- Top of page
Aim: Although inconsistencies in neuropsychological impairments in Tourette's syndrome (TS) have been discussed with respect to comorbid disorders, such as obsessive–compulsive disorder, few studies have focused on the specific dimensions of obsessive–compulsive symptoms (OCS) related to TS, such as aggression and symmetry. The aim of this study was to explore the impact of specific TS-related OCS on neuropsychological performance.
Methods: A series of neuropsychological tasks examining attention and executive functioning were performed in groups of 33 TS participants and 18 healthy controls. The neuropsychological performance of TS with Aggression OCS (n = 11) were compared to TS without Aggression OCS (n = 22) and controls by using mancova controlling for age. In the same way as Aggression, we compared the performance of three groups by Symmetry: TS with Symmetry OCS (n = 14), TS without Symmetry OCS (n = 19) and controls.
Results: TS participants with Aggression OCS tended to make more perseverative errors than those without. Global OCS severity and tic severity did not correlate with any neuropsychological performances. No significant differences were detected between TS participants with and without Symmetry OCS.
Conclusion: Neuropsychological deficits in TS might be affected not by global OCS severity but by specific TS-related OCS.
TOURETTE'S SYNDROME (TS) is a chronic neurodevelopmental disorder with childhood onset characterized by motor tics and at least one vocal tic.1 Since TS is presumed to be related to dysfunction in frontal-striatal circuits,2 frontal dysfunctions in these circuits may lead to neuropsychological impairments.
However, the findings regarding cognitive impairments in TS are not unitary,3 which may be because of the heterogeneous characteristics of TS. Comorbidity is thought to be one of the factors contributing to such inconsistencies.4 Therefore, examining uncomplicated TS without comorbidities could be useful. It is suggested that uncomplicated TS is linked to mild impairments in certain inhibitory tasks.5 Although this approach has made a significant contribution, uncomplicated TS patients are rather rare (about 10%).3,6 This suggests that uncomplicated TS is only one of the subtypes of the disorder and does not explain TS as a whole. Ozonoff et al.4 suggested that a dimensional approach, such as those examining comorbidity or severity, might be more useful than a categorical approach.
Comorbid obsessive–compulsive symptoms (OCS) are commonly exhibited in TS: about 50% of those diagnosed with TS have prominent OCS.7 Also, OCS might affect neuropsychological aspects of TS.3,8,9 Numerous studies suggest that TS and obsessive–compulsive disorder (OCD) share a common dysfunction in frontal-striatal circuits,10 which is consistent with the idea that OCS and tics might be part of a spectrum.11 Therefore, we focused on the impact of OCS on neuropsychological performance.
OCS has distinctly heterogeneous clinical expressions. These clinically different symptoms were suggested to be associated with a distinct pattern of activation of neural regions.12 Therefore, different OCS contents should be associated with different aspects of neuropsychological deficits and some researches support this.13 Four symptom dimensions have been identified in factor analysis,14 two of which are associated with increased familial risk for OCD15 and TS.16 In those two dimensions associated with TS and OCD, the first dimension includes sexual and religious obsessions, and checking compulsions (which is labeled Aggression OCS in our study), and the second dimension includes symmetry and ordering obsessions and compulsions (which is labeled Symmetry OCS in our study). These symptoms are frequently observed in patients with TS.16,17 Therefore, we surmised that Aggression and Symmetry OCS must be related to TS and focused on the effect of these two types of OCS on neuropsychological tasks.
While few studies focused on neuropsychological aspects of Aggression and Symmetry OCS, some indicate indirectly that these two types of OCS might affect cognitive ability. Hartston and Swerdlow18 reported that abnormal performance patterns in visuospatial priming tasks were associated with these two types of OCS in OCD patients. Checking compulsions have also been examined with respect to impaired memory function19–21 and Milner-type errors on the Wisconsin Card Sorting Test (WCST).21 However, these studies did not focus on Aggression and Symmetry OCS separately. In addition, checking compulsions are inherently ambiguous and caused by different types of obsessions, including Aggression and Symmetry OCS.14,22 Therefore, we categorized checking compulsions according to the obsessions causing them.
As Aggression and Symmetry OCS are frequently seen in TS16,17 but have not been focused upon in previous research, an exploration of the effect of Aggression and Symmetry OCS on neuropsychological performance is warranted. Three neuropsychological tasks that examine executive functions and attention were utilized: the WCST, the Stroop Test, and the Continuous Performance Test (CPT).
The main purpose of this study was to investigate cognitive impairments in participants with TS with Aggression OCS and/or Symmetry OCS compared with TS participants without those OCS and with normal controls. We hypothesized that TS with Aggression OCS and/or Symmetry OCS would perform worse on some neuropsychological subsets than both TS without those OCS and normal controls.
- Top of page
The main finding in the current study is that TS participants with Aggression OCS made more perseverative errors than controls and TS participants without Aggression OCS, while no differences in any neuropsychological subsets were seen between TS with and without Symmetry OCS. Total tic severity score and global OCS severity scores did not correlate with any neuropsychological performance.
The finding that tic severity scores did not correlate with WCST performance aligns with previous studies that reported intact performance on the WCST in TS.3,32 In this study, global OCS severity scores were not associated with impaired performance on the WCST in TS. Instead, TS participants with Aggression OCS made more perseverative errors on the WCST, indicating that it was not global OCS severity but specific OCS that were related to impaired set-shifting ability. The results of previous studies that examined cognitive flexibility in OCD and TS compared with normal controls are inconsistent.3,33 So far, these inconsistencies have been discussed in the context of OCS severity.9,33 The current study, however, suggested that these results were not due to global OCS severity, but to specific dimension OCS, especially Aggression OCS.
Whereas previous studies indicated that checking compulsions are related to impaired memory ability19–21 and cognitive flexibility21 in OCD, the current study indicated that Aggression OCS in TS is related to impaired cognitive flexibility, regardless of the presence of checking compulsions. Aggression OCS would have different characteristics from other OCS, both etiologically34 and clinically.35,36 For example, the violence/aggression-dimension OCS have been associated with early onset OCD.34 Also, aggressive obsessions were reported more frequently in OCD patients with major depression compared to those without major depression.35 Furthermore, TS patients with aggression-dimension OCS had lower Global Assessment of Functioning scores and higher frequencies of coprolalia.36 The current study supposed that these clinical difficulties related to Aggression OCS might be partly due to cognitive inflexibility. No significant effects of Symmetry were seen in the current study, which might suppose a closer connection between Aggression OCS and cognitive dysfunction than those with Symmetry OCS.
TS participants tended to perform worse on the WCST with advancing age and duration of illness, while no age effect was found in the control group. As Aggression OCS were more frequent in older TS participants, this difference between TS and controls might be partly due to Aggression OCS.
In contrast to WCST performance, there were no effects of groups on the Stroop test and CPT, indicating that TS participants in the current study had ordinary attention and impulse-control abilities and ordinary ability to inhibit dominant responses.
Although the current study has some important implications, several limitations must be considered.
First, only preliminary examinations of the validity and reliability of the Japanese version of the DY-BOCS were completed,36 although the Japanese version of the DY-BOCS had good criterion-related validity with Y-BOCS in the current study.
A second limitation is that there existed overlap between Aggression OCS and Symmetry OCS. As effect sizes of differences on mancova implied that Aggression OCS related more strongly to cognitive impairments on WCST than Symmetry OCS, an interaction effect of Aggression OCS and Symmetry OCS was not considered.
A third limitation relates to the small number of participants and wide age distribution. In particular, TS participants with Aggression OCS tended to be older than those without Aggression OCS. While the difference between TS with and without Aggression OCS was significant after controlling for the effect of age, further studies with larger samples and age-matched comparisons between TS with and without Aggression and/or Symmetry OCS are needed.
In summary, TS participants with Aggression OCS made more perseverative errors than TS without Aggression OCS, while no differences in any neuropsychological subsets were seen between TS with and without Symmetry OCS. This indicates that it would be fruitful to examine specific OCS related to TS in order to explore heterogeneous aspects of TS.