Hostname: page-component-77c89778f8-fv566 Total loading time: 0 Render date: 2024-07-20T20:53:12.258Z Has data issue: false hasContentIssue false

Neuropathology in Tourette Syndrome

Published online by Cambridge University Press:  07 November 2014

Abstract

The unique clinical presentation of Tourette syndrome (TS) and its symptomatic response to dopamine antagonists are widely cited as evidence for the central role of the limbic-motor interface in the pathophysiology of TS. Nonetheless, the true neuropathology of TS remains elusive, even though significant advances have been made in understanding complex interconnected circuitries within the limbic system and basal ganglia. Neuropathologic and neuroimaging studies—plagued by small samples, clinical heterogeneity, and a number of interpretative problems—are generally supportive of pathology within the orbitofrontal cortex, striatum, and their efferent projections in TS. The specific patterns of abnormalities vary widely across these studies, clouding attempts to define a unifying neuropathology for this disorder. Converging yet circumstantial evidence for frontal cortical, and basal ganglia pathology in TS comes also from studies infields ranging from neuroimmunology to neuropsychology, and from the clinical overlap between TS and disorders such as obsessive-compulsive disorder, attention-deficit/hyperactivity disorder, and Sydenhams chorea. As a “model” neuropsychiatric disorder, TS has stimulated advances in several areas of neurobiology research, yet we still await a real understanding of its pathophysiology in order to move from empirically driven therapeutics to the development of targeted effective treatments.

Type
Feature Articles
Copyright
Copyright © Cambridge University Press 1999

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

REFERENCES

1.Penny, JB, Young, AB. Speculations on the functional anatomy of basal ganglia disorders. Annu Rev Neurosci. 1983; 6: 7394.CrossRefGoogle Scholar
2.Swerdlow, NR, Koob GF., Dopamine, schizophrenia, mania and depression: toward a unified hypothesis of cortico-striato-pallido-thalamic function. Behav Brain Sci. 1987; 10: 197245.CrossRefGoogle Scholar
3.Reiner, A, Albin, RL, Anderson, KD, D'Amato, CJ, Penney, JB, Young, AB. Differential loss of striatal projection neurons in Huntington disease. Proc Natl Acad Sci USA. 1988; 85: 57335737.CrossRefGoogle ScholarPubMed
4.Javoy-Agid, F, Ruberg, M, Taquet, H, et al. Biochemical neuropathology of Parkinson's disease. Adv Neurol. 1984; 40: 189198.Google ScholarPubMed
5.Marsden, CD. Motor disorders in basal ganglia disease. Hum Neurobiol. 1984; 2: 245250.Google ScholarPubMed
6.Krishnan, KRR, McDonald, WM, Escalona, PR, et al. Magnetic resonance imaging of the caudate nuclei in depression. Arch Gen Psychiatry. 1990; 49: 553557.CrossRefGoogle Scholar
7.Baxter, LR, Phelps, ME, Mazziotta, JC, et al. Local cerebral glucose metabolic rates in obsessive-compulsive disorder. Arch Gen Psychiatry. 1987; 44: 211218.CrossRefGoogle ScholarPubMed
8.Modell, JG, Mountz, JM, Curtis, GC, et al. Neurophysiological dysfunction in basal ganglia/limbic striatal and thalamocortical circuits as a pathogenetic mechanism of obsessive-compulsive disorder. J Neuropsychmtry. 1989; l: 2736.Google Scholar
9.Castellanos, FX. Toward a pathophysiology of attention-deficit/hyperactivity disorder. Clin Pediatr (Phila). 1997; 36: 381393.CrossRefGoogle Scholar
10.Rosenberg, DR, Keshavan, MS, O'Hearn, KM, et al. Frontostriatal measurement in treatment-naive children with obsessive-compulsive disorder. Arch Gen Psychiatry. 1997; 54: 824830.CrossRefGoogle ScholarPubMed
11.Modell, JG, Mountz, JM, Beresford, TP. Basal ganglia/limbic striatal and thalamocortical involvement in craving and loss of control in alcoholism. J Neuropsychiatry Clin Neurosci. 1990; 2: 123144.Google ScholarPubMed
12.Van Paesschen, W, Revesz, T, Duncan, JS, King, MD, Connelly, A. Quantitative neuropathology and quantitative magnetic resonance imaging of the hippocampus in temporal lobe epilepsy. Ann Neurol.1997; 42: 756766.CrossRefGoogle ScholarPubMed
13.Csernansky, JG, Kerr, S, Pruthi, R, Prosser, ES. Mesolimbic dopamine receptor increases two weeks following hippocampal kindling. Brain Res. 1988; 449: 357360.CrossRefGoogle ScholarPubMed
14.Swerdlow, NR. Cortico-striatal substrates of cognitive, motor and sensory gating: speculations and implications for psychological function and dysfunction. In: Panksepp, J, ed. Advances in Biological Psychiatry. Vol 2. Greenwich, Conn: JAI Press Inc; 1996: 179208.Google Scholar
15.McElroy, SL, Phillips, KA, Keck, PE Jr. Obsessive compulsive spectrum disorder. J Clin Psychiatry. 1994; 55: 3351.Google ScholarPubMed
16.Cohen, DJ, Leckman, JF, Pauls, D. Neuropsychiatric disorders of childhood: Tourette syndrome as a model. Ada Paediatr. 1997; 422: 106–lll.Google ScholarPubMed
17.Leckman, JF, Peterson, BS. The pathogenesis of Tourette syndrome: epigenetic factors active in early CNS development. Biol Psychiatry. 1993; 34: 425427.CrossRefGoogle ScholarPubMed
18.Swedo, SE, Leonard, HL, Garvey, M, et al. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases. Am J Psychiatry. 1998; 155: 264271.CrossRefGoogle ScholarPubMed
19.Palumbo, D, Maughan, A, Kurlan R., Hypothesis III: Tourette syndrome is only one of several causes of a developmental basal ganglia syndrome. Arch Neurol. 1997; 54: 475483.CrossRefGoogle ScholarPubMed
20.Walkup, J. Psychiatry of Tourette syndrome. CNS Spectrums. 1999; 4(2): 5461.CrossRefGoogle Scholar
21.Richardson, EP. Neuropathological studies of Tourette syndrome. Adv Neurol. 1982; 35: 8387.Google ScholarPubMed
22.Dewulf, A, van Bogaert, L. Etudes anatomo-cliniques de syndromes hypercinetiques complexes. III. Une observation anatomo-clinique de maladie des tics (Gilles de la Tourette). Monatsschr Psychiatr Neurol. 1941; 104: 5361.CrossRefGoogle Scholar
23.Balthasar, K. Uber das anatomische substrat der geralisierten Tic-Krankheit (maladie des tics, Gilles de la Tourette): entwicklungshemmung des corpus striatum. Arch Psychiatr Nervenkr (Berlin). 1957; 195: 531549.CrossRefGoogle Scholar
24.Kurlan, R. Investigating Tourette syndrome as a neurologic sequela of rheumatic fever. CNS Spectrums. 1999; 4(2): 6267.CrossRefGoogle Scholar
25.Haber, SN, Wolfer, D. Basal ganglia peptidergic staining in Tourette syndrome: a follow-up study. Adv Neurol. 1992; 48: 145150.Google Scholar
26.Haber, SN, Kowall, NW, Vonsattel, JP, Bird, ED, Richardson, EP. Gilles de la Tourette syndrome: a postmortem neuropathological and immunohistochemical study. J Neurol Sci. 1986; 75: 225241.CrossRefGoogle ScholarPubMed
27.Singer, HS, Hahn, IH, Moran, TH. Abnormal dopamine uptake sites in postmortem striatum from patients with Tourette syndrome. Ann Neurol. 1991; 30: 558562.CrossRefGoogle Scholar
28.Singer, HS. Neurochemical analysis of postmortem cortical and striatal brain tissue in patients with Tourette syndrome. Arch Neurol. 1992; 58: 135144.Google ScholarPubMed
29.Anderson, GM, Pollak, ES, Chatterjee, D, Leckman, JF, Riddle, MA, Cohen, DJ. Postmortem analysis of subcortical monoamines and amino acids in Tourette syndrome. Arch Neurol. 1992; 58: 123133.Google ScholarPubMed
30.Pulst, SM, Walshe, TM, Romero, JA. Carbon monoxide poisoning with features of Gilles de la Tourette syndrome. Arch Neurol. 1983; 40: 443444.CrossRefGoogle Scholar
31.Tarsy, D. Movement disorders with neuroleptic drug treatment. Psychiatr Clin North Am. 1984; 7: 453471.CrossRefGoogle ScholarPubMed
32.Mogenson, GJ, Yang, CR. The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv Exp Med Biol. 1991; 95: 267290.CrossRefGoogle Scholar
33.Leckman, JF, Riddle, MA, Berrettini, WH, et al. Elevated CSF dynorphin A [1–8] in Tourette syndrome. Life Sci. 1988; 43: 20152023.CrossRefGoogle Scholar
34.Weeks, RA, Turjanski, N, Brooks, DJ. Tourette syndrome: a disorder of cingulate and orbitofrontal cortex? Q J M. 1996; 89: 401408.CrossRefGoogle Scholar
35.Sandyk, R, Gillman, MA. Transient Gilles de la Tourette syndrome following alcohol withdrawal. Br J Addict. 1985; 80: 213214.CrossRefGoogle ScholarPubMed
36.Sandy, KR. The endogenous opioid system in neurological disorders of the basal ganglia. Life Sci. 1985; 37: 16551663.CrossRefGoogle Scholar
37.Baumgardner, TL, Singer, HS, Denckla, MG, et al. Corpus callosum morphology in children with Tourette syndrome and attention deficit hyperactivity disorder. Neurology. 1996; 47: 477482.CrossRefGoogle ScholarPubMed
38.Peterson, B, Riddle, MA, Cohen, DJ, et al. Reduced basal ganglia volumes in Tourette syndrome using three-dimensional reconstruction techniques from magnetic resonance images. Neurology. 1993; 43: 941949.CrossRefGoogle ScholarPubMed
39.Singer, HS, Reiss, AL, Brown, JE, et al. Volumetric MRI changes in basal ganglia of children with Tourette syndrome. Neurology. 1993; 43: 950956.CrossRefGoogle Scholar
40.Moriarty, J, Varma, AR, Stevens, J, Fish, M, Trimble, MR, Robertson, MM. A volumetric MRI study of Gilles de la Tourette syndrome. Neurology. 1997; 49: 410415.CrossRefGoogle Scholar
41.Castellanos, FX, Giedd, JN, Hamburger, SD, Marsh, WL, Rapoport, JL. Brain morphometry in Tourette syndrome: the influence of comorbid attention-deficit/hyperactivity disorder. Neurology. 1996; 47: 15811583.CrossRefGoogle ScholarPubMed
42.Mazziotta, JC, Phelps, ME. Positron emission tomography studies of the brain. In: Phelps, ME, Mazziotta, JC, Schelbert, HR, eds. Positron Emission Tomography and Autoradiography. New York, NY: Raven Press; 1986: 493580.Google Scholar
43.Braun, AR, Stoetter, B, Randolph, C, et al. The functional neuroanatomy of Tourette syndrome: an FDG-PET study. I. Regional changes in cerebral glucose metabolism differentiating patients and controls. Neuropsychopharmacology. 1993; 9: 277291.CrossRefGoogle Scholar
44.Moriarty, J, Costa, DC, Schmitz, B, Trimble, MR, Ell, PJ, Robertson, MM. Brain perfusion abnormalities in Gilles de la Tourette syndrome. Br J Psychiatry. 1995; 167: 249254.CrossRefGoogle Scholar
45.Moriarty, J, Eapen, V, Costa, DC, et al. HMPAO SPET does not distinguish obsessive-compulsive and tic syndromes in families multiply affected with Gilles de la Tourette syndrome. Psychol Med. 1997; 27: 737740.CrossRefGoogle ScholarPubMed
46.Sieg, KG, Buckingham, D, Gaffney, GR, Preston, DF, Sieg, KG. Tc-99m HMPAO SPECT brain imaging of Gilles de la Tourette syndrome. Clin Nucl Med. 1993; 18: 255.CrossRefGoogle Scholar
47.Riddle, MA, Rasmusson, AM, Woods, SW, et al. SPECT imaging of cerebral bloodflow in Tourette syndrome. AdvNeurol. 1992; 58: 207211.Google Scholar
48.Eidelberg, D, Moeller, JR, Antonini, A, et al. The metabolic anatomy of Tourette syndrome. Neurology. 1997; 48: 927934.CrossRefGoogle Scholar
49.Rauch, SL, Jenike, MA, Alpert, NM, et al. Regional cerebral blood flow measured during symptom provocation in obsessive-compulsive disorder using oxygen 15-labeled carbon dioxide and positron emission tomography. Arch Gen Psychiatry. 1994; 51: 6270.CrossRefGoogle ScholarPubMed
50.Peterson, BS, Skudlarski, P, Anderson, AW, et al. A functional magnetic resonance imaging study of tic suppression in Tourette syndrome. Arch Gen Psychiatry. 1998; 55: 326333.CrossRefGoogle ScholarPubMed
51.Wong, DF, Singer, HS, Brandt, J, et al. D2-like dopamine receptor density in Tourette syndrome measured by PET. J Nucl Med. 1997; 38: 12431247.Google ScholarPubMed
52.Syzmanski, S, Galiano, J, Yokoi, F, et al. Basal ganglia dopamine release in Tourette syndrome. J Nucl Med. 1997; 37 (suppl): 12P.Google Scholar
53.Malison, RT, McDougle, CJ, van Dyck, CH, et al. [1231] beta-CIT SPECT imaging of striatal dopamine transporter binding in Tourette disorder. Am J Psychiatry. 1995; 152: 13591361.Google Scholar
54.George, MS, Robertson, MM, Costa, DC, et al. Dopamine receptor availability in Tourette syndrome. Psychiatry Res. 1994; 55: 193203.CrossRefGoogle Scholar
55.Turjanski, N, Sawle, GV, Playford, ED, et al. PET studies of the presynaptic and postsynaptic dopaminergic systems in Tourette syndrome. J Neurol Neurosurg Psychiatry. 1994; 57: 688692.CrossRefGoogle Scholar
56.Wolf, SS, Jones, DW, Knable, MB, et al. Tourette syndrome: prediction of phenotypic variation in monozygotic twins by caudate nucleus D2 receptor binding. Science. 1996; 273: 12251227.CrossRefGoogle ScholarPubMed
57.Chokka, PR, Baker, GB, Bornstein, RA, de Groot CM. The biochemistry of Tourette syndrome. Metab Brain Dis. 1995; 10: 107124.CrossRefGoogle Scholar
58.Leckman, JF, Goodman, WK, Anderson, GM, et al. Cerebrospinal fluid biogenic amines in obsessive-compulsive disorder, Tourette syndrome, and healthy controls. Neuropsychopharmacology. 1995; 12: 7386.CrossRefGoogle ScholarPubMed
59.De Groot, CM, Bornstein, RA, Baker, GB. Obsessive-compulsive symptom clusters and urinary amine correlates in Tourette syndrome. J New Ment Dis. 1995; 183: 224230.CrossRefGoogle ScholarPubMed
60.Chappell, P, Riddle, M, Anderson, G, et al. Enhanced stress responsivity of Tourette syndrome patients undergoing lumbar puncture. Biol Psychiatry. 1994; 36: 3543.CrossRefGoogle ScholarPubMed
61.Dursun, SM, Farrar, G, Handley, SL, Rickards, H, Betts, T, Corbett, JA. Elevated plasma kynurenine in Tourette syndrome. Mol Chem Neuropathol. 1994; 21: 5560.CrossRefGoogle ScholarPubMed
62.Singer, HS, Giulano, JD, Hansen, BH, et al. Antibodies against human putamen in children with Tourette syndrome. Neurology. 1998; 50: 16181624.CrossRefGoogle ScholarPubMed
63.Schultz, RT, Carter, AS, Gladstone, M, et al. Visual-motor integration functioning in children with Tourette syndrome. Neuropsychology. 1998; 12: 134145.CrossRefGoogle ScholarPubMed
64.Georgiou, N, Bradshaw, JL, Phillips, JG, Bradshaw, JA, Chiu, E. The Simon effect and attention deficits in Gilles de la Tourette syndrome and Huntington's disease. Brain. 1995; 118: 13051318.CrossRefGoogle ScholarPubMed
65.Georgiou, N, Bradshaw, JL, Phillips, JG, Chiu, E. The effect of Huntington's disease and Gilles de la Tourette syndrome on the ability to hold and shift attention. Neuropsychologia. 1996; 34: 843851.CrossRefGoogle ScholarPubMed
66.Georgiou, N, Bradshaw, JL, Phillips, JG, Bradshaw, JA, Chiu, E. Advance information and movement sequencing in Gilles de la Tourette syndrome. J Neurol Neurosurg Psychiatry. 1995; 58: 184191.CrossRefGoogle Scholar
67.Castellanos, FX, Fine, EJ, Kaysen, D, Marsh, WL, Rapoport, JL, Hallett, M. Sensorimotor gating in boys with Tourette syndrome and ADHD: preliminary results. Biol Psychiatry. 1996; 39: 3341.CrossRefGoogle ScholarPubMed
68.Farber, RH, Swerdlow, NR, Clementz, BA. Saccadic performance characteristics and the behavioral neurology of Tourette syndrome. J Neurol Neurosurg Psychiatry. In press.Google Scholar
69.Swerdlow, NR, Magulac, M, Filion, D, Zinner, S. Visuospatial priming and latent inhibition in children and adults with Tourette disorder. Neuropsychology. 1996; 10: 485494.CrossRefGoogle Scholar
70.Smith, SJ, Lees, AJ. Abnormalities of the blink reflex in Gilles de la Tourette syndrome. J Neurol Neurosurg Psychiatry. 1989; 52: 895898.CrossRefGoogle ScholarPubMed
71.de Divitiis, E, D'Errico, A, Cerillo, A. Stereotactic surgery in Gilles de la Tourette syndrome. Ada Neurochir (Wien). 1977; 24: 73.Google Scholar
72.Hassler, R, Dieckmann, G. Sterotaxic treatment of tics and inarticulate cries or coprolalia considered as motor obsessional phenomena in Gilles de la Tourette disease. Rev Neurol (Paris). 1970; 123: 89100.Google Scholar
73.Korzen, AV, Pushkov, VV, Kharitonov, RA, et al. Stereotaxic thalamotomy in the combined treatment of Gilles de la Tourette disease. Zh Nevropatol Psikhiatr Im S S Korsakova. 1991; 91: 100101.Google Scholar
74.Robinson, D, Wu, H, Munne, RA, et al. Reduced caudate nucleus volume in obsessive-compulsive disorder. Arch Gen Psychiatry. 1995; 52: 393398.CrossRefGoogle ScholarPubMed
75.Leckman, JF, Zhang, H, Vitale, A, et al. Course of tic severity in Tourette syndrome: the first two decades. Pediatrics. 1998; 102: 1419.CrossRefGoogle ScholarPubMed
76.Gasser, T, Fahn, S, Breakefield, XO. The autosomal dominant dystonias. Brain Pathol. 1992; 2: 297–230.CrossRefGoogle ScholarPubMed
77.Insel, TR. Toward a neuroanatomy of obsessive-compulsive disorder. Arch Gen Psychiatry. 1992; 49: 739744.CrossRefGoogle Scholar