourfar, M, Feigin, A, Tang, CC, etal. Abnormal metabolic brain networks in Tourette syndrome. Neurology. 2011; 76(11): 944952.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
16.Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J. An inventory for measuring depression. Arch Gen Psychiatry. 1961; 4: 561571.CrossRefGoogle ScholarPubMed
17.van Oppen, P, Hoekstra, RJ, Emmelkamp, PM. The structure of obsessive-compulsive symptoms. Behav Res Ther. 1995; 33(1): 1523.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
21.Alexander, GE, DeLong, MR, Strick, PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986; 9: 357381.CrossRefGoogle ScholarPubMed
22.Haber, SN. The primate basal ganglia: parallel and integrative networks. J Chem Neuroanat. 2003; 26(4): 317330.CrossRefGoogle ScholarPubMed
23.Mink, JW. Basal ganglia dysfunction in Tourette's syndrome: a new hypothesis. Pediatr Neurol. 2001; 25(3): 190198.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
28.Stern, E, Silbersweig, DA, Chee, KY, etal. A functional neuroanatomy of tics in Tourette syndrome. Arch Gen Psychiatry. 2000; 57(8): 741748.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
38.Remijnse, PL, van den Heuvel, OA, Veltman, DJ. Neuroimaging in obsessive-compulsive disorder. Current Medical Imaging Reviews. 2005; 1: 331335.CrossRefGoogle Scholar
8
Cited by

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

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

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

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

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

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

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *