Increased ventral striatal monoaminergic innervation in Tourette syndrome
Abstract
BACKGROUND: Excessive striatal dopaminergic innervation is suggested to underlie Tourette syndrome (TS). Prior imaging and postmortem studies yield conflicting data. METHODS: The authors used PET with the type 2 vesicular monoamine transporter ligand [(11)C]dihydrotetrabenazine (DTBZ) to quantify striatal monoaminergic innervation in patients with TS (n = 19) and control subjects (n = 27). Compartmental modeling was used to determine blood to brain ligand transport (K(1)) and tissue to plasma distribution volume (a measure of ligand binding) during continuous infusion of DTBZ. TS data were compared with control data using predefined regions of interest and on a voxel by voxel basis. RESULTS: There were no significant differences in ligand binding or ligand transport between patients with TS and control subjects in the dorsal striatum. With voxel by voxel analysis, there was increased DTBZ binding in the right ventral striatum. CONCLUSIONS: Previously reported differences between patients with TS and control subjects in dorsal striatal dopamine terminal markers may reflect medication-induced regulation of terminal marker expression or be the result of intrinsic differences in striatal dopaminergic synaptic function. Increased right ventral striatal DTBZ binding suggests that abnormal ventral striatal dopaminergic innervation may underlie tics.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
SPECT investigations in TS have found higher DAT binding in the right caudate, the striatum, the putamen after amphetamine challenge, and the basal ganglia.
“Single-photon emission computed tomography investigations in TS have found higher DAT binding in the right caudate [635], the striatum [636-639], the putamen after amphetamine challenge [640], and the basal ganglia [641].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [636]
Cites
The Neuroscience of Natural Rewards: Relevance to Addictive Drugs
Kelley, A. E., & Berridge, K. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03306.2002 · Cited by 1,465 · see citing works
Building neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834 · see citing works
Tourette syndrome, associated conditions and the complexities of treatment
Robertson, M. M. (2000) · Brain · doi:10.1093/brain/123.3.425 · Cited by 704 · see citing works
Leckman, J. F. (2002) · The Lancet · doi:10.1016/s0140-6736(02)11526-1 · Cited by 683 · see citing works
A Functional Magnetic Resonance Imaging Study of Tic Suppression in Tourette Syndrome
Peterson, B. S., Skudlarski, P., Anderson, A. W., Zhang, H., Gatenby, J. C., Lacadie, C. M., Leckman, J. F., & Gore, J. C. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.4.326 · Cited by 483 · see citing works
Jankovic, J. J. (2001) · New England Journal of Medicine · doi:10.1056/nejmra010032 · Cited by 449 · see citing works
Peterson, B. S., Riddle, M. A., Cohen, D. J., Katz, L. D., Smith, J. C., Hardin, M. T., & Leckman, J. F. (1993) · Neurology · doi:10.1212/wnl.43.5.941 · Cited by 394 · see citing works
Volumetric MRI changes in basal ganglia of children with Tourette's syndrome
Singer, H. S., Reiss, A. L., Brown, J. E., Aylward, E., Shih, B., Chee, E., Harris, E. L., Reader, M. J., Chase, G. A., Bryan, R. N., et al. (1993) · Neurology · doi:10.1212/wnl.43.5.950 · Cited by 370 · see citing works
A Functional Neuroanatomy of Tics in Tourette Syndrome
Stern, E., Silbersweig, D., Chee, K.-Y., Holmes, A., Robertson, M. M., Trimble, M., Frith, C., Frackowiak, R. S. J., & Dolan, R. J. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.8.741 · Cited by 338 · see citing works
Smith‐Roe, S. L., & Kelley, A. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07737.2000 · Cited by 321 · see citing works
Reynolds, S. M., & Berridge, K. C. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03261.2001 · Cited by 281 · see citing works
Abnormal dopamine uptake sites in postmortem striatum from patients with tourette's syndrome
Singer, H. S., Hahn, I., & Moran, T. H. (1991) · Annals of Neurology · doi:10.1002/ana.410300408 · Cited by 273 · see citing works
Coding of Serial Order by Neostriatal Neurons: A “Natural Action” Approach to Movement Sequence
Aldridge, J. W., & Berridge, K. C. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-07-02777.1998 · Cited by 263 · see citing works
Elevated Intrasynaptic Dopamine Release in Tourette’s Syndrome Measured by PET
Singer, H. S., Szymanski, S., Giuliano, J., Yokoi, F., Dogan, A. S., Brasic, J. R., Zhou, Y., Grace, A. A., & Wong, D. F. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.8.1329 · Cited by 259 · see citing works
Gilles de la Tourette's syndrome
Haber, S. N., Kowall, N. W., Vonsattel, J. P., Bird, E. D., & Richardson, E. P. (1986) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(86)90097-3 · Cited by 213 · see citing works
Pihlajam�ki, M., Tanila, H., H�nninen, T., Könönen, M., Laakso, M. P., Partanen, K. P. L., Soininen, H. S., & Aronen, H. J. (2000) · Annals of Neurology · doi:10.1002/1531-8249(200004)47:4 · Cited by 210 · see citing works
The vesicular monoamine transporter is not regulated by dopaminergic drug treatments
Borght, T. V., Kilbourn, M. R., Desmond, T. J., Kuhl, D. E., & Frey, K. A. (1995) · European Journal of Pharmacology · doi:10.1016/0014-2999(95)00594-3 · Cited by 205 · see citing works
Self-citationCerebral morphometric abnormalities in Tourette's syndrome
Hyde, T. M., Stacey, M. E., Coppola, R., Handel, S. F., Rickler, K. C., & Weinberger, D. R. (1995) · Neurology · doi:10.1212/wnl.45.6.1176 · Cited by 190 · see citing works
Swanson, C. J., Heath, S., Stratford, T. R., & Kelley, A. E. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00043-9 · Cited by 176 · see citing works
Campbell, K. M., de Lecea, L., Severynse, D. M., Caron, M. G., McGrath, M. J., Sparber, S. B., Sun, L.-Y., & Burton, F. H. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05044.1999 · Cited by 170 · see citing works
The metabolic anatomy of Tourette's syndrome
Eidelberg, D., Moeller, J. R., Antonini, A., Kazumata, K., DHAWAN, V. M., Budman, C. L., & Feigin, A. (1997) · Neurology · doi:10.1212/wnl.48.4.927 · Cited by 167 · see citing works
Braun, A. R., Stoetter, B., RANDOLPH, C. C., Hsiao, J., Vladar, K., Gernert, J., Carson, R. E., Herscovitch, P., & Chase, T. N. (1993) · Neuropsychopharmacology · doi:10.1038/npp.1993.64 · Cited by 167 · see citing works
A Complete Genome Screen in Sib Pairs Affected by Gilles de la Tourette Syndrome
* (1999) · The American Journal of Human Genetics · doi:10.1086/302613 · Cited by 164 · see citing works
High Presynaptic Dopaminergic Activity in Children With Tourette's Disorder
Monique Ernst, D., Zametkin, A. J., Jons, P. H., Matochik, J. A., Pascualvaca, D. M., & Cohen, R. M. (1999) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1097/00004583-199901000-00024 · Cited by 125 · see citing works
Aromatic L‐Amino Acid Decarboxylase Activity of Mouse Striatum Is Modulated via Dopamine Receptors
Hadjiconstantinou, M., Wemlinger, T. A., Sylvia, C.-H., Hubble, J. P., & Neff, N. H. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb03503.x · Cited by 118 · see citing works
A volumetric MRI study of Gilles de la Tourette's syndrome
Moriarty, J., Varma, A. R., Stevens, J., Fish, M., Trimble, M., & Robertson, M. M. (1997) · Neurology · doi:10.1212/wnl.49.2.410 · Cited by 107 · see citing works
Abnormal cerebral activation associated with a motor task in Tourette syndrome.
Biswal, B. B., Ulmer, J. L., Krippendorf, R. L., Harsch, H. H., Daniels, D. L., Hyde, J. S., & Haughton, V. M. (1998) · PubMed Central · Cited by 101 · see citing works
Borght, T. M. V., Sima, A. A. F., Kilbourn, M. R., Desmond, T. J., Kuhl, D. E., & Frey, K. A. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00167-h · Cited by 99 · see citing works
Self-citationBraun, A. R. (1995) · Neuropsychopharmacology · doi:10.1016/0893-133x(95)00052-f · Cited by 97 · see citing works
Dopamine transporter binding in Gilles de la Tourette syndrome
Müller-Vahl, K. R., Berding, G., Brücke, T., Kolbe, H., Meyer, G. J., Hundeshagen, H., Dengler, R., Knapp, W. H., & Emrich, H. M. (2000) · Journal of Neurology · doi:10.1007/pl00007806 · Cited by 95 · see citing works
Koeppe, R. A., Frey, K. A., Kume, A., Albin, R. L., Kilbourn, M. R., & Kuhl, D. E. (1997) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199709000-00001 · Cited by 90 · see citing works
Self-citationA rating scale for Gilles de la Tourette's syndrome
Goetz, C. G., Tanner, C. M., Wilson, R. S., et al. (1987) · Neurology · doi:10.1212/wnl.37.9.1542 · Cited by 87 · see citing works
A simple synthesis of [11C]Dihydrotetrabenazine (DTBZ)
Jewett, D. M., Kilbourn, M. R., & Lee, L. C. (1997) · Nuclear Medicine and Biology · doi:10.1016/s0969-8051(96)00213-2 · Cited by 79 · see citing works
Self-citationZhu, M., Juorio, A. V., Paterson, I. A., & Boulton, A. A. (1993) · European Journal of Pharmacology · doi:10.1016/0014-2999(93)90843-7 · Cited by 78 · see citing works
Koeppe, R. A., Frey, K. A., Kuhl, D. E., & Kilbourn, M. R. (1999) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-199912000-00011 · Cited by 77 · see citing works
Self-citationRegulation of DOPA Decarboxylase Activity in Brain of Living Rat
Cumming, P. D., Kuwabara, H., Ase, A. R., & GJEDDE, A. H. (1995) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1995.65031381.x · Cited by 74 · see citing works
Striatal presynaptic monoaminergic vesicles are not increased in Tourette’s syndrome
Meyer, P., Bohnen, N. I., Minoshima, S., Koeppe, R. A., Wernette, K., Kilbourn, M. R., Kuhl, D. E., Frey, K. A., & Albin, R. L. (1999) · Neurology · doi:10.1212/wnl.53.2.371 · Cited by 69 · see citing works
Self-citationChronic L-deprenyl-induced up-regulation of the dopamine uptake carrier
Wiener, H. L., Hashim, A., Lajtha, Á., et al. (1989) · European Journal of Pharmacology · doi:10.1016/0014-2999(89)90418-4 · Cited by 59 · see citing works
Neuropathological studies of Tourette syndrome.
Ep, R. (1982) · PubMed · Cited by 43 · see citing works
Meiergerd, S. M., Hooks, S. M., & Schenk, J. O. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63041277.x · Cited by 26 · see citing works
A neurobiological model for Tourette syndrome centered on the nucleus accumbens
Brito, G. N. O. (1997) · Medical Hypotheses · doi:10.1016/s0306-9877(97)90218-8 · Cited by 18 · see citing works
Worsley (1996) · doi:10.1002/(sici)1097-0193(1996)4:1
Flagged first, then by citations
Cited by
Sorted by citations
Recent advances in Tourette syndrome research
Albin, R. L., & Mink, J. W. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.01.001 · Cited by 478 · see citing works
Self-citationBerridge, K. C., Aldridge, J. W., Houchard, K. R., & Zhuang, X. (2005) · BMC Biology · doi:10.1186/1741-7007-3-4 · Cited by 309 · see citing works
Dichter, G. S., Damiano, C. A., & Allen, J. A. (2012) · Journal of Neurodevelopmental Disorders · doi:10.1186/1866-1955-4-19 · Cited by 299 · see citing works
Wong, D. F., Brašić, J. R., Singer, H. S., Schretlen, D. J., Kuwabara, H., Zhou, Y., Nandi, A., Maris, M. A., Alexander, M., Ye, W., et al. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301528 · Cited by 253 · see citing works
Neurobiology of Tourette Syndrome: Current Status and Need for Further Investigation: Table 1.
Felling, R. J., & Singer, H. S. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0150-11.2011 · Cited by 227 · see citing works
Perani, D., Garibotto, V., Gorini, A., Moresco, R. M., Henin, M., Panzacchi, A., Matarrese, M., Carpinelli, A., Bellodi, L., & Fazio, F. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.233 · Cited by 219 · see citing works
Neuromodulation in Tourette syndrome: dopamine and beyond
Buse, J., Schoenefeld, K., Münchau, A., & Roessner, V. (2013) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.10.004 · Cited by 185 · see citing works
Enhanced habit formation in Gilles de la Tourette syndrome
Delorme, C., Salvador, A., Valabrègue, R., Roze, E., Palminteri, S., Vidailhet, M., de Wit, S., Robbins, T., Hartmann, A., & Worbe, Y. (2016) · Brain · doi:10.1093/brain/awv307 · Cited by 154 · see citing works
Stillman, A. A., Krsnik, Ž., Sun, J., Rašin, M., State, M. W., šestan, N., & Louvi, A. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21919 · Cited by 95 · see citing works
STEEVES, T., & FOX, S. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00924-2 · Cited by 79 · see citing works
Yeh, C.-B., Lee, C.-S., Ma, K.-H., Lee, M.-S., Chang, C.-J., & Huang, W.-S. (2007) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2007.01.003 · Cited by 41 · see citing works
Evaluation of Tourette’s syndrome by 99mTc-TRODAT-1 SPECT/CT imaging
Liu, H., Dong, F., Meng, Z., Zhang, B., Tan, J., & Wang, Y. (2010) · Annals of Nuclear Medicine · doi:10.1007/s12149-010-0389-3 · Cited by 34 · see citing works
[99mTc]TRODAT-1/[123I]IBZM SPECT studies of the dopaminergic system in Tourette syndrome
Hwang, W.-J., Yao, W.-J., Fu, Y.-K., & Yang, A.-S. (2008) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2007.04.006 · Cited by 29 · see citing works
- Authors
- Albin, R. L., Koeppe, R. A., Bohnen, N. I., Nichols, T. E., Meyer, P., Wernette, K., Minoshima, S., Kilbourn, M. R., & Frey, K. A.
- Affiliations
- University of Washington (US)
- Venue
- Neurology
- Published
- 2003-08-12
- Volume
- 61
- Issue
- 3
- Pages
- 310-315
- ISSN
- 0028-3878 (ISSN-L)
- 1526-632X
- OpenAlex
- W1982077726
- Cited by
- 150
- References
- 42
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 1 · 2019: 5 · 2018: 4 · 2017: 3 · 2016: 5 · 2015: 3 · 2014: 4 · 2013: 11 · 2012: 14
- FWCI
- 13.29
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Michigan
- National Institute of Neurological Disorders and Stroke (P01NS015655)
- Topics
- Social Sciences › Psychology › Clinical Psychology › Obsessive-Compulsive Spectrum Disorders
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- Tourette syndrome, ventral striatum, dopaminergic innervation, tics, dihydrotetrabenazine, vesicular monoamine transporter, dorsal striatum, compartmental modeling
- MeSH terms
- Adolescent, Adult, Binding, Competitive, Body Fluid Compartments, Carbon Radioisotopes, Corpus Striatum, Female, Tourette Syndrome, Humans, Image Processing, Computer-Assisted, Ligands, Magnetic Resonance Imaging, Male, Membrane Glycoproteins, Middle Aged, Models, Biological, Neurons, Neuropeptides, Reference Values, Tetrabenazine, Tomography, Emission-Computed, Biogenic Monoamines, Presynaptic Terminals, Membrane Transport Proteins, Vesicular Biogenic Amine Transport Proteins, Vesicular Monoamine Transport Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
