Edited by: Hauke R. Heekeren, Freie Universität Berlin, Germany
Reviewed by: Nils I. Landro, University of Oslo, Norway; Bogdan Draganski, University of Lausanne, Switzerland
*Correspondence: Martial Mermillod, Laboratoire de Psychologie et Neurocognition, Université Pierre Mendès-France, BP 47, 38040 Grenoble Cedex 9, France. e-mail:
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Tourette’s syndrome (TS) is a neuropsychiatric syndrome defined by multiple chronic motor and vocal tics. Moreover, TS is a pathology associated with a high occurrence of comorbid conditions (Robertson,
In addition to the possibility of a potential emotional deficit in TS due to dopaminergic modulation at the level of the central nervous system, recent studies falling within the general framework of embodiment theory suggest that motor disorders at a peripheral level could have major consequences for both cognitive (Boulenger et al.,
A number of studies have been undertaken in order to investigate the possibility of emotional disorders in TS. Among these different studies, those performed by Sprengelmeyer et al. (
In addition to these global emotional deficits that are possibly induced by motor disorders, potential subcortical dysfunctions in TS may have other consequences for specific emotional processes that occur at the level of the basal ganglia. The subcortical hyperdopaminergy assumed to occur at the level of the basal ganglia in TS might induce a disturbance of subcortical limbic integration. This type of subcortical disturbance may have functional consequences for the integration of the low spatial frequency information associated with emotional stimuli. Various neuroimaging (Vuilleumier et al.,
We assumed that it might be possible to reveal widespread emotional deficits in TS by presenting the stimuli rapidly in order to reduce the use of perceptual strategies that may potentially compensate for emotional disorders. Moreover, based on the above-mentioned literature reporting a preferential link between subcortical emotional processes and LSF visual information, we assume that these emotional impairments might be observed more specifically on the LSF than on the HSF components of EFE. The average categorization rate of TS patients was compared with that of matched healthy controls (MHC).
The study protocol was approved by the regional Medical School Ethics Committee (AU701) and the study was conducted in accordance with the principles set out in the Declaration of Helsinki and with French legislation (the Huriet law). The nature and potential risks of the study were fully explained and written informed consent was obtained from each patient and MHC participant. The study was also registered with the clinical trial-specific website (NCT: 00664300).
Patients were included if they corresponded to a DSM-IV-R diagnosis of TS, stabilized for at least 1 month, and were receiving medical treatment. They were recruited during a multidisciplinary consultation at the Clermont-Ferrand and Lyon university hospitals. The diagnoses of TS and comorbidities were established by two experienced neurologists and psychiatrists. Patients with other comorbidities described below were excluded from the experiment.
In order to compare the performance of TS patients in the categorization of EFEs, these patients were paired with 18 healthy controls matched with them for age, gender, and educational level (Table
Sex | TS with OCD (9) |
Matched healthy controls (9) |
TS without OCD (9) |
Matched healthy controls (9) |
||||
---|---|---|---|---|---|---|---|---|
Female (3) | Male (6) | Female (3) | Male (6) | Female (3) | Male (6) | Female (3) | Male (6) | |
Mean | SD | Mean | SD | Mean | SD | Mean | SD | |
Age | 28.67 | 12.85 | 28.78 | 13.44 | 37.33 | 17.71 | 39.00 | 17.61 |
EL | 2.33 | 1.41 | 2.89 | 1.62 | 2.56 | 1.24 | 2.22 | 1.20 |
MMS | 29.00 | 1.00 | 29.89 | 0.33 | 29.78 | 0.44 | 30.00 | 0.00 |
The severity of the tics was evaluated using the Yale Global Tic Severity Scale (YGTSS) (Leckman et al.,
In order to characterize the comorbid psychiatric conditions that are most commonly encountered in TS (Cavanna et al.,
With regard to the potential ADHD, we first evaluated the patients using the Copeland Symptom Checklist for Adult Attention-Deficit Disorders (Copeland,
The final assessment of potential comorbidities was performed for each patient on the basis of the M.I.N.I. version 5.0.0 and an individual diagnosis established by a psychiatrist according to DSM-IV-R criteria (American Psychiatric Association,
We also assessed the patients for ADHD, OCD (based on Pauls’ questionnaire), anxiety and mood disorders based on the HAD and MDQ questionnaire, and tic severity (YGTSS). Both self-rating scales and an interview with a psychiatrist were necessary in order to classify the different types and lifetime appearances of obsessions or compulsions from which TS patients suffer (Worbe et al.,
Repetitive behaviors and thoughts were identified using the M.I.N.I. version 5.0.0, a semi-directed psychiatric interview (Worbe et al.,
First of all, IQ was assessed using the Wechsler Adult Intelligence Scale (WAIS-III, Wechsler,
A Mini Mental State (MMS, Folstein et al.,
Brickenkamp and Zillmer (
In order to assess for potential problems relating to prosopagnosia in the TS patients or MHC, we administered a Benton Facial Recognition Test. In the Benton Facial Recognition Test (Levin et al.,
Because we were investigating the ability to perform emotional categorization in different SF channels, we administered a VISTECH visual perception test to ensure that neither TS patients nor MHC were suffering from any visual deficit in specific SF channels. VISTECH is a standard test of sensitivity to contrast and spatial frequency in which participants are asked to determine the orientation of lines filtered at different spatial frequencies.
Finally, to assess whether the participants correctly understood emotional words, we administered a task requiring the semantic recognition of such words (Sprengelmeyer et al.,
The participants were tested individually in a shielded room where they sat at a viewing distance of 90 cm in front of a 19″ CRT ViewSonic® monitor connected to a PC. The experimental events were controlled by E-Prime® 1.2 (Psychology Software Tools, Pittsburg, PA, USA).
The images were taken from Ekman and Friesen’s (
In order to make it less likely that the participants would be able to use perceptual strategies to categorize the EFE, we employed a task in which they had to categorize EFEs that were presented only briefly. After a fixation cross had been presented for 5 s, an EFE was immediately displayed in the center of the computer screen for 200 ms. Each face was followed by a 30 ms mask to avoid retinal persistence. The participants performed a 12-trial training session in order to ensure that they correctly understood the aim of the task. This training session was followed by the experimental session which consisted of 210 trials. In response to each picture, and subject to no time constraints, the participants had to state the name of the EFE, which they categorized as one of the six basic emotions or as a neutral expression. To help them, they could see a card on which the names of the seven possible responses were written. Because of the motor disorders present in TS, the experimenter either pressed one of the seven keys corresponding to their responses or recorded the fact that the participant had not perceived the face at all. Moreover, because of potential attention disorders in TS, a screen was displayed before each trial and the participant pressed the space bar to move on to the next trial only when he or she was ready to do so.
We conducted an analysis of variance (ANOVA) on the ratio of correct responses for both the TS and MHC groups. We used a between-group repeated-measures ANOVA with the factors “EFEs” (Anger vs. Disgust vs. Fear vs. Happiness vs. Neutrality vs. Sadness vs. Surprise) and “Spatial Frequencies” (BSF; HSF; LSF) as within-subjects variables and Experimental Group (TS patients vs. MHC participants) as between-subject variable. In order to correct a violation of the sphericity assumption (inhomogeneity of covariance) for within-subject variables such as Emotion and Emotion × Group, we applied a Huynh–Feldt adjustment. Next, again due to the violation of sphericity, we conducted non-parametric analyses for local comparisons. Consequently, the categorization performance of the TS patients was compared with that of MHC using a two-tailed Mann–Whitney
First, we verified that age, sex, and level of education did not statistically differ between MHC and TS patients.
Eighteen TS patients (12 men, 6 women) aged 16–68 years (
TS N° | GAF | Disorders |
||||||
---|---|---|---|---|---|---|---|---|
Anxiety | OCD | Mood | Addictions | |||||
1 | 61 | – | – | No | – | – | – | – |
2 | 70 | – | – | No | MDD | Past | Alcohol | Past |
3 | 61 | – | – | No | – | – | – | – |
Agoraphobia | Past and present | |||||||
4 | 61 | Social phobia | Past and present | No | MDD | Past | – | – |
GAD | Past and present | |||||||
5 | 48 | Agoraphobia | Past and present | No | Suicide risk (light) | Present | Alcohol | Present |
6 | 50 | – | – | No | – | – | – | – |
7 | 50 | – | – | No | – | – | – | – |
8 | 41 | Social phobia | Past | No | – | – | – | – |
9 | – | No | Suicide risk (high) | Present | Cannabis | Past | ||
10 | 51 | Personality | Past and present | Yes | Suicide risk (light) | Present | ||
Hypomanic | Past | – | – | |||||
11 | 49 | GAD | Past | Yes | MDD | Past | – | – |
MDD | Present | |||||||
12 | 50 | – | – | Yes | Dysthymia | Present | – | – |
Manic episode | Past | |||||||
13 | 51 | Agoraphobia | Past and present | Yes | – | – | – | – |
14 | 41 | GAD | Past | Yes | MDD | Past | Alcohol | Past |
15 | 45 | GAD | Present | Yes | Suicide risk (light) | Present | – | – |
16 | – | – | – | Yes | – | – | – | – |
17 | – | GAD | Present | Yes | MDD | Past | – | – |
18 | 60 | Agoraphobia | Present | Yes | – | – | – | – |
GAD | Present |
TS with OCD (9) |
TS without OCD (9) |
TS (18) |
||||||
---|---|---|---|---|---|---|---|---|
Female (3) | Male (6) | Female (3) | Male (6) | Female (6) | Male (12) | |||
Mean | SD | Mean | SD | Mean | SD | |||
Age | 28.7 | 12.8 | 37.3 | 17.7 | 33.0 | 15.7 | ||
Wais-III | 98.4 | 14.1 | 102 | 15.3 | 100 | 14.4 | ||
MMS | 29.8 | 0.4 | 29.0 | 1.0 | 29.4 | 0.8 | ||
GAF | 49.6 | 5.88 | 55.3 | 9.47 | 52.8 | 8.26 | ||
Inattention/Distractibility | 52.4 | 22.2 | 31.7 | 23.7 | 42.1 | 24.7 | ||
Impulsiveness | 44.8 | 26.5 | 32.6 | 16.0 | 38.7 | 22.1 | ||
Overactivity/hyperactivity | 45.7 | 24.8 | 26.5 | 15.2 | 36.1 | 22.2 | ||
Underactivity | 37.3 | 19.8 | 26.5 | 19.6 | 31.9 | 19.9 | ||
Under-achievement/disorganization/learning disorder | 36.7 | 23.5 | 22.9 | 9.9 | 29.8 | 18.9 | ||
GZ | 419 | 172 | 426 | 61.0 | 448 | 70.2 | ||
14.3 | 19.9 | 20.6 | 14.7 | 18.5 | 17.2 | |||
GZ – F | 468 | 66.6 | 406 | 67.4 | 435 | 72.4 | ||
KL | 165 | 74.9 | 156 | 31.3 | 170 | 36.7 | ||
SB | 12.2 | 6.0 | 12.2 | 4.3 | 12.9 | 4.2 | ||
Reading 1 | 95.3 | 13.8 | 98.4 | 4.7 | 96.9 | 10.1 | ||
Reading 2 | 90.6 | 14.6 | 87.7 | 13.5 | 89.1 | 13.7 | ||
Spelling | 70.8 | 14.5 | 75.7 | 10.2 | 73.2 | 12.4 | ||
Interference | 42.4 | 10.2 | 39.2 | 11.0 | 40.8 | 10.4 | ||
Overall score | 28.3 | 11.6 | 36.4 | 14.0 | 32.4 | 13.1 | ||
Benton | 46.4 | 4.4 | 42.4 | 7.3 | 44.4 | 6.2 |
The patients obtained normal IQ scores of between 90 and 109 (
The scores obtained by the TS patients on Benton’s Facial Recognition Test did not differ statistically from those of the MHC (
A canonical analysis revealed a significant main effect of Emotion,
Moreover, and in accordance with the literature on presentation times above 50 ms (Schyns and Oliva,
BSF faces |
HSF faces |
LSF faces |
||||
---|---|---|---|---|---|---|
TS | MHC | TS | MHC | TS | MHC | |
Anger | 61.7* | 75.0 | 58.9 | 64.4 | 40.0 | 38.3 |
Disgust | 58.9 | 66.1 | 52.2 | 60.6 | 31.1 | 42.8 |
Fear | 67.2 | 54.4 | 53.9 | 47.8 | 40.0 | 46.7 |
Happiness | 93.3 | 96.7 | 92.2 | 95.6 | 87.8 | 96.1 |
Neutrality | 81.1 | 83.9 | 86.7 | 86.7 | 74.4 | 76.1 |
Sadness | 66.1 | 71.1 | 60* | 74.4 | 42.2 | 49.4 |
Surprise | 72.2* | 88.3 | 66** | 84.4 | 70.0 | 79.4 |
Local comparisons of TS and MHC were performed using a two-tailed Mann–Whitney
In order to understand how these misclassifications occurred in the TS patients, we computed an average confusion rate for TS and MHC participants. As shown in Figure
BSF faces |
HSF faces |
LSF faces |
||||
---|---|---|---|---|---|---|
TS | MHC | TS | MHC | TS | MHC | |
Anger | 6.3* | 4.17 | 6.57 | 5.83 | 9.54 | 9.91 |
Disgust | 6.39 | 5.56 | 7.50 | 6.11 | 10.93 | 9.26 |
Fear | 5.37 | 7.41 | 7.69 | 8.43 | 9.44 | 8.80 |
Happiness | 0.93 | 0.56 | 1.20 | 0.74 | 1.67 | 0.56 |
Neutrality | 3.06 | 2.50 | 2.04 | 2.13 | 4.54 | 4.44 |
Sadness | 5.00 | 4.35 | 5.93 | 3.80 | 8.70 | 7.87 |
Surprise | 5.28** | 2.13 | 5.93* | 3.06 | 4.91 | 3.52 |
In the same way as for the correct categorization rate, the canonical analysis revealed a significant main effect of Emotion,
Because there was no systematic homogeneity of covariance, we used a two-tailed Mann–Whitney
In order to test the possibility of a relationship between the severity of the tics and emotional impairment in the recognition of facial expressions, we applied a median split (median value = 37) to the YGTSS results. The ANOVA on the factors “EFEs” and “Spatial Frequencies” as within-subjects variables and Experimental Group (low YGTSS patients vs. high YGTSS patients) as between-subject variable revealed no significant differences for EFE, SF, Experimental Group, or any significant interactions among these factors.
In the light of Sprengelmeyer et al.’s (
Nine TS patients with OCD were compared with nine TS patients without OCD in terms of their ability to correctly categorize EFE. An ANOVA corrected for non-sphericity revealed that the OCD factor (TS with OCD vs. TS without OCD) was significant,
Our current results indicate that, once the potential use of cognitive strategies based on a perceptual analysis of the images had been restricted, TS patients produced significant impairments in response to the EFEs of anger and surprise in unfiltered BSF faces. Moreover, the results revealed a significantly lower level of recognition of sadness and surprise in the HSF channels but no impairments on LSF faces. In addition, it is possible that the same trend observed for other emotional expressions (the happy and disgusted EFEs, in particular) might not be significant due to a lack of power or because our task, even though it reduced the possible use of
Since HSF are processed by temporal cortical areas, these results suggest that the locus of the potential dysfunctioning of emotional processes in TS may be found at the level of temporal cortical areas rather than subcortical structures. This possibility is consistent with the neural basis of embodiment theory (Niedenthal et al.,
We also observed a specific deficit on disgusted faces which was limited to TS without OCD only. These results reveal striking differences with previous papers on this topic involving TS patients (Sprengelmeyer et al.,
Without OCB | With OCB | |
---|---|---|
Cleaning/washing | 0.00 | 37.04 |
Checking | 1.85 | 14.81 |
Repetition | 0.00 | 27.78 |
Count | 11.11 | 22.22 |
Ordering/order | 3.70 | 37.04 |
Collection | 0.00 | 44.44 |
Others | 3.70 | 17.78 |
Aggressivity | 1.59 | 14.29 |
Contamination | 0.00 | 11.11 |
Sexual | 0.00 | 11.11 |
Collection, accumulation | 11.11 | 0.00 |
Religious | 0.00 | 0.00 |
Symmetry, accuracy, order | 1.85 | 20.37 |
Others | 4.76 | 23.02 |
Physical | 0.00 | 18.52 |
Finally, we did not observe any difference between TS patients and MHC participants on LSF faces. It therefore seems that emotional impairments in TS may not be due to a deficit at the level of subcortical structures. One theoretical interpretation of our findings is that a potential hyperdopaminergy of subcortical structures (Albin and Mink,
The current study indicates that the rapid visual presentation paradigm makes it possible to identify various EFE deficits (at the level of the emotions of anger and surprise) that are not revealed by the standard visual presentation procedure previously reported in the literature (Sprengelmeyer et al.,
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This work was supported by the French National Center for Scientific Research (UMR 6024), the Institut Universitaire de France, Grant ANR-06-BLAN-0360-01 and Grant ANR-BLAN08-1_353820 from the French National Research Agency (ANR) awarded to Martial Mermillod and “Programme Hospitalier de Recherche Clinique” as well as by the Universitary Hospital Center of Clermont-Ferrand and the French Association of Gilles de la Tourette Syndrome (AFSGT) which provided financial support to Isabelle Jalenques and Franck Durif. The authors thank the patients who participated in this study.