Compared to healthy controls (HCs), adult Tic Disorder (TD) patients exhibit a lower interoceptive accuracy (IAcc) in heartbeat perception. Since the lower IAcc is not evident in children, the age at which tics develop, but in adults only (Pile et al., 2018, https://doi.org/10.1007/s10803-018-3608-8), lower IAcc may reflect a pathological mechanism relevant with regard to tics, premonitory urges (PUs) or the resulting impairment. Although tics are a motor phenomenon, up to date, IAcc has been assessed only with a heartbeat-counting task. This study aims at comparing cardiac and muscular IAcc using two different paradigms and investigates how IAcc is related to premonitory urges in youth.
Interoceptive measures (heartbeat-counting task, muscle tension paradigm) of 28 youth with TD were compared to 23 control participants and related to self-rated premonitory urges and tic symptoms.
TD patients did not differ from HCs in any IAcc measures. However, within TD patients, IAcc explained additional variance in PUs when controlling for tic severity. Muscular IAcc in TD patients is related to urges and tics, but the direction of this association is unclear. IAcc is lower in TD patients than in HCs, indicating imprecise sensory input which is more easily overcome by priors within the predictive coding framework.
Muscle tension feedback tasks could extend interoceptive trainings aimed at improving IAcc to improve accuracy of urge perception (more precise sensory input) to foster the ability to control tics via HRT. Longitudinal studies could provide further insights in causal relationships between IAcc, premonitory urges and tics.
A muscle tension paradigm assessed interoceptive accuracy. Patients with tics did not differ from healthy controls in interoceptive accuracy. Muscular interoceptive accuracy in patients relates to premonitory urges and tics. Muscular tension feedback tasks could improve treatment via habit reversal training.
Tics are sudden repetitive movements or vocalizations that occur in up to 21% of children (
In psychotherapy, the perception of PUs is both necessary and problematic. On the one hand, in line with habit reversal training, a precise perception of PUs improves the ability to successfully suppress tics (
The capability to perceive bodily signals (‘interoception’) entails several different facets: IAcc is defined as the process of accurately detecting and tracking internal bodily sensations (
Adult individuals suffering from a TD exhibit a lower IAcc in a heartbeat perception tasks whilst reporting a heightened perception of sensory stimuli (interoceptive sensibility) as compared to individuals without tics. However, this lower IAcc is not evident in children but in adults only (
According to a predictive coding account of bodily symptom perception, bodily changes such as heart activity or muscle tension often are weak and imprecise signals. Against this background, a heightened interoceptive sensibility for tic related symptoms may be the result of overly precise interoceptive priors. Specifically, in TDs, an overactive putamen and insula may lead to overly precise predictions at hierarchically higher levels, overriding the actual weak and imprecise sensory inputs. The resulting prediction error may be reduced by performing an ‚involuntary’ tic and/or be the basis for the perception of an unpleasant PU (
On the behavioral level, PUs may represent a conditioned response to aversive external stimuli such as criticism, offenses or social marginalization as result of tic execution. In the course of a TD, tics may become associated with those negative emotional valences that subsequently constitute the PU. After a tic is executed, the unpleasant PU dissolves and ticking is negatively reinforced, promoting maintenance of tics (
Thus, in this study we wanted to test the hypotheses, that children and adolescents with pathological tics exhibit lower IAcc with regard to both heart activity as well as facial muscle tone as compared to children and adolescents without tics. We also test the hypotheses, that variance in PUs is explained by IAcc scores. Furthermore, we compare muscular to cardiac IAcc, using two different paradigms.
A total of 51 children and youth between 10 and 19 years old were recruited at the University Hospital Cologne (28 patients and 23 control participants) and surrounding schools. One patient fulfilled the criteria of a chronic TD, 27 patients fulfilled the criteria of Tourette’s Syndrome according to ICD-10. Inclusion criteria were a previously diagnosed tic disorder, age 10-21 years and fluency in German. Exclusion criteria were insufficient German language skills and the absence of any tic during the last week. Twenty of these 28 TD patients (71%) were male (13 of 23 HCs, 57%). 7 TD patients were diagnosed with a comorbid disorder via diagnostic checklists (5 ADHD, 1 OCD, 1 conduct disorder, 1 trichotillomania). Two TD patients received anti-tic medication (Aripiprazole, Tiapride), three received medication targeting ADHD (Methylphenidate). TD patients and HCs did not differ with respect to gender (χ2 = 1.229,
A two-group design compared TD patients with control participants not suffering from a TD (HC). TD patients and their parents additionally completed questionnaires regarding tic symptomatology and other psychopathology measures. Participation took between 70 to 90 minutes. The experimental paradigms measuring IAcc were presented via computer screen. Participants received an allowance of 8€ per hour. The current study was carried out according to the Declaration of Helsinki. The Ethics Commission of the University of Cologne’s Faculty of Medicine approved the study (CSHF0044) and the study was pre-registered (see
The German version of the Child Behavior Checklist (CBCL;
The self-rated Symptom Checklist for Tic Disorders SCL-TIC-S (SCL-TIC-S) and SCL-TIC-P (parent-rated) are part of the DISYPS-III diagnostic system (
The Premonitory Urge To Tic Scale (PUTS) consists of 10 items and assesses PUs (
The Mental Tracking paradigm (
Facial EMG was assessed by skin electrodes placed on the masseter and corrugator supercilii on the left side of each participant’s face. EMG placement followed the EMG guidelines by (
The correlation between perceived and via EMG measured muscle tension represent masseter and corrugator IAcc scores, respectively. The heartbeat perception accuracy score (HIAcc) indicated the ability to perceive one’s own heartbeat accurately and was calculated by employing the following formula with i = time intervals (25s, 35s, 45s) and no = measured heartbeats ns = counted heartbeats:
The resulting scores ranged between 0 to 1 with higher scores indicating higher cardiac accuracy. Independent samples two-tailed
When investigating IAcc scores,
Variable | TD patients |
Healthy Controls |
Cohen's |
||||
---|---|---|---|---|---|---|---|
Age | 28 | 12.65 (2.21) | 23 | 12.86 (2.47) | .75 | -0.09 | |
CBCL Total Score | 27 | 32.19 (17.13) | 21 | 11.24 (7.84) | < .001*** | 1.51 | |
YSR Total Score | 26 | 49.96 (18.50) | 23 | 45.26 (10.62) | .29 | 0.31 | |
Interoceptive Accuracy Scores | |||||||
HIAcc | 27 | 0.59 (0.28) | 23 | 0.61 (0.29) | .81 | -0.07 | |
MIAcc | 26 | 0.42 (0.32) | 23 | 0.53 (0.33) | .27 | -0.32 | |
CIAcc | 26 | 0.26 (0.36) | 20 | 0.43 (0.34) | .11 | -0.48 |
***
SCL-TIC-S score was
Variable | 1 | 2 | 3 | 4 | 5 | 6 |
---|---|---|---|---|---|---|
1. PUTS-9 | ||||||
– | .14 | .47 | -.06 | .39 | .24 | |
.50 | .01 | .77 | .05 | .22 | ||
(27) | (26) | (26) | (26) | (27) | ||
2. SCL-TIC-P | ||||||
– | .34 | .06 | .11 | .00 | ||
.08 | .77 | .59 | .99 | |||
(27) | (26) | (25) | (27) | |||
3. SCL-TIC-S | ||||||
– | .12 | .36 | .07 | |||
.57 | .08 | .73 | ||||
(26) | (25) | (27) | ||||
4. CIAcc | ||||||
– | .58** | -.30 | ||||
.00 | .14 | |||||
(25) | (26) | |||||
5. MIAcc | ||||||
– | -.23 | |||||
.27 | ||||||
(25) | ||||||
6. HIAcc | – |
*
In youth, tic symptoms vary substantially with age parallel to PUs, so tic severity should be accounted for when investigating PUs. Multiple regression analysis was used to investigate how IAcc relates to PUs. With PUTS total score as the dependent variable, self-reported tic total score was entered in Step 1 to control for tic severity. HIAcc and CIAcc and MIAcc scores were entered in Step 2. Adding the IAcc scores in Step 2 led only to a marginally significant change in
Predictors | 95% CI |
β | Zero-order correlation | Partial correlation | ||||
---|---|---|---|---|---|---|---|---|
Step 1 | ||||||||
Constant | 13.45 | 9.39 | 17.50 | 1.96 | < .001** | |||
SCL-TIC-S | 0.78 | 0.13 | 1.42 | 0.31 | .46 | .02* | .462 | .462 |
Step 2 | ||||||||
Constant | 9.70 | 4.00 | 15.40 | 2.73 | .002* | |||
SCL-TIC-S | 0.50 | -0.15 | 1.14 | 0.31 | .30 | .12 | .462 | .340 |
HIAcc | 5.14 | -1.51 | 11.79 | 3.19 | .29 | .12 | .279 | .339 |
CIAcc | -4.40 | -10.62 | 1.82 | 2.98 | -.31 | .16 | -.059 | -.313 |
MIAcc | 8.09 | 0.88 | 15.31 | 3.46 | .52 | .03* | .378 | .464 |
*
In the present sample of children and adolescents with and without tics, we found that neither HIAcc nor proprioceptive IAcc scores differed between these groups. These results are in line with recent studies that also did not find any difference in interoceptive accuracy (IAcc) in children with TD (
Within TD patients, recent studies found IAcc to be positively correlated with PUs in adults (
HIAcc score did marginally significantly correlate with the PUTS in our sample of children and adolescents. Children have smaller hearts and a lower stroke volume, associated with a higher heart rate which influences heartbeat detection positively (
In summary, these results on the association between IA and PU provide an ambiguous picture. On the one hand, IA clearly is associated with PU, but the direction of this association remains unclear. Following our hypotheses, we would have assumed that IA should be negatively associated with PU, as was the case for corrugator perception. In contrast, we find a clear positive association between the perception of cardiac activity as well as tension of the masseter and PU. Obviously, more research is needed here.
Note that the findings linking interoception and PUs rely on the PUTS to represent PUs. However, the PUTS is a self-report measure that more likely represents interoceptive sensibility. Interoceptive sensibility is known to be altered in children and adults with TD (
We find it especially intriguing to interpret our findings within the predictive coding framework (
There are a number of limitations to the current study that offer opportunities for future research. Studies investigating the perception of muscle tension in adult TD patients are yet to be conducted to gain further insights on the development of PUs over the life span. Since the current cross-sectional study allows correlative interpretations only, the longitudinal comparison of chronological changes in HIAcc, MIAcc and CIAcc scores, PUTS and urge thermometers over the lifespan would provide further information on their etiological meanings. In addition, the exploratory findings on IA in child and adolescent TD patients need to be replicated, preferably in larger samples. Our study exclusively focused on IAcc in youth with TD. Future studies may extend our findings to interoceptive sensibility to disentangle the influence of interoceptive sensibility and IAcc on the self-reported perception on premonitory urges. Altogether, our sample size was relatively small, compromising statistical power to some degree.
TD patients usually differ from HCs not only with regard to tics but also with regard to comorbidities such as ADHD or OCD, depression or anxiety. When comparing TD patients to typically developing children, our study cannot account for the impact of comorbidities such as ADHD or OCD due to the relatively small sample size. Therefore, the relationship between interoception and tics and PUs in TD patients with multiple comorbid diagnoses is hard to disentangle. Panic and somatic ratings, for example, were found to correlate with higher HIAcc in adults in children (
The PUTS measures PUs as a whole but does not differentiate between context- and time-dependent urges as a state and the PU as a general trait. It is yet to be examined how context- and time-dependent urges, measured by urge thermometers, vary in relation with changes in PUs as a trait and changes in IAcc.
Similar to the PUTS that measures PUs as a general trait, the SCL-TIC-S and SCL-TIC-P measure self- and parent-reported mean tic severity over the course of a week. It is not clear how accurate self-assessed tic frequency reflects actual tic expression. On the one hand, both child and adult patients underestimate their tic expression (
The current study holds clinical implications. Interoceptive trainings specifically targeting interoceptive domains that are impaired in TD may be more beneficial than multisystem interventions (
Christina Schütteler reports no conflict of interest. Katrin Woitecki received royalties from treatment manuals published by Hogrefe. Manfred Döpfner received consulting income and research support from Lilly, Medice, Takeda, and eyelevel GmbH and research support from the German Research Foundation, German Ministry of Education and Research, German Ministry of Health, and Innovation Fund. He received income as head, supervisor, and lecturer of the School of Child and Adolescent Cognitive Behaviour Therapy at the University Hospital Cologne and as consultant for Child Behaviour Therapy at the National Association of Statutory Health Insurance Physicians (Kassenärztliche Bundesvereinigung). He also received royalties from treatment manuals, books and psychological tests published by Beltz, Elsevier, Enke, Guilford, Hogrefe, Huber, Kohlhammer, Schattauer, Springer, Wiley. Alexander L. Gerlach reports no conflict of interest.
For this article, a data set is freely available (
The Supplementary Materials contain the following items (for access see
Pre-registration protocol
Research data
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