Pathophysiological evidence suggests an involvement of frontostriatal circuits in Tourette syndrome (TS) and cognitive abnormalities have been detected in tasks sensitive to cognitive deficits associated with prefrontal damage (verbal fluency, planning, attention shifting, working memory, cognitive flexibility, and social reasoning). A disorder in counterfactual thinking (CFT), a behavioural executive process linked to the prefrontal cortex functioning, has not been investigated in TS. CFT refers to the generation of a mental simulation of alternatives to past factual events, actions, and outcomes. It is a pervasive cognitive feature in everyday life and it is closely related to decision-making, planning, problem-solving, and experience-driven learning—cognitive processes that involve wide neuronal networks in which prefrontal lobes play a fundamental role. Clinical observations in patients with focal prefrontal lobe damage or with neurological and psychiatric diseases related to frontal lobe dysfunction (e.g., Parkinson’s disease, Huntington’s disease, and schizophrenia) show counterfactual thinking impairments. In this work, we evaluate the performance of CFT in a group of patients with Tourette’s syndrome compared with a group of healthy participants. Overall results showed no statistical differences in counterfactual thinking between TS patients and controls in the three counterfactual measures proposed. The possible explanations of this unexpected result are discussed below.
Tourette’s syndrome (TS) is a neuropsychiatric disorder characterized by chronic multiple motor tics and one or more phonic/vocal tics, defined as semivoluntary, repetitive, and stereotyped movements and vocalization [
There is still debate as to the extent to which TS is associated with cognitive impairment. In general, subtle cognitive changes have been detected in tasks involving verbal fluency, planning, attention shifting, working memory, cognitive flexibility, and social reasoning [
CFT is the capacity to “do otherwise” in situations and is critically influenced by the ability to mentally represent possible behaviours and probable scenarios. This human skill is known as counterfactual reasoning, or thinking (CFT), and consists of the “
Recent neuroscientific evidence suggests that CFT is active in different brain regions. Barbey et al. [
Studies conducted with patients with frontal lobe damage provide evidence that they cannot generate a normal level of different behaviours and their choices are made using a very limited number of alternatives [
Two main methods have been proposed for the quantitative evaluation of CFT [
Here we compared patients with TS and healthy controls on measures of CFT. This represents a novel direction in TS literature since difficulty with CFT has been hypothesized in this population but has not previously been examined.
Forty-eight consecutive adult patients with TS were recruited from two centres, the Movement Disorders and Tourette Centre of the Department of Functional Neurosurgery, IRCCS Galeazzi, Milan, Italy, and the San Marco Hospital of Zingonia in Bergamo, Italy. The group was composed of 14 females and 34 males. The average age of patients was 33.9 (SD 11.7), with a mean age onset of tic at 8.2 years (SD 4.4), ranging from 18 to 60 years of age. Ten patients out of 48 already had an activated deep brain stimulation (DBS) implant.
Patients met the DSM-V [
Demographic, clinical, and neuropsychological data of TS patients (
Factors | TS patients ( |
Controls ( |
| ||
---|---|---|---|---|---|
M (SD) |
|
M (SD) |
| ||
Age (years) | 33.9 (11.7) | 48 | 30.5 (9.3) | 46 | 0.12 |
Gender (female/male) | 14/34 | 48 | 14/32 | 46 | 0.93 |
Education (years) | 10.9 (3,2) | 48 | 10.9 (3.3) | 46 | 0.90 |
Right/left-handed | 43/5 | 48 | 40/6 | 46 | 0.74 |
Onset of the disease (years) | 8.3 (4.4) | 45 | |||
DBS (yes/not) | 10/38 | 48 | |||
YGTSS (total score) | 36.9 (24.7) | 48 | |||
DEX-S (total score) | 24.9 (14.8) | 47 | cut off >18 | [ |
|
MMSE (total score) | 28.2 (1.6) | 48 | cut off 23.80 | [ |
|
Verbal fluency (total score) | 27.2 (8.9) | 48 | cut off >17 |
[ |
|
FAB (total score) | 15.3 (1.4) | 48 | cut off >13.50 | [ |
Presence of comorbidity and associated symptoms in TS patients. Data are expressed in percentage (%).
Comorbidities/coexisting symptoms | TS patients |
---|---|
OCB/OCD (YBOCS total score ≥16) | 75% |
SIB | 22% |
ADHD | 67% |
DSA | 35% |
Behavioural disorders | 69% |
Depression | 30% |
Anxiety | 73% |
To evaluate the cognitive status of each patient, in addition to the
CFT was evaluated using three measures, proposed by Hooker et al. [
The third CFT test focuses on the
The
Scenery | Response | |
---|---|---|
(1) | Janet is attacked by a mugger only 10 metres from her house. |
( |
|
||
(2) | Ann gets sick after eating at a restaurant she often visits. |
(a) Ann |
|
||
(3) | Jack misses his train by five minutes. Ed misses his train by more than one hour. |
( |
|
||
(4) | John gets into a car accident while driving on his usual way home. |
(a) John |
One-third of participants received the scenario exactly as described above (
The last third of participants were asked to imagine an alternative end to the same scenario (
Different endings in versions A and B are aimed at inducing a specific CFT that evokes a feeling of regret, influencing participants’ decision-making. In fact, the anticipation of counterfactual regret is assumed to influence later behavioral intentions. Prior to a decision, participants induced to consider a potential regret (versions A and B) will be more likely to choose behaviors that minimize the chances of experiencing that negative regret.
After imaging themselves in these situations, participants were asked to decide whether they would go back to check their car or go straight to the office for the job interview.
Finally, we also assessed the participants’ level of
As reported in Table
Correct responses produced by TS patients and in control subjects in
Correct responses produced by under 30-year-old and over 30-year-old TS patients in
To analyze if age among TS patients played a part in performance, we divided the TS sample into two subgroups one under 30 years old and the second over. Using the Mann-Whitney statistical test, we found that three measures (YGTSS, FAB, and Verbal Fluency) revealed better scores among TS patients over thirty years old (see Table
Differences between under 30 years old and over 30 years old TS patients.
Factors | TS patients 18–30 y |
TS over 30 y |
|
---|---|---|---|
YGTSS (total score) | 49.1 (23.4) | 26.6 (21.2) | 0.001* |
MMSE (total score) | 28.1 (1.5) | 28.4 (1.6) | 0.51 |
Verbal fluency (total score) | 22.5 (8.8) | 31.1 (7.1) | 0.0005* |
FAB (total score) | 14.7 (1.2) | 15.7 (1.3) | 0.01* |
DEX (total score) | 28.4 (14.2) | 22.1 (15.1) | |
DBS (1) | 18 (81.8%) | 20 (76.9%) | 0.74# |
Gender (2) | 15 (68.2%) | 19 (73.1%) | 0.76# |
Education | 10.8 (3.3) | 10.9 (3.1) | 0.87 |
CFT | |||
Spontaneous generation (number of alternatives) | 2.6 (1.1) | 2.0 (1.3) | 0.12 |
CIT (total score) | 1.8 (1.2) | 1.65 (1.2) | 0.64 |
Regret (1) | 12 (54.6%) | 16 (61.5%) | 0.77# |
Confidence level (0–5) | 3.45 (0.96) | 3.92 (1.02) | 0.110 |
Over the last decade, there has been an accumulating body of evidence showing that CFT is sustained by a brain network in which a main role is played by the prefrontal cortex. Patients with focal prefrontal lobe damage or with neurological and psychiatric diseases related to frontal lobe dysfunction (e.g., Parkinson’s, Huntington’s, and schizophrenia) show CFT impairments. A deficit in CFT has only been hypothesized but never examined in TS.
Thus, the aim of this study is to analyze, for the first time, CFT in a sample of 48 adults with TS, compared to a group of healthy control participants. We administered three CFT measures: one focused on the frequency of counterfactual thinking in response to a personal real-life event, one showing that affective and judgmental reactions regarding social events are influenced by counterfactual thinking, and one on the influence of anticipated counterfactual regrets on behaviour. Data demonstrated that the TS group was able to generate as comparable a numbers of alternatives, in response to recalling a negative event, as were controls. TS patients were also as skilful as controls in using CFT in order to make inferences regarding hypothetical social events. This could be considered an unexpected result if we look at previous studies on patients with frontostriatal damage, such as Parkinson’s and Huntington’s, in which an impairment in CFT was detected. However, some accounts can be offered to explain this result.
When compared with PD and HD patients, TS patients display a dissimilar involvement of the basal ganglia and different evolutions of the cognitive condition over time. It is well documented that in early adulthood, roughly three-quarters of TS patients will have greatly diminished childhood tic symptoms and over one-third will be tic free [
We can speculate that also the cognitive status, including executive functions, may follow a similar trend in TS. Differently to conditions involving progressive subcortical neurodegeneration, such as PD and HD, in TS the potential heterogeneity determines varied neural abnormalities and a clinical course in which changes in cognitive function may range from mild to absent. Varied prefrontal circuitry may be involved in TS and such differences in the syndrome leave room for the possibility that in a considerable number of patients prefrontal functions are partially or totally preserved. Our TS patients could be considered to represent a group whose executive functions are relatively intact, especially when measured through CFT tasks that do not appear to evaluate these abilities in depth. Moreover, another explanatory hypothesis takes into account the ability of working memory. The production of CFT requires an important load of the working memory: to evoke a counterfactual thought, it is necessary to hold the memory of a past unpleasant event in the working memory long enough to compare what actually happened with the counterfactually derived alternative. To hold such complex information in the working memory requires resisting interference, which is a well-documented process mediated by the prefrontal lobes. Thus, CFT tests are strongly mediated by working memory abilities. Several studies showed how TS patients do not differ significantly from healthy subjects on measures of working memory [
The authors declare that there is no conflict of interests regarding the publication of this paper.