Interoceptive Accuracy in Youth with Tic Disorders: Exploring Links with Premonitory Urge, Anxiety and Quality of Life
Journal of Autism and Developmental Disorders
Interoceptive Accuracy in Youth with Tic Disorders: Exploring Links with Premonitory Urge, Anxiety and Quality of Life
Victoria Pile 0 1 2
Jennifer Y. F. Lau 0 1 2
Marta Topor 0 1 2
Tammy Hedderly 0 1 2
Sally Robinson 0 1 2
0 Paediatric Neuropsychology Service, St Georges University Hospitals NHS Foundation Trust, St Georges Hospital , London SW17 0QT , UK
1 Tic and Neurodevelopmental Movements Service (TANDeM), Children's Neurosciences Centre, Evelina London Children's Hospital, Guys and St Thomas' NHS Foundation Trust, St Thomas' Hospital , Westminster Bridge Road, London SE1 7EH , UK
2 King's College London, Department of Psychology, Institute of Psychiatry Psychology and Neuroscience , De Crespigny Park, London SE5 8AF , UK
3 Sally Robinson
Aberrant interoceptive accuracy could contribute to the co-occurrence of anxiety and premonitory urge in chronic tic disorders (CTD). If it can be manipulated through intervention, it would offer a transdiagnostic treatment target for tics and anxiety. Interoceptive accuracy was first assessed consistent with previous protocols and then re-assessed following an instruction attempting to experimentally enhance awareness. The CTD group demonstrated lower interoceptive accuracy than controls but, importantly, this group difference was no longer significant following instruction. In the CTD group, better interoceptive accuracy was associated with higher anxiety and lower quality of life, but not with premonitory urge. Aberrant interoceptive accuracy may represent an underlying trait in CTD that can be manipulated, and relates to anxiety and quality of life.
Tourette syndrome; Anxiety; Heartbeat perception; Interoceptive awareness; Tic disorders
Chronic tic disorders (CTD) are heritable and impairing
neuropsychiatric conditions, typically with onsets in early
(Ganos et al. 2015)
. While tics are considered
the main feature of CTD, the majority of people with CTD
report a premonitory urge (PU), which is an uncomfortable
sensation before tic onset, relieved by expressing the tic.
PU is associated with quality of life
(Crossley and Cavanna
and, compellingly, 71% of adults report they would
not tic if the urge was not present
(Kwak et al. 2003)
the mechanisms underlying PU are poorly understood,
especially in children. Another significant feature of CTD is
(Bitsko et al. 2015)
. As well as being very common
in youth with CTD, anxiety persists even if tics wane and
may moderate the relationship between tic severity and
(Lewin et al. 2011)
. Despite the close and
detrimental relationship between tics and anxiety, research
investigating mechanisms linking them is sparse. One factor
implicated independently in PU and anxiety is interoception.
Khalsa and Lapidus (2016)
define interoception as “the
process of how the brain senses and integrates signals
originating from inside the body, providing a moment by moment
mapping of the body’s internal landscape”. One study has
investigated interoceptive accuracy (IA) in adults with CTD
to explain PU, but no studies have investigated IA in
childhood CTD or used IA to consider why youth with CTD are
at enhanced risk of anxiety. The current study addressees
these limitations by exploring IA and its relationship to PU
and symptoms of anxiety in youth with CTD, with the aim
of informing clinical treatments.
Interoception is multifaceted and includes
information processing that is conscious and non-conscious.
Garfinkel et al. (2015) distinguish interoceptive accuracy
(“performance on objective behavioural tests of heartbeat
detection”) from interoceptive sensibility (“self-evaluated
assessment of subjective interoception”) and
interoceptive awareness (“metacognitive awareness of IA”). Here,
we investigate a general marker of IA to provide insight
into the ability to gauge internal bodily signals accurately.
This is distinguished from the cognitive interpretation (or
indeed catastrophic misinterpretation) of these signals, for
example as indicating an oncoming tic or a heart attack.
Heartbeat detection tasks are frequently used to quantify
individual differences in IA, which is partly pragmatic as
heartbeats are frequent and discrete internal events that are
(Garfinkel et al. 2015)
. The mental
has been extensively used
to measure heartbeat perception (HBP) and is considered
to produce the most consistently replicable results
et al. 2004)
. In this paradigm, participants are asked to
count their heartbeats for a certain period of time, with
the counted number of heartbeats compared to
electrocardiogram (ECG) record to gauge accuracy.
The only study of HBP in CTD has been conducted in
(Ganos et al. 2015)
. They found that heightened
HBP was associated with greater PU, with HBP
identified as a better indicator of PU than tic severity or
obsessive–compulsive symptoms. The authors proposed that
PU represents enhanced (but unhelpful)
IA—interestingly, similar brain regions have been implicated in both
PU and IA
(Craig 2003; Jackson et al. 2011)
. In contrast
to predictions, however, the CTD group had lower HBP
than controls. The authors suggested that participants may
have down-regulated their interoception to manage PU.
Furthermore, Ganos et al. (2015) did not find associations
between HBP and other clinical features, such as anxiety.
This is in contrast to studies in the general population,
where heightened awareness of bodily arousal (alongside
misattributions of what this arousal signifies) is proposed
to contribute to and maintain anxiety across the age range
(Domschke et al. 2010; Dunn et al. 2010; Eley et al. 2007;
Stevens et al. 2011)
To date, no studies have explored HBP in youth with
CTD, but it is plausible that aberrant HBP could contribute
to both difficulties with PU and anxiety. If IA is aberrant in
youth with CTD and associated with anxiety, it could offer a
novel intervention target to address common co-morbidities
in CTD. For IA to be a valid treatment target, it is vital that
it can be experimentally manipulated. Woods et al. (2005)
suggest that a lack of early awareness of PU results in tic
expression, which is consistent with the Ganos et al. (2015)
finding that the CTD group had lower HBP compared to
the control group. Indeed, current psychological
interventions for tics aim to enhance awareness (and tolerance) of
internal sensations to prevent tic expression
(McGuire et al.
2014; Van de Griendt et al. 2013)
. Whilst it is important to
distinguish HBP from PU (as HBP offers a general marker
of IA and not a tic-specific marker), HBP provides a
wellestablished paradigm to investigate whether IA is aberrant
and can be manipulated in youth with CTD. Experimental
attempts to alter IA in the general population have mostly
(e.g. Khalsa et al. 2008; Stevens et al. 2011)
though some recent research has increased HBP using
(Ainley et al. 2012, 2013)
. Yet, no
research has investigated whether IA can be manipulated in
youth with CTD.
The current study sought to extend findings from non-tic
(Domschke et al. 2010; Eley et al. 2007; Stevens
et al. 2011)
and adults with CTD
(Ganos et al. 2015)
exploring IA and its relationship to PU and symptoms of
anxiety in youth with CTD. Depression/dysphoria is
associated with reduced IA and has been suggested as an
explanation for mixed findings
(Dunn et al. 2007; Pollatos et al.
; inattention is commonly reported for individuals with
CTD (Bloch and Leckman 2009) and likely to impact on
performance. Therefore, controlling for these symptoms is
important. Finally, reduced quality of life has been
associated increased anxiety and PU
(Conelea et al. 2011; Crossley
and Cavanna 2013; Eapen et al. 2016; Hesapçıoğlu et al.
. As such, identifying whether HBP relates to
quality of life in youth with CTD is of interest, especially if
interoceptive awareness is to be considered as a possible
transdiagnostic treatment target.
Here we used the experimental task described above
(HBP) to investigate IA under two conditions (1) HBP
Baseline and (2) HBP Manipulation. The first condition followed
(Eley et al. 2004; Ganos et al. 2015)
whilst in the second condition participants were instructed
not to move whilst counting their heatbeats. The aim of this
was to artificially enhance self-awareness and mirror
situations where youth with CTD are asked to suppress tics.
We anticipated that this would result in youth with CTD
exhibiting fewer movements in condition 2 than condition
1. To ensure group differences in HBP were not the result
of co-morbidities; we controlled for anxiety, depression and
inattention, and explored the relationship between these
clinical variables and IA. In line with the adult literature,
we predicted that (1) HBP at baseline would be lower in
youth with CTD relative to matched typically developing
controls, and (2) HBP would increase between the HBP
Baseline and HBP Manipulation conditions for youth with
CTD, but not controls. The HBP Baseline condition was also
used to investigate whether enhanced HBP was associated
with increased PU, elevated levels of anxiety or poorer
ticrelated quality of life for youth with CTD.
Fifty-seven participants completed the study. Three
participants were excluded due to equipment failure (n = 1),
not understanding instructions (n = 1) and being a control
Means and standard deviations reported are prior to transformation to enable ease of interpretation
participant with significant tics (n= 1). This resulted in 29
participants with CTD (14 female; age: x̄ = 11.27, SD = 1.68)
and 25 controls (12 female; age: x̄ = 11.17, SD = 2.46). In the
CTD group, 24 participants had a diagnosis of Tourette
syndrome and five a diagnosis of another CTD. Eight
participants in the CTD group had additional diagnoses, including
autism spectrum disorder (n = 3); attention deficit
hyperactivity disorder (ADHD) (n = 5); obsessive compulsive
disorder only (n = 3). These figures include two participants who
had diagnoses of both ADHD and ASD and one participant
diagnosed with ASD, ADHD and OCD. In terms of
medication at the time of completing the study, four participants
were prescribed clonidine and two prescribed aripiprazole.
IQ and demographic factors were recorded in order to match
the two groups. IQ was assessed using the two-subtest
version (Vocabulary and Matrix Reasoning) of the Wechsler
Abbreviated Scale of Intelligence—Second UK Edition
(WASI-IIUK; Wechsler 2011)
. There was no significant
difference between groups for gender, age, ethnicity, IQ and
socio-economic status (Table 1).
Participants were recruited via advertisements on
Tourette’s Action volunteer webpage, King’s College London
volunteer webpage, the Tics and Neurodevelopmental
Movements Service (TANDeM) at Evelina London Children’s
Hospital and schools in London. The Psychiatry, Nursing
and Midwifery Research Ethics Committee at King’s
College London and from the National Research Ethic Service
Committee South Central-Oxford C gave ethical approval.
The study was completed in accordance with the Declaration
of Helsinki (7th revision, 2013). All participants and their
parents provided informed consent.
Exclusion criteria included being outside of the age range
8–19; not being able to understand and complete the consent
form and measures; and participants with any other
diagnosed neurological condition or diagnosed learning
disability. A diagnosis of CTD or TS was necessary for inclusion
in the CTD group. For the control group, participants were
excluded if they had a diagnosis of CTD or displayed
significant tics. In an initial interview with the first author of
the study (who is a trained clinician), parents were asked
brief screening questions to list any medical (including
psychiatric and neurological) diagnoses that the young
person had received. Due to the well-established high rates of
co-morbidity in CTD, participants with comorbid
neurodevelopmental (providing that they were able to understand
the consent process and measures) or psychiatric diagnoses
were not excluded. A formal diagnostic assessment was not
conducted due to time constraints.
Yale Global Tic Severity Scale (YGTSS)
(Leckman et al. 1989)
assesses tic 1severity and
is administered as a clinical interview with the young person
and their parent. The YGTSS has good internal consistency
and inter-rater reliability, as well as good convergent,
divergent and discriminant validity
(Leckman et al. 2006)
. In the
current study an experienced clinician (Removed for Blind
Review, clinical psychologist) rated the YGTSS, with a
subsample (n = 14) co-rated by trained undergraduate students
demonstrating good inter-rater reliability (94% agreement).
Premonitory Urge for Tics Scale (PUTS)
(Woods et al. 2005)
is a nine-item self-report
questionnaire assessing premonitory experiences prior to tic
onset. The PUTS demonstrates good internal consistency and
test–retest reliability, as well as good construct and concurrent
(Reese et al. 2014; Woods et al. 2005)
. In the present
study, internal consistency was good (Cronbach’s alpha=0.82).
Gilles de la Tourette Quality of Life scale (GTS‑QoL)
(Cavanna et al. 2008)
is a 27-item disease
specific self-report questionnaire measuring quality of life.
Good internal consistency, test–retest reliability and
convergent validity have been demonstrated
(Cavanna et al. 2008)
1 Tic-specific measures were administered to participants with CTD
Internal consistency was excellent (Cronbach’s alpha = 0.91)
in this study.
Measures of Clinical Co‑morbidities
Revised Child Anxiety and Depression Scale (RCADS)
(Chorpita et al. 2005)
is a 47 item self-report
questionnaire measuring anxiety and depression. Summed
scores are converted into standardised T-scores for the
young person’s age. The RCADS demonstrates high internal
consistency and convergent validity
(Chorpita et al. 2005;
Ebesutani et al. 2011)
. In the current study, the internal
consistency for the anxiety scale was excellent (Cronbach’s
alpha = 0.92), but questionable for the depression scale
(Cronbach’s alpha = 0.63).
Inattention Subscale of the Swanson, Nolan, and Pelham,
Version IV Rating Scale (SNAP‑IV)
is a reliable and valid
measure of ADHD symptoms that has three subscales:
inattention, hyperactivity and opposition defiance
(Bussing et al.
2008; Swanson et al. 2001)
. The internal consistency for the
inattention subscale was excellent in this study (Cronbach’s
alpha = 0.93).
Heartbeat Counting Task
This is a standard Mental Tracking Paradigm designed to
. Participants were asked to
count their heartbeats (counted heartbeats) during two
conditions (HBP Baseline and HBP Manipulation) of three
separate trials (35, 25 and 45 s). Condition 1 (HBP Baseline)
participants were given standard instructions that were
consistent with previous research
(“count all the heartbeats you
feel in your body”; Dunn et al. 2007; Eley et al. 2004;
Garfinkel et al. 2015)
. Condition 2 (HBP Manipulation)
participants were instructed to inhibit their movements and count
their heartbeats (“Now what I would like you to do, is to do
your best not to move your body at all whilst you count your
heartbeats”). In both conditions, participants were asked not
to use any pulse-taking methods or employ strategies such
as holding their breath. Movement frequency was monitored
by the researchers as a manipulation check, which was
measured using a count of the number of movements the young
person made during the trials, including tics. To ensure that
condition 1 was consistent with previous protocols, all trials
for condition 1 preceded condition 2. There was a 20-s break
in between each trial and a two-minute break between each
condition. Apart from the instruction, there were no
differences between condition 1 and condition 2.
The actual number of heartbeats was recorded with Polar
RCS800CX. Polar Pro Trainer 5 software was used to
analyse the data. Accuracy for each condition was calculated
1 − ( actual heartbeats − counted heartbeats ∕
Researchers met participants individually to complete the
testing session. Tasks were administered in a set order, with the
researcher present throughout. First participants completed the
WASI-IIUK, then the questionnaire measures, next the HBP
task and finally the YGTSS as part of a larger experimental
battery, which included two other experimental cognitive tasks
(unrelated to the present study). Participants were reimbursed
for their time (£15) and any travel expenses they incurred.
Anxiety, depression and inattention scores were compared
across groups. The anxiety data were not normally
distributed and so reciprocal transformations were applied. When
there were significant group differences between these
clinical variables, they were included as covariates in further
analyses. To investigate group effects on HBP in the two
conditions, a mixed-measures ANCOVA with Condition
(HBP Baseline; HBP Manipulation) as the within-subject
variable and group (CTD; control) as the between-subject
variable was performed. As comorbidity and medication use
in the CTD group has the potential to impact on group
differences, we also replicated this analysis excluding participants
(1) with comorbidity and (2) currently taking medication.
Another mixed-measures ANOVA was performed to check
the manipulation, with movement frequency per Condition
as the within-subjects factor and Group as the
between-subjects factor. HBP data was inspected for outliers and data
points (n = 3) more than three standard deviations above the
mean were removed. For data that did not meet distributional
assumptions, bootstrapping2 was used for inference.
To examine the relationships between HBP and PU in
the CTD group, partial correlations were computed, while
2 Bootstrapping is a computer-intensive, non-parametric approach
to statistical inference that provides valid standard errors, confidence
intervals and p values for hypothesis tests. It only assumes that the
sampled data provide a reasonable representation of the population
from which they came and therefore do not have to meet
distributional assumptions (Davison & Hinkley, 2006).
controlling for tic severity. Regression analysis was then
used to investigate the relationship between HBP and
anxiety. To investigate whether this relationship varied by
group, moderation analysis using multiple regression was
performed. Continuous variables were mean-centred and the
product of the two predictor variables (group × HBP) were
entered as an interaction term. Correlation analyses were
used to follow-up any significant findings. Partial
correlations, controlling for tic severity, were then used to
investigate the association between HBP and quality of life in the
Independent t-tests revealed a main effect of Group (CTD,
control) on anxiety and inattention scores but not
depression scores, with the CTD group reporting more
symptoms of each (Table 1). As anxiety and inattention differed
across groups, these variables were included as covariates
in subsequent analyses. Inattention data was missing for one
control participant, excluding them from relevant
analyses. Inattention did not correlate significantly with anxiety
[r(51) = 0.26, p = 0.058] or accuracy scores in Condition 1
[r(51) = − 0.068, p = 0.63] but inattention did significantly
correlate with accuracy in Condition 2 [r(51) = − 0.35,
p = 0.01].
HBP in Youth with CTD versus Typically Developing
The mixed measures ANCOVA for HBP revealed a main
effect of Condition and significant Group-by-Condition
and Inattention-by-Condition interactions (Table 2). The
Group-by-Condition interaction was followed-up using
ANOVAs for each condition separately. [Inattention and
anxiety were included as covariates in this analysis, anxiety
was then removed as it had no significant effect on accuracy
across conditions.] This revealed a significant difference in
accuracy between the groups for condition 1 (HBP
Baseline) only [F(1, 52) = 4.55, p = 0.038, p2= 0.083], where the
CTD group ( x̄ = 0.58; SD = 0.22) were less accurate than
controls ( x̄ = 0.72; SD = 0.22). There was no significant
difference between the groups for Condition 2 [F(1,52) = 0.22,
p = 0.64; CTD group: x̄ = 0.63; SD = 0.20; control group:
x̄ = 0.66; SD = 0.21). [Of note, the same pattern of results
is found when inattention is not included as a covariate.]
The Inattention-by-Condition interaction was followed-up
by calculating difference scores in accuracy across the
conditions. This revealed a significant relationship between
inattention and change in accuracy over the two conditions
(r(51) = − 0.30, p = 0.032), with those reported as being
more inattentive showing smaller increases in accuracy
from condition 1 to 2.
To check the impact of comorbid diagnoses on group
differences, this analysis was rerun excluding participants
with diagnoses of ADHD, OCD and/or ASD, resulting
in 21 participants in the CTD group. The same pattern
of results was observed with main effects of Condition,
F(1,42) = 7.77, p = 0.008, p2 = 0.16, and significant
Groupby-Condition, F(1,42) = 7.09, p = 0.011, p2 = 0.14 and
Inattention-by-Condition interactions, F(1,42) = 5.56, p = 0.023,
p2 = 0.12. The Group-by-Condition interaction was driven
by a significant difference in accuracy between the groups
for condition 1 (F(1, 42) = 5.99, p = 0.019, p2 = 0.12), with
no significant difference between the groups for Condition
2 (F(1,42) = 2.45, p = 0.13). The same pattern of results was
also observed when young people who were currently
taking medication were excluded, leaving a sample of n = 23
in CTD group [main effects of Condition, F(1,44) = 4.85,
p = 0.033, p2= 0.099; significant Group-by-Condition
interaction, F(1,44) = 4.45, p = 0.042, p2= 0.092; significant
Inattention-by-Condition interaction, F(1,44) = 4.15, p = 0.086,
p2= 0.086; significant difference in accuracy between the
groups for condition 1 (F(1,44) = 4.71, p = 0.035, p2= 0.097)
but not Condition 2 (F(1,44) = 0.28, p = 0.60)].
The repeated-measures ANOVA with movement
frequency revealed a main effect of Group and a significant
Group-by-Condition interaction (Table 2). Follow-up
analyses using difference scores in movements revealed larger
increases in movements in the CTD group compared to
controls, t(52) = 4.34, p < 0.01 (CTD: x̄ = 3.17, SD=4.00;
control: x̄ = 0.52, SD = 1.50). A single item measure of tic
suppression (PUTS item 10) was significantly correlated with
increased movements, r(27) = − 0.39, p < 0.05, wherein those
who rated themselves as worse at suppressing tics displayed
Partial correlations (controlling for tic severity) were then
used to investigate the relationship between quality of life
and HBP in condition 1, this revealed a significant positive
relationship [r(26) = 0.39, p = 0.041].
more movements from condition 1 (HBP Baseline) to
condition 2 (HBP Manipulation). Movement frequency in the
control group was very low across conditions (condition 1:
x̄ = 1.16; SD = 1.82; condition 2: x̄ = 0.76; SD = 1.85).
Movement frequency in the CTD group was also fairly low in
condition 1 ( x̄ = 0.1.93; SD = 2.43) and rose considerably in
condition 2 ( x̄ = 0.5.10; SD = 4.56).
Clinical Features and HBP in Youth with CTD
HBP in condition 1 (HBP Baseline) did not significantly
correlate with PU when tic severity was controlled for
[r(26) = 0.11, p = 0.56]. Regression analysis with anxiety as
the dependent variable and Group, HBP Baseline,
depression and inattention as predictor variables was significant
[F(4,52) = 12.20, p < 0.001, R2 = 0.50], but indicated that
there was no main effect of HBP on anxiety across groups
and only depression significantly predicted anxiety score
(Table 3). Moderation analysis, including depression as a
covariate, revealed a significant interaction between Group
and HBP (F(4,53) = 13.65, p < 0.001, R2 = 0.53 ∆R2 = 0.038;
see Table 3 for full analysis; inattention was controlled for
initially and then removed as it was non-significant in
previous analysis). Follow-up analysis revealed HBP significantly
correlated with anxiety in the CTD group, r(27) = 0.40,
p = 0.032 but not the control group, r(23) = − 0.13, p = 0.54.
Theoretical interest in altered IA in both CTD
(Ganos et al.
and anxiety disorders
(e.g. Domschke et al. 2010)
has been growing independently. This is the first study
to connect the two fields and investigate HBP as a
common factor for anxiety and PU in youth with CTD. This
study has three main sets of findings relating to, (1) HBP
when measured traditionally, (2) experimental
manipulation of HBP using an instruction to inhibit movements
and (3) the relationship between HBP and clinical features
of youth with CTD. Consistent with predictions, youth
with CTD had reduced IA compared to controls when
measured traditionally (even when participants with
comorbidity/medication use were excluded). In response to
the experimental manipulation, IA increased so that the
groups were no longer significantly different. Finally, in
the CTD group, increased HBP was associated with more
anxiety symptoms and reduced quality of life (but not PU,
depression or inattention).
Our finding that youth with CTD had lower HBP
compared to controls (even when comorbidities were
controlled for) replicates and extends previous findings in
adults with CTD
(Ganos et al. 2015)
. Reduced IA may
therefore reflect an underlying trait in CTD, although it is
unclear whether this trait precedes tic onset or arises as a
compensatory mechanism to help the person manage the
tics. In contrast to the adult study, we did not replicate the
finding that HBP was associated with PU, which suggests
that the internal perception of sensory phenomena differs
across the age span for people with CTD. This may reflect
age-associated changes in PU, as research indicates that
awareness of PU increases with age
. However, whether this age related
change reflects a stronger PU, increased IA or a
combination of these and other factors is unclear. Performance on
a more PU-specific measure of IA, such as muscle
tension, and multiple measures of PU
administered; McGuire et al. 2016)
would further understanding of
whether there is a reliable age-related relationship between
Previous attempts to experimentally alter HBP in the
general population have been mixed
(Ainley et al. 2012,
2013; Fairclough and Goodwin 2007; Stevens et al. 2011)
and this is the first study to demonstrate that it is possible
to experimentally manipulate HBP in youth with CTD.
Psychological therapies for tic disorders assume that it
is possible to modify an individual’s internal awareness
(Van de Griendt et al. 2013). Thus, our finding that HBP
was lower in the CTD group and that accuracy increased
with the instruction to inhibit movement, supports this
premise, as well as the notion that IA can be influenced
by state factors
(Ainley et al. 2012)
. Interestingly, but
perhaps unsurprisingly, youth with higher levels of
inattention exhibited smaller increases in IA and inattention
correlated with IA in the second condition. This is
consistent with research identifying that comorbid ADHD
reduces treatment response to behavioural therapy for tics
(McGuire et al. 2014)
and reinforces the need to consider
an individual’s level of cognitive control and attentional
processing style when delivering tic treatments. The
increase in movements for youth with CTD in response
to the instruction to ‘inhibit’ movements is also of
interest as it highlights how direct instruction to inhibit can
actually exacerbate movements. It is speculated that this
may have arisen due to increased allocation of attention to
movement and accompanying tic-related cognitions, which
previous research has shown can increase tic frequency
(Brandt et al. 2014; Misirlisoy et al. 2015; O’Connor et al.
. Exploration of cognitive aspects of interoception
(i.e. interoceptive sensibility and awareness) would be of
interest to help elucidate the relationship between
movements, internal bodily sensations and tic-related cognitions
for individuals with CTD.
In relation to clinical features, increased HBP was
associated with increased anxiety symptoms and reduced quality
of life for youth with CTD.3 Aberrant HBP is implicated in
the development and maintenance of anxiety during typical
development and this current finding is consistent with that
(Eley et al. 2004, 2007)
. The association between
HBP and quality of life suggests that for youth with CTD
increased awareness of internal bodily sensations is related
to a general reduction in well-being and satisfaction with
life. Given that enhanced HBP is associated with anxiety and
that youth with CTD are at an increased risk of developing
anxiety and lower quality of life, the finding that those with
CTD exhibited lower levels of IA than controls is perhaps
unexpected (albeit consistent with adults with CTD). These
results require replication but highlight the importance of
considering co-morbidities in research on tics and in the
treatment of youth with CTD, with IA offering a potential
transdiagnostic treatment target.
Habit Reversal Therapy (HRT), a leading evidence-based
psychological therapy for tic disorders, emphasises the need
to increase awareness of internal sensations to learn when
tics are likely to occur
(Van de Griendt et al. 2013)
3 Quality of life was only assessed in the CTD group as we used a tic
current findings suggest a secondary outcome for tic-related
therapies could be to learn that these internal sensations are
not threatening (i.e. they no longer signal tic onset), similar
to cognitive models for anxiety disorders. Perhaps an
important difference between HRT and cognitive therapy for
anxiety disorders is that whilst HRT aims (in part) to enhance
internal awareness, cognitive therapy for anxiety can include
training to shift attentional focus from internal sensations
to the external environment. Cognitive behavioural and
metacognitive techniques that encourage attentional control
and flexible attentional shifting could be a useful addition
to current therapies for tic disorders
. Importantly, what our data cannot determine
is whether an underlying interoceptive ability has the same
relationship with anxiety as taught awareness (such as in
psychological therapies); it would be informative for future
research to track changes in IA during treatment.
This current study had limitations. Firstly, the data are
cross-sectional and so causal effects cannot be determined,
with a need for longitudinal studies to understand the
direction of the links between HBP and anxiety, as well as
whether HBP does change with therapy. Secondly, we did
not replicate findings linking HBP and PU. This is likely to
be due to age differences, as such studies that use multiple
age groups and larger samples would be helpful. Thirdly,
the sample did not have diagnoses of anxiety disorders, so,
to disentangle the relationships between HBP, anxiety and
CTD, it may be valuable to compare a sample of youth with
CTD and an anxiety disorder to with those with CTD
without anxiety disorders, and those with anxiety disorders
without CTD. Adding to this, some research suggests that OCD
presents differently in youth with Tourette syndrome,
compared to those with chronic motor or vocal tic only
et al. 2006)
, so it may also be important to distinguish these
groups when investigating relationships with anxiety.
There are also several limitations in terms of our sample,
including the small sample size, diagnostic comorbidity and
use of medication. Given that both comorbidity and
medication use is high in the CTD population
(Kumar et al. 2016)
it did not seem representative to exclude participants with
comorbidity or medication use. Although both could impact
on task performance (for example difficulties with attention),
group differences in HBP remained when participants with
comorbidity/medication use were excluded and inattention
was controlled for in principal analyses. Future studies with
larger sample sizes (enabling detailed subgroup analysis)
would permit a more thorough investigation of the impact
that comorbidities and medication could have on
interceptive accuracy. It would also be valuable for future studies
to investigate the role of attention processes on IA in
children with CTD. Furthermore, it is possible that there are
differences between those participants who overestimate and
underestimate their heart rate, and that the relationships vary
within these groups with anxiety and PU. Larger samples
that could evaluate relationships within subgroups would
be helpful to establish whether these findings are consistent
across performance or specific to those that underestimate or
overestimate their heart rate. Finally, although our analysis
was hypothesis driven, we did conduct multiple analyses
and did not include statistical corrections for multiple
testing. However, a two-tailed level of significance was used
throughout, due to the exploratory nature of this study.
In summary, despite the limitations of the study, these
data demonstrate a relationship between enhanced HBP and
anxiety and lower quality of life in youth with CTD. They
indicate that, like adults, HBP is reduced in youth with CTD
compared to controls, with the novel finding that HBP can
be experimentally enhanced in this group. These results
highlight important questions for treatment development for
youth with CTD and comorbid anxiety, with interoception
offering a novel treatment target.
Acknowledgments We would like to thank all the families that
participated in this research study as well as Tourettes Action and the
schools for all their help. This study represents independent research
supported by the National Institute for Health Research (NIHR)
Biomedical Research Centre at Guy’s and St Thomas’ NHS Foundation
trust and King’s College London, and the National Institute for Health
Research (NIHR) Biomedical Research Centre at the South London
and Maudsley NHS Foundation Trust and King’s College London
and from a Clinical Doctoral Research Fellowship (Dr Victoria Pile,
ICA-CDRF-2015-01-007) supported by the National Institute for
Health Research and Health Education England. The views expressed
in this publication are those of the authors and not necessarily those
of the NHS, NIHR, Health Education England or the Department of
Health and Social Care.
Author Contributions VP, SR, JYL & TH conceived the study and
participated in the design and co-ordination of the study. VP & MT
were responsible for data collection and data entry. All authors read,
contributed to and approved the final manuscript.
Compliance with Ethical Standards
Conflict of interest The authors declare that they have no conflict of
Open Access This article is distributed under the terms of the
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mmons.org/licenses/by/4.0/), which permits unrestricted use,
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credit to the original author(s) and the source, provide a link to the
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