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Keywords Abstract
Cardiac perception, decision making,
interoception, Iowa Gambling Task, panic Objective: Somatic marker theory predicts that somatic cues serve intuitive
disorder, somatic marker hypothesis decision making; however, cardiovascular symptoms are threat cues for patients
with panic disorder (PD). Therefore, enhanced cardiac perception may aid
Correspondence intuitive decision making only in healthy individuals, but impair intuitive deci-
Stefan M. Schulz, Department of Psychology sion making in PD patients. Methods: PD patients and age- and sex-matched
I, University of Würzburg, Würzburg,
volunteers without a psychiatric diagnosis (n = 17, respectively) completed the
97070 Germany.
Iowa Gambling Task (IGT) as a measure of intuitive decision making. Interin-
Tel: +49 931 31 80184; Fax: +49 931 31
82733; dividual differences in cardiac perception were assessed with a common men-
E-mail: [email protected] tal-tracking task. Results: In line with our hypothesis, we found a pattern of
opposing associations (Fisher’s Z = 1.78, P = 0.04) of high cardiac perception
Funding Information with improved IGT-performance in matched control-participants (r = 0.36,
Preparation of this manuscript was supported n = 14) but impaired IGT-performance in PD patients (r = 0.38, n = 13).
by the Federal Ministry of Education and
Conclusion: Interoceptive skills, typically assumed to aid intuitive decision
Research, BMBF, project 01EO1004 (S. M. S.,
making, can have the opposite effect in PD patients who experience interocep-
Comprehensive Heart Failure Center [CHFC],
University of Würzburg, Germany). tive cues as threatening, and tend to avoid them. This may explain why PD
patients frequently have problems with decision making in everyday life.
Received: 16 May 2013; Revised: 25 Screening of cardiac perception may help identifying patients who benefit from
November 2013; Accepted: 28 November specifically tailored interventions.
2013
doi: 10.1002/brb3.206
ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. This is an open access article under the terms of 1
the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
Cardiac Perception and Decision Making J. Wölk et al.
(Bechara et al. 1997). The main body of literature has previous studies (Domschke et al. 2010; Grosche et al.
considered skin conductance response as a proxy for vis- 2011), we expected to find enhanced cardiac perception
ceral somatic markers (Dunn et al. 2006), although the in PD patients as compared to matched controls without
SMH suggests that cardiac cues may play a similar role. psychiatric diagnosis. In control participants we further
In line with this assumption, interindividual differences in hypothesized cardioceptive perception accuracy to be pos-
trait cardiac perception accuracy have been found to itively associated with performance in intuitive decision
affect emotional bias on speeded reactions in healthy vol- making. In PD patients, we expected to find the opposite
unteers (Sütterlin et al. 2013). Moreover, at least one pattern of results, that is high cardioceptive accuracy to
study has demonstrated that healthy participants with impair intuitive decision making due to PD patients’ cat-
particularly high cardiac perception outperform those astrophic interpretation of such cues.
with lower accuracy in the IGT (Werner et al. 2009).
The perception and cognitive evaluation of physical
symptoms is considered to play a crucial role in the Methods
development and maintenance of panic disorder (PD).
The psychophysiological model of PD (Ehlers and Marg- Sample
raf 1989) describes a vicious circle of perception of physi- The patient sample consisted of 17 inpatients (eight
cal cues and their catastrophizing evaluation, which female patients; M = 41.59 years, SD = 13.30), admitted
increases the probability of panic attacks. While healthy to a psychosomatic hospital (Schön Klinik Roseneck,
individuals attribute the experience of physical changes Hospital of Behavioral Medicine, Prien, Germany). All
(e.g., beating heart, shortness of breath, etc.) to a variety patients had a principal diagnosis of PD as assessed by
of internal or external stressors, patients with PD habitu- trained clinical psychologists. Diagnoses were based on
ally associate such sensations with imminent threat (Clark DSM-IV-TR criteria (American Psychiatric Association
et al. 1988; Hofmann et al. 2008). 2000), and verified by J. W., based on the PD-related
Increased sensitivity to physical cues (Barsky 1992; parts of the SKID-I (Wittchen et al. 1997). The control
Ehlers and Breuer 1996; Eley et al. 2004; Hoehn-Saric group comprised of 17 volunteers (eight female volun-
et al. 2004) and their catastrophizing appraisal are typical teers; M = 36.53 years; SD = 12.10) without mental dis-
features of PD and are often principal targets for PD orders, matched for gender and age. As indicated by self-
treatment (Hofmann et al. 2008). A large body of disclosure, none of the control participants had a psychi-
research further supports the role of biased perception atric diagnosis or any cardiac and/or neurological disor-
and interpretation of physical symptoms in the develop- der and, therefore, no related medication. Moreover,
ment (Bouton et al. 2001) and maintenance of PD (Ehlers none of the participants had taken benzodiazepines within
1993; Richards et al. 2003). There is evidence for 2 weeks prior to the experimental assessment. Patients
increased perception of physical symptoms in PD patients with an additional diagnosis of somatoform disorder were
(Domschke et al. 2010). Physical symptom perception is excluded, due to the suggested role of abnormal percep-
often part of PD patients’ reported symptomatology tion of physical symptoms in this diagnostic category.
(Zoellner and Craske 1999) with cardiac symptoms such Nevertheless, those meeting criteria for secondary anxiety
as heart rate playing a prominent role (Hartl 1995). disorders (social phobia n = 1, 11.76%), generalized anxi-
In addition to increased symptom perception and its ety disorder (n = 1, 5.88%), or major depression (n = 16,
biased attribution to impending threat, there is also 94.10%) were included, thus representing a typical sample
evidence for intolerance of uncertainty in patients with of PD patients in clinical practice (Kaufmann and Char-
PD (Carleton et al. 2012; Mahoney and McEvoy 2012), ney 2000; Brown et al. 2001).
reduced risk-taking behavior (Giorgetta et al. 2012),
increased latency in speeded decision making (Kaplan
et al. 2006) and heightened sensitivity to errors (Ludewig Materials
et al. 2003). Yet, whether increased perception of physical Equipment
cues would impact upon intuitive decision making in PD
patients remains unclear. Given PD patients’ habitual ECG was recorded with the NeXus-10 system (Mind
catastrophizing interpretation of physical cues, it could be Media BV/Roermond-Herten, Netherlands) using Eintho-
argued that increased interoceptive awareness is detrimen- ven lead I configuration with Ambu Blue Sensor VL
tal for intuitive decision making in patients with PD. (Ambu GmbH/Bad Nauheim/Germany) electrodes. Data
The aim of this study was to examine the effects of were sampled at 512 Hz. A freeware IGT application was
increased perception and processing of somatic markers run on a personal computer (ASUS, Taipeh, Taiwan)
on decision-making processes in PD patients. In line with with Windows XP operating system and presented on a
2 ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
J. Wölk et al. Cardiac Perception and Decision Making
Each time a card is drawn from one of the decks, the associated gain is won but counterbalanced by a potential loss that is selected at random
from the respective batch of losses. The net amount per draw results from subtracting the loss from the gain. Furthermore, achieving a positive
net gain only occurs at a certain probability.
15-inch LCD-monitor at 1024 9 768 pixel screen resolu- fixed order. Instructions were given in written form to
tion with ~40 cm head-to-screen distance. standardize the instruction (Ehlers et al. 1995). We added
an initial warm-up trial to allow sufficient time for the
transition from the instructional phase to the different
Iowa Gambling Task
mode of processing during interoception. The warm-up
The IGT consists of four decks of cards (A, B, C, D). trial was not included in the analysis, as we aimed for an
Drawing cards from deck A or B results in large gains but optimal compromise between keeping the scores compa-
high losses, leading to an overall loss. In comparison, rable with previous reports as much as possible and the
drawing cards from decks C and D results in small gains added benefit of reducing task-irrelevant training effects
but similarly small losses and an overall net profit (see in a situation unfamiliar for most participants (Sütterlin
Table 1 for details). Participants are instructed to draw et al. 2013).1
100 cards from these decks, with the aim to maximize
their profit. Typically, control participants begin by select-
Self-report data
ing cards more or less randomly, followed by a period of
implicit learning with a preference for the net gain option The German version of the State–Trait Anxiety Inventory
and finally explicit knowledge resulting in a clear prefer- (Laux et al. 1981) was used to assess habitual trait and
ence for decks C and D. state anxiety on two scales comprising 20 items each.
Items are rated from 0 (not at all) to 3 (very much so),
resulting in a scale range of 0–60 for each measure.
Mental-tracking task
Higher scores indicate higher anxiety. Cronbach’s a is
Following Herbert et al. (2012), the participants were about 0.90 for both scales (Laux et al. 1981). The current
instructed to quietly count the heartbeats, which they sample achieved a Cronbach’s a of 0.92 for the STAI-
experienced in the time interval between a start and a State and 0.96 for the STAI-Trait.
stop signal without any supplementary aids such as taking The German 21-item version of the Beck Depression
their pulse or estimating the expected number of heart- Inventory (BDI) was used to assess dysphoric mood and
beats based on the (estimated) elapsed time. This task depression. Items are rated on a four-point scale from 0
was performed for four time intervals with 20, 25, 35, to 3, resulting in an overall score ranging from 0 to 63.
and 45-sec duration and a 60-sec rest time between the Higher scores represent more severe symptoms of depres-
time intervals. During this procedure, participants were sion. Internal consistency is good with Cronbach’s
asked to close their eyes, to sit relaxed, and to breathe a = 0.89 (Hautzinger et al. 2006).
consistently. Start and stop of each interval was indicated Trait anxiety sensitivity was assessed with the German
verbally by the experimenter. Particularly in small sam- version of the Anxiety Sensitivity Index (ASI, Peterson
ples, randomization often does not produce comparable and Plehn 1999). Notably, high scores on the ASI have
distributions of conditions across groups. Hence, the
order of time intervals was not randomized, to increase
procedural comparability between the two groups. Impor- 1
It may be noted that including these data in the analysis did
tantly, the individual participants were not aware of the not affect the results.
ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 3
Cardiac Perception and Decision Making J. Wölk et al.
4 ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
J. Wölk et al. Cardiac Perception and Decision Making
Table 2. Means (M), standard deviations (SD), or frequencies (n) and percent (%) significance level (P) and effect size (Cohen’s d, calculated on
basis of control group’s standard deviation) of group characteristics for patients with panic disorder (PD) versus matched controls.
BMI, body mass index (kg/m2); STAI, state trait anxiety inventory; ASI, anxiety sensitivity index; Hauptschule, Realschule, and (Fach-)Abitur can be
considered different levels of high school degrees (in ascending order).
1
In parentheses: international standard classification of education (ISCE) according to the UNESCO guidelines from 2011. *P < 0.05,
***P < 0.001.
ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 5
Cardiac Perception and Decision Making J. Wölk et al.
6 ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
J. Wölk et al. Cardiac Perception and Decision Making
generalization and maintenance of PD. In complex deci- due to error variance. Future studies should therefore pay
sion-making tasks this may have detrimental effects, when particular attention to such moderating factors. Third, it
attention to associated information is withdrawn due to has been suggested that the mental-tracking task may
generalized avoidance of somatic cues as described in the reflect cognitive ability rather than interoceptive skill.
SMH. Although the present task was designed to prevent the
Future studies should examine real-life decision making respective strategy of estimating the time passed during
in PD patients based on such models. This could well counting of heartbeats, we cannot completely rule out
lead to better explanations why PD patients’ history is that cognitive ability is confounded with cardiac percep-
often characterized by decision difficulties (Ludewig et al. tion scores. Nevertheless, the reverse association of high-
2003; Lorian and Mahoney 2012). cardiac perception and decision-making performance
Although the group difference was not significant, con- found in panic patients would still be at odds with this
trols exercised about twice as long per week as panic alternative explanation. Moreover, it appears quite hard
patients. Although cardiac perception was similar in both to find a plausible explanation why high-cognitive skill
groups and the correlations with decision making were may predict impaired decision making. Hence, we con-
not stronger in the control group, this indicates that sider our interpretation as the more parsimonious one.
panic patients may be less familiar with experiencing car- Fourth, the small sample size limits the generalizability of
diac symptoms in a safe context. In patients with high our results, therefore, warranting future replications in
cardiac perception, this may further add to the presumed larger samples. An independent replication of these results
detrimental effect of experiencing cardiac somatic cues on with a larger sample size and consequently more hetero-
decision making. From a clinical point of view, it may geneous sample (e.g., including typical comorbidities)
therefore be interesting to address such a potential associ- could increase the generalizability of our conclusions.
ation of (cardiac) somatic cues with panic-related (nega- Nevertheless, several observations support the reliability
tive) associations. Symptom-focused exposure (e.g., of the current results. First, the correlations are similar to
elicited by physiological provocation tasks and discrimi- previously published results on interoceptive accuracy and
nation learning) could help to weaken these associations. anxiety (Pollatos et al. 2007; Domschke et al. 2010) or
Once cardiac symptoms are not experienced as threaten- those achieved with a similar task (Sütterlin et al. 2013).
ing anymore, this may also withdraw the basis for the Second, the sample was homogeneous and carefully
side effects of (cardiac) somatic markers on decision mak- selected to minimize effects of comorbidity and medica-
ing as delineated above. Screening for cardiac perception tion, and third the results do not depend on outliers, sin-
may help identify patients who may profit from such an gle participants or small groups of individuals (see
approach. Figs. 2, 3). Fifth, the test situation in the laboratory may
have induced moderate stress in all participants. This may
have induced particular attention to or salience of cardiac
Limitations
cues in some PD patients. On the other hand, a similarly
First, it should be noted, that almost no patient reached stressful context is present in many real-life situations
the stage of explicitly understanding the effects of select- requiring decision making, hence, this could also be seen
ing a particular deck in the IGT. Therefore, our findings as a factor increasing the ecological validity of this study,
only apply to the stage where participants decide ran- improving generalizability of these findings to real-life
domly or rely on a hunch. However, it is clear from situations.
somatic marker theory that this is the stage where cardio-
ception would be considered to have the largest impact
Conclusion
on behavior. Second, we did not find a main effect of
group. This is at odds with previous studies suggesting This is the first study to demonstrate a detrimental effect
that PD patients may generally have higher cardiac per- of enhanced cardiac perception on intuitive decision mak-
ception (for a review see, Domschke et al. 2010). How- ing in PD patients. These findings extend previous results
ever, not all previous studies have found this difference, indicating that PD patient experience heightened aware-
and the small to medium effect size in our study could ness and dysfunctional cognitive processing of somatosen-
become significant in a larger sample. Comparing these sory cues, particularly cardiac activity (Hofmann et al.
studies, it is interesting that both participants recruited 2008) and associated bias (Amrhein et al. 2005). Together
from inpatient versus outpatient settings occur. Maybe with cognitive models comprising of a vicious circle
differences in symptom severity, comorbidity, treatment involving vigilance-anxiety-avoidance (Clark et al. 1988),
intensity, time since diagnosis, etc. contribute to a larger our findings provide new insight into the basis for detri-
heterogeneity in our patient group, reducing effect size mental decision making in PD patients.
ª 2013 The Authors. Brain and Behavior published by Wiley Periodicals, Inc. 7
Cardiac Perception and Decision Making J. Wölk et al.
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