Bilateral globus pallidus lesions in a patient with Tourette syndrome and related disorders

doi:10.1016/S0006-3223(99)00087-6

Biological Psychiatry

Volume 46, Issue 6, 15 September 1999, Pages 863-867

https://doi.org/10.1016/S0006-3223(99)00087-6 Get rights and content

Abstract

Background: The neuroanatomic and pathologic basis of Tourette’s syndrome or related disorders such as obsessive-compulsive disorder and attention deficit-hyperactivity disorder remains unknown. Although a substantial body of neuroimaging and other data implicate basal ganglia and some point out specifically the globus pallidus in the etiopathogenesis of these three related disorders, no clear or pathologically significant isolated lesions restricted to this region have yet been demonstrated, with the exception of obsessive-compulsive disorder.

Methods: A seventeen-year-old male case of Tourette syndrome with comorbid obsessive-compulsive disorder, attention deficit-hyperactivity disorder, stuttering and gait disturbance, who had negative family history is presented.

Results: The patient has failed to respond to drug treatment and his MRI scan revealed bilateral and symmetrical globus pallidus lesions with specific “tiger’s eye” appearance of unknown etiology.

Conclusions: Well-localized lesions in the globus pallidus support growing data suggesting the involvement of this brain region in Tourette syndrome and related disorders.

Introduction

Although neuroanatomic and pathologic basis of Tourette syndrome (TS) remains unknown, a substantial body of data implicates basal ganglia (BG) (Moriartry et al 1997) and some researchers point out specifically the globus pallidus (GP) Haber and Wolfer 1992, Peterson et al 1993b, Robertson et al 1990, Singer et al 1993. We present a case with TS and related comorbidities such as obsessive-compulsive disorder (OCD) and attention-deficit hyperactivity disorder (ADHD), stuttering, and gait disorder in whom radiologic evidence was found bilaterally and restricted to the GP, with specific “tiger’s eye” appearance.

Section snippets

Case report

A seventeen-year-old male patient was referred by his family to the inpatient unit of a university hospital with the complaints of stuttering, aggressive behavior, coordination difficulties when walking and sitting, and a history of one suicide attempt. His chief complaint was stuttering, which had been evident at around the age of 9 years and become increasingly prominent. Childhood history included hyperactive and inattentive behavior, frequent falls with multiple head injuries, and failure

Discussion

Whether the GP lesions visible on the MRI are congenital or acquired, static or degenerative is unknown. Multiple head traumas in childhood could be an explanation. There is no evidence of perinatal anoxia or carbon monoxide poisoning. He was fully conscious when he arrived at the emergency room after the suicide attempt, thus anoxia following profuse blood loss was ruled out as a possible cause of the lesions. Besides, neurologic deficits such as gait disturbance or motor incoordination, which

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Spatio-temporal gait characteristics in children with Tourette syndrome: A preliminary study
2014, Research in Developmental Disabilities
Citation Excerpt :
The age influence of the gait was not explored in the present study because of the small sample size. Previous case reports have indicated that some subjects with severe tic problems demonstrate tic-induced gait problems (Fasano et al., 2012), and visually obvious gait problems (Demirkol et al., 1999). Therefore, a future study might fruitfully longitudinally examine the relationship between tic severity and gait performance in children with TS.
Earlier studies had suggested that variability of stride length in gait is a pathological sign of basal ganglia disease. Some evidence implicates the involvement of the basal ganglia and related thalamocortical circuitry in Tourette syndrome (TS). To date, the gait of subjects with TS has only discussed in case reports. This investigation compared the spatial and temporal gait characteristics of a sample of children with TS (N = 8) with those of healthy controls (HC; N = 8). All children were instructed to walk under two speed conditions: “preferred” and “fastest.” Gait parameters were measured using an electronic walkway. Spatial and temporal gait parameters were compared using a two-way (group) × (conditions) repeated measures ANOVA. The preliminary results suggested that similar to HC children, children with TS were capable of regulating temporal characteristics of gait based on walking speed. They also exhibited subtle gait anomalies such as irregular step length, as evidenced by significant differences in step length differential (p = 0.003), detectable despite the small sample size. These findings warrant further investigation into the gait control of children with TS.
Neurosurgical targets for compulsivity: What can we learn from acquired brain lesions?
2013, Neuroscience and Biobehavioral Reviews
Citation Excerpt :
Laplane et al. (1989) described three patients with checking and counting compulsions, stereotypy and apathy following bilateral globus pallidus lesions. Demirkol et al. (1999) described a 17-year-old male with bilateral globus pallidus lesions, who subsequently developed washing and orderliness compulsions. This patient also developed stuttering and Tourette's syndrome with simple and complex motor and vocal tics.
Treatment efficacy of deep brain stimulation (DBS) and other neurosurgical techniques in refractory obsessive-compulsive disorder (OCD) is greatly dependent on the targeting of relevant brain regions. Over the years, several case reports have been published on either the emergence or resolution of obsessive-compulsive symptoms due to neurological lesions. These reports can potentially serve as an important source of insight into the neuroanatomy of compulsivity and have implications for targets of DBS. For this purpose, we have reviewed all published case reports of patients with acquired or resolved obsessive-compulsive symptoms after brain lesions. We found a total of 37 case reports describing 71 patients with acquired and 6 with resolved obsessive-compulsive symptoms as a result of hemorrhaging, infarctions or removal of tumors. Behavioral symptoms following brain lesions consisted of typical obsessive-compulsive symptoms, but also symptoms within the compulsivity spectrum. These data suggests that lesions in the cortico-striato-thalamic circuit, parietal and temporal cortex, cerebellum and brainstem may induce compulsivity. Moreover, the resolution of obsessive-compulsive symptoms has been reported following lesions in the putamen, internal capsule and fronto-parietal lobe. These case reports provide strong evidence supporting the rationale for DBS in the ventral striatum and internal capsule for treatment of compulsivity and reveal the putamen and fronto-parietal cortex as promising new targets.
Obsessive-compulsive disorder
2012, Handbook of Clinical Neurology
Citation Excerpt :
In OCD, cognitions and motivations to act would persist (as obsessions with attendant anxiety), since feedback from motor behavior would fail to reset these thoughts and motivations, driving repetitive stereotyped behaviors (compulsions) (Rauch, 2003). Although relatively few in number, there are striking case reports in which obsessions and compulsions developed after damage to corticobasal sites implicated in OCD, including the basal ganglia (Laplane et al., 1989; Demirkol et al., 1999; Thobois et al., 2004), orbitofrontal cortex (Ogai et al., 2005), a midline tumor affecting the caudate, lenticulate, internal capsule, and interventricular septum (Gamazo-Garran et al., 2002), or traumatic brain injury (Ko, 1997; Berthier et al., 2001), including focal contusions in the frontotemporal cortices, subcortical structures (caudate nucleus), or both. More recently, obsessional symptoms were reported to increase rapidly after resection of left frontal primary brain tumors (Mainio et al., 2005).
Activity modulation of the globus pallidus and the nucleus entopeduncularis affects compulsive checking in rats
2011, Behavioural Brain Research
Citation Excerpt :
The STN is highly connected with the internal and external segments of the globus pallidus (GP) [29]. Furthermore, bilateral GP lesions have been shown to induce OC symptoms [27], and the GP has been shown to be hyperintense [28] or of altered volume [29–32] in OCD patients compared to healthy controls. Together, these reports implicate the pathophysiological relevance of the GP in OCD.
Deep brain stimulation at high frequencies (HFS) is currently studied in the treatment of therapy-refractory obsessive–compulsive disorder (OCD). The diversity of targeted brain areas and the discrepancy in demonstrating beneficial effects, highlight the need for better mapping of brain regions in which HFS may yield anti-compulsive effects. This goal may be achieved by investigating the effects of HFS in appropriate animal models of OCD. The present study tested the effect of bilateral HFS or pharmacological inactivation (as induced by intracerebral administration of the GABA-agonist muscimol) of both the Globus pallidus (GP; rodent equivalent to human GP externus) and the Nucleus entopeduncularis (EP; rodent equivalent to human GP internus) on checking behaviour in the quinpirole rat model of OCD. We demonstrate that HFS of the GP does not and HFS of the EP only partially reduces OCD-like behaviour in rats. In contrast, pharmacological inactivation of both GP and EP significantly reduces OCD-like behaviour in the model. These data contrast previously derived data on the effectiveness of HFS of the subthalamic nucleus, nucleus accumbens, GP and EP in the same and other rat models of OCD. We conclude that (i) although GP and EP play an important role in the pathophysiology of OCD, these areas may not represent first choice target structures for HFS, (ii) the effectiveness of HFS may depend on different subtypes of OCD, represented in different animal models, and (iii) differential net mechanisms may subserve the effectiveness of HFS and pharmacological inactivation.
The semantic Simon effect in Tourette's syndrome and obsessive-compulsive disorder
2006, Brain and Cognition
Core symptoms of Tourette’s syndrome (TS) and obsessive-compulsive disorder (OCD) may be attributed to an impairment in inhibitory control. Neuropsychological studies have addressed inhibition in both disorders, but findings have been inconsistent. The aim of this study was to examine cognitive inhibition, using a semantic Simon effect paradigm, in patients with TS and OCD. Furthermore, to address comorbidity a group of TS + OCD patients was also examined. Results indicated that patients with TS and OCD were affected by the inhibitory components of the task. TS groups performed similarly to controls on simple and choice RT tasks, but were particularly compromised as increasingly complex inhibitory demands were imposed. OCD patients were slower and committed more errors than controls, especially in the more cognitively demanding conditions, and were particularly disadvantaged by incongruent stimulus-response compatibilities. Findings implicate possible fronto-striatal dysfunction, are consistent with previously reported inhibitory deficits in TS and OCD, and support the theory that comorbid TS + OCD is more closely linked to pure TS than OCD.
Electrophysiological characteristics of limbic and motor globus pallidus internus (GPI) neurons in two cases of Lesch-Nyhan syndrome
2005, Neurophysiologie Clinique
Objective. – Lesch–Nyhan syndrome is a rare and debilitating condition characterized by dystonia and self-mutilating behavior. In order to shed light on the pathophysiology of dystonia, we report the pallidal electrophysiological activity recorded in two patients during deep brain stimulation surgery (DBS).
Methods. – Microrecordings were performed on 162 neurons along four tracks aimed at the right and left anterior (limbic) and posterior (motor) globus pallidus internus (GPI).
Results. – Regardless of the anesthetic agent used (propofol or sevoflurane), both patients showed similar neurons firing rates in the four regions studied, namely the limbic and motor portions of the globus pallidus externus (GPE) or GPI. In both patients, firing rates were similar in the GPE (12.2 ± 1.8 Hz, N = 38) and GPI (13.2 ± 1.0 Hz, N = 83) portions of the limbic track, while the motor GPE fired at a higher frequency (23.8 ± 2.7 Hz, N = 18) than the motor GPI (12.5 ± 1.4 Hz, N = 23).
Conclusions. – These results demonstrate that light propofol or sevoflurane anesthesia influences pallidal activity in a similar way. Electrophysiological recordings suggest that Lesch–Nyhan syndrome might be characterized by analogous firing frequencies in the limbic GPE and GPI while motor GPE would tend to fire at higher rate than the motor GPI. It is therefore tempting to suggest that the symptoms that are observed in Lesch–Nyhan syndrome might result from motor GPI inhibition.
Significance. – This observation may confirm the Albin and Delong's model of the basal nuclei in hypokinetic and hyperkinetic disorders.
Objectifs. – Le syndrome de Lesch-Nyhan est une pathologie rare, caractérisée par une dystonie accompagnée d'actes d'automutilation. Pour mieux comprendre la physiopathologie de cette maladie, nous avons enregistré l'activité électrophysiologique chez deux patients lors de la pose de stimulateurs profonds (DBS) dans le pallidum.
Méthode. – Des enregistrements unitaires ont été effectués sur 162 neurones le long de 4 trajectoires en direction du pallidum interne (GPI) antérieur (limbique) et postérieur (moteur).
Résultats. – Quel que soit l'agent anesthésique utilisé (propofol ou sévoflurane), les deux patients montrèrent des fréquences de décharge similaires dans les quatre régions étudiées, soit le pallidum externe (GPE) moteur et limbique et le GPI limbique et moteur. Chez les deux patients, les fréquences de décharges étaient similaires dans le GPE (12.2 ± 1.8 Hz, n = 38) et le GPI (13.2 ± 1.0 Hz, n = 83) limbique alors que le GPE moteur déchargeait à une fréquence plus élevée (23.8 ± 2.7 Hz, n = 18) que le GPI moteur (12.5 ± 1.4 Hz, n = 23).
Conclusions. – Ces résultats montrent qu'une légère anesthésie au propofol ou au sévoflurane modifie de manière similaire l'activité dans le pallidum. Les enregistrements électrophysiologiques suggèrent que le syndrome de Lesch-Nyhan pourrait être caractérisé par des fréquences de décharge analogues dans le GPE et le GPI limbique alors que le GPE moteur déchargerait avec une fréquence plus élevée que le GPI moteur. Il est donc tentant de penser que les symptômes observés dans la maladie de Lesch-Nyhan correspondraient à une inhibition du GPI.
Signifianc. – Cette observation va dans le sens du modèle de Albin et Delong de fonctionnement des noyaux gris centraux dans les mouvements anormaux.

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Case ReportBilateral globus pallidus lesions in a patient with Tourette syndrome and related disorders

Abstract

Introduction

Section snippets

Case report

Discussion

Trends Neurosci

Psychiatr Clin North Am

J Am Acad Child Adolesc Psychiatry

Biol Psychiatry

Trends Neurosci

Psychiatry Res: Neuroimag

Magn Reson Imaging

Biol Psychiatry

Basal ganglia volumes in children with attention-deficit hyperactivity disorder

J Child Neurol

Uber das anatomische substrat der generalisierten tic-krankeit (maladie des tics, Gilles de la Tourette)Entwicklungshemmung des corpus striatum. (On the anatomic substrate of generalized tic-disorder (maladie des tics, Gilles de la Tourette): Developmental defect of the corpus striatum.)

Archiv für Psychiatrie und Nervenkrankheit