J Behav Med DOI 10.1007/s10865-014-9564-7

The impact of cardiac perception on emotion experience and cognitive performance under mental stress Nicole K. Kindermann • Natalie S. Werner

Received: May 29, 2013 / Accepted: March 21, 2014 Ó Springer Science+Business Media New York 2014

Abstract Mental stress evokes several physiological responses such as the acceleration of heart rate, increase of electrodermal activity and the release of adrenaline. Moreover, physiological stress responses interact with emotional and behavioral stress responses. In the present study we provide evidence that viscero-sensory feedback from the heart (cardiac perception) is an important factor modulating emotional and cognitive stress responses. In our study, we compared participants with high versus low cardiac perception using a computerized mental stress task, in which they had to respond to rapidly presented visual and acoustic stimuli. Additionally, we assessed physiological responses (heart rate, skin conductance). Participants high in cardiac perception reported more negative emotions and showed worse task performance under the stressor than participants low in cardiac perception. These results were not moderated by physiological responses. We conclude that cardiac perception modulates stress responses by intensifying negative emotions and by impairing cognitive performance. Keywords Cardiac perception  Interoception  Mental stress  Emotion  Cognitive performance

Introduction ‘‘Faster, higher, further’’ is the slogan of the modern achievement-oriented society. There are however heavy costs that come with the benefits of such a mentality for N. K. Kindermann (&)  N. S. Werner Department Psychologie, Ludwig-Maximilians-Universitaet, Leopoldstr. 13, 80802 Munich, Germany e-mail: [email protected]

both the individual as well as for society as a whole. The European Agency for Safety and Health at Work reports that up to 40 million Europeans complain about stress at work, which leads to costs of 20 billion Euros in both lost time and health care (EU-OSHA, 2003). Among the costs for the individual, stress is associated with an increased risk for physiological and psychological disorders (Jones & Bright, 2007). In particular the cardiovascular system has become a crucial concern in this context. Chronic life stressors can lead to more cardiovascular reactivity, which over time may lead to the development of arteriosclerosis (Low et al., 2009). In the current study we were interested in the perception of cardiovascular responses as an influencing factor on cognitive and emotional responses under mental stress. The ability to perceive cardiovascular responses is referred to as cardiac perception. A variety of methods for the quantification of cardiac perception have been developed. The two principal types are tracking and discrimination paradigms. In tracking paradigms, participants have to press a button or tap a finger in time with the rhythm of their heart rate (McFarland, 1975) or they are asked to count their heartbeats (Carroll & Whellock, 1980; Dale & Anderson, 1978; Schandry, 1981). In discrimination paradigms, participants have to judge whether a series of externally presented stimuli (e.g. tones) matches their heart rate (Brener, 1974; Brener & Kluvitse, 1988; Katkin et al., 1982; Whitehead et al., 1977). The ability to perceive cardiac signals varies among individuals. Factors such as gender, percentage of body fat and physical fitness are suggested as influences upon cardiac perception (Cameron, 2001; Jones, 1994; Katkin, 1985; Schandry & Bestler, 1995; Vaitl, 1996). Accordingly, on average men perform better in a cardiac perception test (Harver et al., 1994; Katkin et al., 1981), which may be primarily due to their

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lower percentage of body fat (Rouse et al., 1988). Furthermore, physically fit individuals achieve higher scores in cardiac perception tests than unfit individuals (Jones & Hollandsworth, 1981; Montgomery et al., 1984). It is supposed that physical fitness results in an enlargement of the left cardiac ventricle, which in turn leads to an increased stroke volume. An increased stroke volume can result in a stronger cardiac signal and thus a better perception of heartbeats (see Schandry et al., 1993). Some authors also consider increased autonomic reactivity to be related to cardiac perception (Herbert et al., 2010; Pollatos et al., 2007b, c). However, the evidence is inconsistent (Eichler & Katkin, 1994; Hantas et al., 1982; Werner et al., 2009a, b). Critchley et al. (2004) and Pollatos et al. (2007a) identified neural structures associated with cardiac perception: the insula, the somatomotor and anterior cingulate cortex. In particular, better performance in a heartbeat perception task was positively associated with enhanced activity in the right insular cortex (Critchley et al., 2004). To date research on cardiac perception has mainly focused on emotional experience. Psychophysiological theories of emotions have suggested that somatic processes impact upon emotional experience (Bechara & Naqvi, 2004; Cacioppo et al., 1992; Damasio, 1994; James, 1884; Thayer & Lane, 2000). William James (1884) was one of the first who postulated that feedback from the body is closely related to emotional experience. Damasio (1994) extended this approach in his somatic marker hypothesis. According to this theory, situational somatic processes, called ‘somatic markers’, occur depending on the consequences of an event, and evoke certain emotional processes. In similar situations these somatic markers are reactivated and guide emotional and behavioral responses. In accordance with these theories, it has been repeatedly shown that high cardiac perception is related to more intense emotional experience (e.g. Barrett et al., 2004; Hantas et al., 1982; Pollatos et al., 2005, 2007c, Schandry, 1981, 1983; Wiens et al., 2000). Although stress can provoke strong emotional and physiological responses, to date there are only a few studies considering the relationship between cardiac perception and stress. Eichler and Katkin (1994) demonstrated that participants high in cardiac perception compared to participants low in cardiac perception showed greater left ventricular contractility as well as greater shortening of pre-ejection period during a mental arithmetic task. In a study of Herbert et al. (2010), participants high in cardiac perception also showed a greater shortening of pre-ejection period, a greater left ventricular contractility as well as a greater increase in mean heart rate when performing a mental arithmetic test. The authors concluded that high cardiac perception is associated with greater sympathetic reactivity in response to a mental stressor. Two recent studies investigated the emo-

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tional impact of cardiac perception in socially stressful situations. When confronted with a public speaking situation participants high in cardiac perception reported significantly less anxiety as compared to participants low in cardiac perception (Werner et al., 2009a). Likewise when confronted with a social exclusion situation, participants high in cardiac perception showed a smaller increase in negative affect as well as a smaller decrease of positive affect (Werner et al., 2013). On the first view, these two studies seem to contradict previous studies on emotion experience as participants high in cardiac perception reported less intensive negative emotions in the socially stressful situations. We assume however, that everyday situations such as social exclusion or public speaking are probably familiar to the participants and that these situations reactivated somatic markers. Accordingly, individuals high in cardiac perception, who have a better access to somatic markers, were familiar with the physiological arousal evoked and thus were able to deal with the socially stressful situations more effectively. However, in new and unfamiliar situations as in laboratory situations somatic markers are not available and first have to be established. Therefore, individuals with better access to somatic processes may experience more arousal which in turn may intensify emotions as proposed by physiological emotion theories (Damasio, 1994; James, 1884). According to the Competition of Cues Theory of Pennebaker (1982) the elaboration of internal stimuli, such as cardiovascular stimuli, may interfere with the simultaneous elaboration of external stimuli. Thus, Pennebaker postulated that cognitive capacity is limited and that the elaboration of internal stimuli shares the same cognitive resources as the elaboration of external stimuli. For this reason, internal and external stimuli compete for the same limited cognitive resources and interference may occur if attention is bonded by external or internal stimuli. As individuals high in cardiac perception have better access to their cardiovascular signals as compared to individuals low in cardiac perception, these processes might interfere with the elaboration of external stimuli. In order to clarify the relation between cardiac perception and stress responses, we investigated whether and how the perception of cardiac signals affects emotional experience and cognitive functioning under mental stress in the current study. According to the data based on cardiac perception and emotion experience we hypothesized that individuals high in cardiac perception report more negative emotions under mental stress compared to individuals low in cardiac perception. With regard to cognitive performance previous studies have shown enhanced decision making, emotional memory and attention processes in individuals with high cardiac perception (Matthias et al., 2009; Pollatos & Schandry, 2008; Werner et al., 2009c, 2010). As however stress evokes strong somatic and

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emotional responses, which may interfere with cognitive responses according to Pennebaker’s (1982) attention theory, individuals more sensitive to somatic processes are probably more distracted by the internal signals. Thus, we hypothesized that individuals high in cardiac perception show worse cognitive performance under stress compared to individuals low in cardiac perception.

Methods Participants Fifty participants took part in the study (26 men, 24 women). The mean age was 23.92 years (SD = 3.01). All participants had a university-entrance diploma. Forty-six were university students and 4 were in the workforce. The sample consisted of 25 participants with high cardiac perception and 25 participants with low cardiac perception (for assignment of participants to the two cardiac perception groups see next section). To be included, potential participants had to be free of any history of cardiac or cardiovascular diseases or any axis one disorders, as defined by the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV, American Psychiatric Association, 1994). Additionally, participants included in the study did not take any medication affecting the cardiac or respiratory system. We screened participants’ health status using the Stamm-Screening Questionnaire (SSQ, Wittchen & Perkonig, 1996). All participants gave written informed consent and received a financial remuneration of 12 €. Assessment of cardiac perception The participants were assigned to the high versus low cardiac perception group according to their performance in the heartbeat detection task (Schandry, 1981). In this task participants were instructed to count their heartbeats silently without taking their pulse or attempting any other physical manipulations, which could facilitate the detection of heartbeats. First, participants had to relax during a 5-min rest period. Afterwards, three counting phases followed. These lasted for 25, 35, and 45 s, which were separated by rest periods of 30 s. Start and stop signals for counting were given by the investigator. An individual heartbeat perception score was calculated by relating the reported to the actual heartbeats according to the following formula: Heartbeat perception score ¼ X 1=3 ð1  ðjactual heartbeats  reported heartbeatsjÞ= actual heartbeatsÞ

The heartbeat perception score ranges from 0 to 1. Large differences between reported and actual heartbeats result in low scores and indicate low cardiac perception, whereas small differences between reported and actual heartbeats result in high scores and indicate high cardiac perception. In accordance with previous studies, we used a cut-off score of .85 to assign participants to the high versus low cardiac perception group (e.g. Montoya et al., 1993; Pollatos et al., 2005; Schandry et al., 1986). In our study, the high cardiac perception group had significantly higher heartbeat perception scores (M = 0.95, SD = 0.04) as compared to the low cardiac perception group (M = 0.67, SD = 0.12) [t(48) = 10.70, p \ .001]. The groups with high and low cardiac perception did not differ regarding gender (per group 13 men and 12 women). The groups did also not differ either in their mean age (high cardiac perception: M = 24.12, SD = 2.83; low cardiac perception: M = 23.72, SD = 3.22; t(48) = 0.47, p = .64) or in their body mass index (high cardiac perception: M = 22.13, SD = 2.29; low cardiac perception: M = 22.42, SD = 2.50; t(48) = 0.42, p = .68). The distribution of participants according to graduation and profession was comparable: All participants had a universityentrance diploma. In the high cardiac perception group, 22 participants were university students and three were in the workforce. In the low cardiac perception group, 24 participants were university students and one was in the workforce. The groups did not differ significantly regarding their profession (v2 = 3.58, p = .36). Mental stress induction In order to induce mental stress, participants had to conduct the Determination Test (Vienna Testsystem, SCHUFRIED GmbH, Mo¨dling, Austria). This test assesses the ability to react under pressure. During the test, participants had to respond simultaneously to visual stimuli (red, green, yellow, blue and white dots on a computer screen) and acoustic signals (two tones of different pitches presented via speakers) by pressing a button. The response panel consisted of five colored buttons (red, green, yellow, blue and white), each associated with the correspondingly colored dot presented on the computer screen. There was also one light grey button and one dark grey button. The former had to be pressed when the high tone was presented, and the latter had to be pressed when the low tone was presented. The stimuli were presented continuously and rapidly with fixed time limits. The stress test consisted of three stress periods with different time limits (1,583, 948 and 1,078 ms).

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Assessment of emotional experience and cognitive performance Emotional experience was assessed using the Multidimensional Mood Questionnaire (Steyer et al., 1997). This questionnaire consists of three bipolar dimensions that describe the current emotional state of an individual: (1) good versus bad mood, (2) wakefulness versus sleepiness and (3) calmness versus restlessness. Participants had to judge 24 adjectives on 5-point Likert scales (1 = definitely not, 5 = very much). Low sum scores on the dimensions indicate bad mood, wakefulness and restlessness. Cronbach’ s Alpha for the subscales is between .86 and .94 (Steyer et al., 1997). Cognitive performance was assessed by several outcome variables of the Determination Test: (1) the number of correct reactions, (2) the number of incorrect reactions and (3) the number of omitted reactions. In order to intensify the participants’ stress experience, participants were instructed to work as fast as possible and to make as few mistakes as possible. Additionally, they were told that their financial remuneration would depend on their test performance.

Assessment of control variables To control for the impact of third variable effects, we additionally assessed trait anxiety, since this variable has been associated with cardiac perception (Pollatos et al., 2007a, b, 2009) and stress responses (Gonzalez-Bono et al., 2002; Wilken et al., 2000). Trait anxiety was assessed with the items for trait anxiety of the German adaptation of the State-Trait-Anxiety Inventory (STAI, Laux et al., 1981). The items describe how one feels in general and are answered along 4-point Likert scales (1 = almost never, 4 = almost always). Furthermore, we assessed performance motivation in order to ensure that differences in emotional experience during stress periods were not affected by current effort. Performance motivation was controlled with two items, which participants had to judge on 10-point Likert scales (0 = not at all, 9 = very much). First, participants answered how important it was for them to perform well on the Determination Test (performance motivation) and second, how important it was for them to win a lot of money (financial motivation). As fitness can also affect physiological processes (e.g. Forcier et al., 2006), we asked the participants to answer two items, which assessed how much exercise they do (in minutes per week) and what kind of exercise they do (power and/or endurance training).

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Procedure Upon arrival at the laboratory, participants were given written information about the experiment and informed consent was obtained. Thereafter, they were seated on a chair and were fitted with electrodes to measure heart rate and skin conductance. The experiment began with a 10-min rest period, followed by the heartbeat perception task. Subsequently, the Determination Test was carried out, beginning with a short practice period to ensure comprehension of the task. The Determination Test lasted for 8 min. The Multidimensional Mood Questionnaire was completed immediately after the rest period and the Determination Test. Questionnaires assessing the control variables were completed at the end of the Determination Test. Physiological recording Heart rate and mean skin conductance level were assessed during the rest and the stress periods using the Biopac MP 150 (Biopac Systems, Inc., Goleta, CA). An electrocardiogram (ECG) was recorded with nonpolarizable Ag– AgCl electrodes, which were attached to the right mid clavicle and lower left rib cage. ECG activity was digitized at a sampling rate of 500 Hz. R-waves were detected automatically and converted into heart rate. For skin conductance recording, electrodes filled with an isotonic gel were attached to the thenar and hypothenar of the nondominant hand. Skin conductance was sampled at 250 Hz. Mean heart rate and mean skin conductance level were analyzed using the software Biopac AcqKnowledge 3.9.1 (BIOPAC Systems, Inc., Goleta, CA) for the rest period and the stress period. Data analysis Differences between the cardiac perception groups in emotional experience, heart rate and skin conductance level were assessed using repeated measurement ANOVAS with experimental condition (rest period vs. stress period) as within-subject factor and cardiac perception group (high vs. low cardiac perception) as between-subject factor. Degrees of freedom were adjusted according to Greenhouse and Geisser where appropriate. We carried out follow-up contrasts for differences between cardiac perception groups. As the variables of cognitive performance were not normally distributed and in order to compare the three cognitive parameters, we z-standardized (1) the number of correct reactions, (2) the number of incorrect reactions and (3) the number of omitted reactions. We used the z-values

J Behav Med Good mood score

sum score

40

*

30 20 10 0 Rest period

Stress period

High cardiac perception

Low cardiac perception

Wakefulness score 40

sum score

to indicate differences between participants high and low in cardiac perceptions regarding cognitive performance using a MANOVA procedure. Pearson correlation coefficients were calculated for the relation between the heartbeat perception score and the mean of negative emotions as well as the three z-standardized cognitive performance parameters (correct reactions, incorrect reaction, omitted reactions). Furthermore, we used t tests to indicate group differences in trait anxiety, performance motivation, financial motivation and the time per week the participants spend exercising. Pearson’s Chi square test was conducted in order to analyze differences between participants high and low in cardiac perception with respect to current exercise activity (power and/or endurance training).

Results

30 20 10 0 Rest period

Emotional experience

Stress period

High cardiac perception

Low cardiac perception

Calmness score 40

sum score

The repeated measurement ANOVA for the dimension good versus bad mood revealed a significant main effect of experimental condition [F(1, 48) = 91.49, p \ .001, g2p = .66] with a lower good mood score during the stress period compared to the rest period. The main effect of cardiac perception group on the dimension good versus bad mood was not significant [F(1, 48) = 2.72, p = .11, g2p = .05]. But there was a significant interaction effect between experimental condition and cardiac perception group [F(1, 48) = 4.44, p = .04, g2p = .09]. While the groups did not differ during the rest period (high cardiac perception: M = 35.11, SD = 3.43; low cardiac perception: M = 35.38, SD = 1.84; t(48) = 0.35, p = .73), participants high in cardiac perception showed a lower good mood score (M = 27.92, SD = 5.92) as compared to participants low in cardiac perception (M = 30.79, SD = 3.74) during the stress period [t(48) = 2.05, p = .047] (see Fig. 1). For the dimension wakefulness versus sleepiness, the repeated measurement ANOVA did not reveal a main effect of experimental condition [F(1, 48) = 0.52, p = .47, g2p = .01] nor did it show a main effect of cardiac perception group [F(1, 48) = 0.04, p = .84, g2p \ .01]. Finally, there was no interaction effect between experimental condition and cardiac perception group [F(1, 48) = 0.32, p = .58, g2p \ .01]. The repeated measurement ANOVA for the dimension calmness versus restlessness revealed a significant main effect of experimental condition [F(1, 48) = 306.00, p \ .001, g2p = .86] with a lower calmness score during the stress period (M = 20.31, SD = 5.67) compared to the rest period (M = 35.88, SD = 2.65). There was no main

30 20 10 0

Rest period

High cardiac perception

Stress period

Low cardiac perception

Fig. 1 Mean values of emotional experience of participants high versus low in cardiac perception during the rest period and the stress period

effect of cardiac perception group [F(1, 48) = 0.46, p = .50, g2p \ .01], nor was there any interaction effect between experimental condition and cardiac perception group [F(1, 48) \ 0.01, p = .97, g2p \ .001]. Cognitive performance The MANOVA revealed no group differences regarding the number of correct reactions [F(1, 48) = 0.25, p = .62, g2p = .01]. However, there was a significant difference between participants high in cardiac perception and participants low in cardiac perception regarding the number of incorrect reactions [F(1, 48) = 12.59, p = .001, g2p = .21], with participants high in cardiac perception showing more incorrect reactions than participants low in cardiac perception. There was also a significant difference

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J Behav Med Number of correct reactions

Mean number

600 550 500 450 400 350 300 High cardiac perception

Low cardiac perception

Number of incorrect reactions

Mean number

10 8

**

6 4 2 0 High cardiac perception

Low cardiac perception

Number of omitted reactions 10 8

Mean number

tively with the dimension good versus bad mood for the stress period (r = -.26, p = .07). However, there was no significant correlation between cardiac perception and the dimension wakefulness versus sleepiness (r = -.09, p = .56) or the dimension calmness versus restlessness (r = .01, p = .97) for the stress period. There was also no significant correlation between cardiac perception and the three emotional dimensions during the rest period (all rs \.17, all ps [.23). With regard to cognitive performance, correlation analyses revealed that cardiac perception correlated positively with the number of incorrect reactions (r = .43, p \ .01). However, there were no significant correlation between cardiac perception and the number of correct reactions (r = -.01, p = .97) or the number of omitted reactions (r = -.23, p = .11).1

6

*

4 2 0 High cardiac perception

Low cardiac perception

Fig. 2 Cognitive performance of participants high versus low in cardiac perception during the stress period

regarding the number of omitted reactions [F(1, 48) = 4.65, p = .04, g2p = .09], with participants high in cardiac perception showing less omitted reactions than participants low in cardiac perception (see Fig. 2). To analyze whether participants high and low in cardiac perception differed in their sum errors, we calculated an errorscore by subtracting the z-standardized number of omitted reactions from the z-standardized number of incorrect reaction. Participants high in cardiac perception (M = 0.75, SD = 1.12) showed significantly more errors in the Determination Test than participants low in cardiac perception (M = -0.74, SD = 1.36) (t (48) = 4.25, p \ .001). Relationship between cardiac perception and emotion experience and cognitive performance With regard to emotion experience, correlation analyses revealed that cardiac perception correlated by trend nega-

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Impact of emotional experience on cognitive performance In order to clarify the impact of emotional experience and cardiac perception on cognitive performance, a regression analysis was computed with the good mood score during rest and stress as well as the heartbeat perception score as predictor variables and the error-index as the dependent variable. Only the heartbeat perception score entered the model as a significant predictor (R2 = .26; heartbeat perception score: beta = .42, p = .003; good mood score during rest: beta = .23, p = .13; good mood score during stress: beta = -.21, p = .17). Multicollinearity did not bias the model (heartbeat perception score: tolerance = .93, VIF = 1.08; good mood score during rest = .77 VIF = 1.30; good mood score during stress: tolerance = .72, VIF = 1.39). Physiological response Regarding mean heart rate, a repeated measurement ANOVA revealed a significant main effect of experimental condition [F(1, 45) = 71.91, p \ .001, g2p = .62] with higher heart rates during the stress period (M = 82.84, SD = 11.08) than during the rest period (M = 73.87, SD = 10.48). Participants high in cardiac perception did 1

Additionally we conducted correlation analyses between heart rate and skin conductance level under stress and emotional experience as well as cognitive performance. There was neither a significant correlation between heart rate under stress and emotional experience (all rs \.23, all ps [.12) nor between skin conductance level under stress and emotional experience (all rs\.17, all ps[.24). There was also no significant correlation between skin conductance level under stress and cognitive performance (all rs \.12, all ps [.42). Only the correlation between heart rate under stress and correct reactions (r = -.29, p \ .05) as well as heart rate under stress and omitted reactions (r = .29, p = .05) reached significance.

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not differ from participants low in cardiac perception during the rest period (high: M = 73.63, SD = 13.86 vs. low: 74.11, SD = 5.33) nor during the stress period (high: M = 80.78, SD = 13.95 vs. low: 84.98, SD = 6.62; [F(1, 45) = 0.62, p = .43, g2p = .02]. There was no significant interaction between experimental condition and cardiac perception group [F(1, 45) = 3.06, p = .09, g2p = .06]. Regarding skin conductance level, the repeated measurement ANOVA also revealed a significant main effect of experimental condition [F(1, 48) = 192.75, p \ .001, g2p = .80], with higher skin conductance levels during the stress period (M = 6.33, SD = 2.50) than during the rest period (M = 3.33, SD = 2.37). Participants high in cardiac perception did not differ in skin conductance level from participants low in cardiac perception during the rest period (high cardiac perception: M = 3.42, SD = 2.54 vs. low cardiac perception: M = 3.25, SD = 2.23) nor during the stress period (high cardiac perception: M = 6.08, SD = 2.49 vs. low cardiac perception: M = 6.59, SD = 2.54; F(1, 48) = 0.06, p = .80, g2p \ .01). There was no significant interaction between experimental condition and cardiac perception group in skin conductance level [F(1, 48) = 2.41, p = .13, g2p = .05]. Control variables Participants high and low in cardiac perception did not differ with respect to trait anxiety (high cardiac perception: M = 35.28, SD = 8.53 vs. low cardiac perception: M = 32.92, SD = 5.76, t(48) = 1.15, p = .26), performance motivation (high cardiac perception: M = 8.54, SD = 0.66 vs. low cardiac perception: M = 8.40, SD = 0.82, t(48) = 0.67, p = .51), financial motivation (high cardiac perception: M = 6.67, SD = 2.14 vs. low cardiac perception: M = 6.60, SD = 2.40, t(48) = 0.10, p = .92) or the amount time per week they spent exercising (high cardiac perception: M = 175.55 min, SD = 132.30 min vs. low cardiac perception: M = 200.22 min, SD = 119.42 min, t(48) = 0.69, p = .49). They also did not differ with respect to their frequency distribution regarding power training (v2 = 3.00, p = .15) and endurance training (v2 = 1.56, p = .32).

Discussion Our study aimed at investigating whether and how cardiac perception affects emotional experience and cognitive performance during mental stress. In accordance with our hypotheses, we found that participants high in cardiac perception reported worse mood during mental stress and made more reaction errors than participants low in cardiac

perception. Cognitive performance deterioration during mental stress was not explained by worse mood but by cardiac perception. The results were not moderated by physiological responses, as the cardiac perception groups did not differ in their heart rate or skin conductance level during the rest and the stress period. We see our finding on emotional experience in line with emotion theories, which emphasize the importance of somatic feedback for emotional processes (Bechara & Naqvi, 2004; Cacioppo et al., 1992; Damasio, 1994; James, 1884; Thayer & Lane, 2000). According to James (1884) and Damasio (1994), somatovisceral feedback is essential for emotional experience. Accordingly, we assume that individuals high in cardiac perception experience the increase in heart rate during mental stress to a stronger degree, which affects emotional experience. The result is also in line with previous studies reporting stronger emotional experience in individuals high in cardiac perception compared to individuals low in cardiac perception (e.g. Hantas et al., 1982; Pollatos et al., 2007a, c, 2005; Schandry, 1981, 1983; Wiens et al., 2000). Moreover, our data extend previous findings on cardiac perception and emotional experience by demonstrating that individuals high in cardiac perception report more negative emotions under mental stress. This substantiates our earlier study where we were able to demonstrate that individuals high in cardiac perception reported more negative emotions during a mental arithmetic task than individuals low in cardiac perception (Kindermann & Werner, accepted). In the present study we were able to replicate this finding by using a different method for stress induction. We did not however find differences between the groups on the mood dimensions wakefulness versus sleepiness and calmness versus restlessness for the stress period. As these latter dimensions describe more general bodily states than specific emotional experience, it seems plausible that both groups had a similar level of arousal during the mental stress task. Furthermore, the items of these dimensions describe general somatic symptoms such as e.g. ‘‘fresh’’ or ‘‘exhausted’’ and thus do not relate directly to cardiovascular signals, which might affect individuals high in cardiac perception to a stronger degree. Our data also indicate that mental stress does not only affect emotional responses in high cardiac perception but also impairs cognitive performance. In the current study, individuals high in cardiac perception showed more incorrect reactions as well as a higher error-index in the mental stress test than individuals low in cardiac perception. Incorrect reactions represent difficulty in inhibiting irrelevant responses and hint at impairment in attention in the Determination Test (Neuwirth & Benesch, 2007). As cognitive performance was not related to mood but to cardiac perception in our study, cognitive impairment does

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not seem to result from stronger emotional disturbances during mental stress. Thus, we assume that the decreased cognitive performance in high cardiac perception may be explained by directing attention to cardiac signals, which might interfere with directing attention to the task. We see this in accordance with Pennebaker’ s (1982) Competition of Cues Theory, which states that external and internal stimuli share the same limited cognitive resources. Thus, interference may occur if internal stimuli and external stimuli compete for the same cognitive resources. Accordingly, we assume that participants high in cardiac perception had less cognitive resources for the Determination Test, because their better perception of internal stimuli competed with the elaboration of external stimuli. As a result, participants high in cardiac perception were less accurate in the elaboration of external stimuli, which in turn could have led to more errors. This reasoning is also in line with a recent study demonstrating that individuals high in cardiac perception show attention interference for emotional words in an emotional Stroop task compared to individuals low in cardiac perception (Werner et al., 2014). At first glance, our results on cognitive functioning seem to contradict studies showing a better cognitive functioning for high cardiac perception as compared to low cardiac perception. Former studies have shown benefits in decision making, emotional memory and attention processes in high cardiac perception (Matthias et al., 2009; Werner et al., 2009c, 2010). However, these former studies investigated the relationship between cardiac perception and cognitive functioning under non-stress conditions. Regarding a stressful condition, our study showed a negative effect of cardiac perception on cognitive functioning. We assume that, in stressful situations the resulting physiological arousal is more distracting and requires more cognitive resources for individuals more sensitive to interoceptive processes and thus, leads to cognitive impairment. Relating to the physiological variables, our results do not show differences between individuals high and low in cardiac perception. Nonetheless, both groups showed an increase in heart rate and skin conductance level in the stress condition, indicating that the Determination Test was experienced as challenging. We reason that differences in emotional experience or cognitive performance under stress are not due to a stronger physiological arousal under stress in participants high in cardiac perception as compared to participants low in cardiac perception. Instead, we hold that these differences are due to a better perception of somatovisceral feedback in participants high in cardiac perception. This is in line with previous studies showing no differences in heart rate or skin conductance between participants high and low in cardiac perception (Eichler & Katkin, 1994; Hantas et al., 1982; Werner et al., 2009a, b; Wiens et al., 2000). As we however did not assess car-

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diodynamic measures we cannot rule out the possibility that differences in cardiodynamic mechanisms could account for the differences in cognitive performance under stress with regard to cardiac perception. Previous studies have shown that high cardiac perception is related to increased contractility of the heart (Herbert et al., 2010; Schandry et al., 1993). Thus increases in cardiac contractility under stress may be perceived by individuals high in cardiac perception and impair cognitive processes. Our study suggests that individuals high in cardiac perception may be especially at risk of developing stressrelated diseases as they show a more pronounced emotional vulnerability to stress and their cognitive performance is more impaired under stress. This matches well with early studies on cardiac perception and anxiety where cardiac perception has been assumed to be of particular importance for the etiology and the maintenance of anxiety and anxiety disorders (cf. Domschke et al., 2010; Ehlers & Breuer, 1996). For instance, research has shown that patients with panic disorder display a more accurate cardiac perception than do healthy controls (Ehlers & Breuer, 1992; Eley et al., 2004; Van der Does et al., 2010). However, there are also studies suggesting a positive effect of cardiac perception on emotion regulation (e.g. Werner et al., 2013) and cognitive performance (Matthias et al., 2009; Werner et al., 2009a, b, c, 2010). Therefore it seems that a tripartite model of cardiac perception may explain the relation between cardiac perception and emotional responses best. Accordingly, low levels of cardiac perception are accompanied by less emotional stress responses, high cardiac perception by dysfunctional emotional stress responses and middle cardiac perception by average emotional stress responses. Dunn et al. (2010) already distinguished three groups of cardiac perception (average, better and worse) and showed that bodily signals affected decision-making more in high cardiac perception than in low cardiac perception. Finally, some limitations of the study have to be considered. The stress induced in the study was quite moderate, as ratings of the emotional experience indicate. Nevertheless, there were significant increases in heart rate and skin conductance level from the rest period to the stress period. However, it is necessary to analyze the relationship between cardiac perception, performance and emotional experience in more distressing situations in order to generalize the present findings. In this context, it would be interesting to investigate whether cardiac perception moderates emotional experience and performance in a sample of participants having been exposed to severe stressful events, like patients with burnout or posttraumatic stress disorder. Furthermore, it would be interesting to investigate the relationship between cardiac perception and cardiovascular diseases, as these diseases are strongly

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related to chronic stress experiences. This could provide new insights into the etiology and therapy of this disorder. Another limitation concerns the artificial stressor that we used in our study. To determine the relevance of our results for daily life, it is necessary to analyze the impact on cardiac perception on cognitive performance and emotions under a natural stressor, such as examination stress. In summary, our study showed a moderating effect of cardiac perception on emotional experience and cognitive performance in response to a stressor. Our results indicate that cardiac perception processes affect stress processes. Therefore, cardiac perception should be taken into consideration as a further factor explaining variance in the individual stress response. Conflict of interest Authors Nicole K. Kindermann and Natalie S. Werner declare that they have no conflict of interest. Animal and Human Rights and Informed Consent All procedures followed were in accordance with ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, as revised in 2000. Informed consent was obtained from all patients for being included in the study.

References American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (Vol. 4). Washington, D.C.: American Psychiatric Association. Barrett, L. F., Quigley, K. S., Bliss-Moreau, E., & Aronson, K. R. (2004). Interoceptive sensitivity and self-reports of emotional experience. Journal of Personality and Social Psychology, 87, 684–697. doi:10.1037/0022-3514.87.5.684 Bechara, A., & Naqvi, N. (2004). Listening to your heart: Interoceptive awareness as a gateway to feeling. Nature Neuroscience, 7, 102–103. doi:10.1038/nn0204-102 Brener, J. (1974). A general model of voluntary control applied to the phenomena of learned cardiovascular change. In P. A. Obrist, A. H. Black, J. Brener, & L. V. DiCara (Eds.), Cardiovascular psychophysiology (pp. 365–391). Chicago: Aldine. Brener, J., & Kluvitse, C. (1988). Heartbeat detection: Judgements of the simultaneity of external stimuli and heartbeats. Psychophysiology, 25, 554–561. doi:10.1111/j.1469-8986.1988.tb01891.x Cacioppo, J. T., Berntson, G. G., & Klein, D. J. (1992). What is an emotion? The role of somatovisceral afference, with special emphasis on somatovisceral ‘‘illusions’’. In M. S. Clark (Ed.), Emotion and social behaviour (pp. 63–98). Thousand Oaks, CA: Sage. Cameron, O. G. (2001). Interoception: The inside story—A model for psychosomatic processes. Psychosomatic Medicine, 63, 697–710. doi:0033-3174/01/6305-0697 Carroll, D., & Whellock, J. (1980). Heart rate perception and the voluntary control of heart rate. Biological Psychology, 11, 169–180. doi:10.1016/0301-0511(80)90053-8 ¨ hman, A., & Dolan, R. J. Critchley, H. D., Wiens, S., Rotshtein, R., O (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189–195. doi:10.1038/nn1176 Dale, A., & Anderson, D. (1978). Information variables in voluntary control and classical conditioning of heart rate: Field dependence

and heart-rate perception. Perceptual and Motor Skills, 47, 79–85. doi:10.2466/pms.1978.47.1.79 Damasio, A. R. (1994). Descartes’ error: Emotion, reason, and the human brain. New York: Grosset/Putnam Books. Domschke, K., Stevens, S., Pfleiderer, B., & Gerlach, A. L. (2010). Interoceptive sensitivity in anxiety and anxiety disorders: An overview and integration of neurobiological findings. Clinical Psychology Review, 30, 1–11. doi:10.1016.j.cpr.2009.08.008 Dunn, B. D., Galton, H. C., Morgan, R., Evans, D., Oliver, C., Meyer, M., et al. (2010). Listening to your heart: How interoception shapes emotion experience and intuitive decision making. Psychological Science. doi:10.11.77/0956797610389191. Ehlers, A., & Breuer, P. (1992). Increased cardiac awareness in panic disorder. Journal of Abnormal Psychology, 101, 371–382. doi:10.1037//0021-843X.101.3.371 Ehlers, A., & Breuer, P. (1996). How good are patients with panic disorder at perceiving their heartbeats? Biological Psychology, 42, 165–182. doi:10.1016/0301-0511(95)05153-8 Eichler, S., & Katkin, E. S. (1994). The relationship between cardiovascular reactivity and heartbeat detection. Psychophysiology, 31, 229–234. doi:10.1111/j.1469-8986.1994.tb02211.x Eley, T. C., Stirling, L., Ehlers, A., Gregory, A. M., & Clark, D. M. (2004). Heart-beat perception, panic/somatic symptoms and anxiety sensitivity in children. Behaviour Research and Therapy, 42, 439–448. doi:10.1016/S0005-7967(03)00152-9 European Agency for Safety and Health at Work (EU-OSHA). (2003). Annual report 2002. ISBN 92-9191-024-4. Forcier, K., Stroud, L. R., Papandonatos, G. D., Hitsman, B., Reiches, M., Krishnamoorthy, J., et al. (2006). Links between physical fitness and cardiovascular reactivity and recovery to psychological stressors: A meta-analysis. Health Psychology, 25, 723–739. doi:10.1037/0278-6133.25.6.723 Gonzalez-Bono, E., Moya-Albiol, L., Salvador, A., Carrillo, E., Ricarte, J., & Gomez-Amor, J. (2002). Anticipatory autonomic response to a public speaking task in women: The role of trait anxiety. Biological Psychology, 60, 37–49. doi:10.1016/S03010511(02)00008-X Hantas, M., Katkin, E. S., & Blascovich, J. (1982). Relationship between heartbeat discrimination and subjective experience of affective state. Psychophysiology, 19, 563. doi:10.1111/j.14698986.1982.tb02584.x Harver, A., Katkin, E. S., & Bloch, E. (1994). Signal-detection outcomes on heartbeat and respiratory resistance detection tasks in male and female subjects. Psychophysiology, 30, 223–230. doi:10.1111/j.1469-8986.1993.tb03347.x Herbert, B. M., Pollatos, O., Flor, H., Enck, P., & Schandry, R. (2010). Cardiac awareness and autonomic cardiac reactivity during emotional picture viewing and mental stress. Psychophysiology, 47, 342–354. doi:10.1111/j.1469-8986.2009.00931.x James, W. (1884). What is an emotion? Mind, 9, 188–205. Jones, G. E. (1994). Perception of visceral sensations: A review of recent findings, methodologies, and future directions. In J. R. Jennings, P. K. Ackles, & M. G. H. Coles (Eds.), Advances in psychophysiology (pp. 55–191). London: Jessica Kingsley. Jones, F., & Bright, J. (2007). Stress: Health and illness. In A. Monat, R. S. Lazarus, & G. Reevy (Eds.), The Praeger handbook on stress and coping (Vol. 1). Westport, CT: Praeger. Jones, G. E., & Hollandsworth, J. G. (1981). Heart rate discrimination before and after exercise-induced augmented cardiac activity. Psychophysiology, 18, 252–257. doi:10.1111/j.1469-8986.1981. tb03029.x Katkin, E. S. (1985). Blood, sweat, and tears: Individual differences in autonomic self-perception. Psychophysiology, 22, 125–137. doi:10.1111/j.1469-8986.1985.tb01573.x Katkin, E. S., Blascovich, J., & Goldband, S. (1981). Empirical assessment of visceral self-perception: Individual and sex

123

J Behav Med differences in the acquisition of heartbeat discrimination. Journal of Personality and Social Psychology, 40, 1095–1101. doi:10.1037/0022-3514.40.6.1095 Katkin, E. S., Morell, M. A., Goldband, S., Bernstein, G. L., & Wise, J. A. (1982). Individual differences in heartbeat discrimination. Psychophysiology, 19, 160–166. doi:10.1111/j.1469-8986.1982. tb02538.x Kindermann, N. K., & Werner, N. S. Cardiac perception enhances stress experience. Journal of Psychophysiology (accepted). Laux, L., Glanzmann, P., Shaffner, P., & Spielberger, C. D. E. (1981). Das State-Trait-Angstinventar. Weinheim: Beltz Test. Low, C. A., Salomon, K., & Matthews, K. A. (2009). Chronic life stress, cardiovascular reactivity, and subclinical cardiovascular disease in adolescents. Psychosomatic Medicine, 71, 927–931. doi:0033-3174/09/7108-0927 Matthias, E., Schandry, R., Duschek, S., & Pollatos, O. (2009). On the relationship between interoceptive awareness and the attentional processing of visual stimuli. International Journal of Psychophysiology, 72, 154–159. doi:10.1016/j.ijpsycho.2008.12.001 McFarland, R. A. (1975). Heart rate perception and heart rate control. Psychophysiology, 12, 402–405. doi:10.1111/j.1469-8986.1975. tb00011.x Montgomery, W. A., Jones, G. E., & Hollandsworth, J. G. (1984). The effects of physical fitness and exercise on cardiac awareness. Biological Psychology, 18, 11–22. doi:10.1016/0301-0511(84) 90022-X Montoya, P., Schandry, R., & Mueller, A. (1993). Heartbeat evoked potentials (HEP): Topography and influence of cardiac awareness and focus of attention. Electroencephalography and Clinical Neurophysiology, 88, 163–172. doi:10.1016/0168-5597(93) 90001-6 Neuwirth, W., & Benesch, M. (2007). Wiener test system manual. Determinations test. Mo¨dling: Schuhfried GmbH. Pennebaker, J. W. (1982). The psychology of physical symptoms. New York: Springer. Pollatos, O., Gramann, K., & Schandry, R. (2007a). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28, 9–18. doi:10.1002/hbm.20258 Pollatos, O., Herbert, B. M., Kaufmann, C., Auer, D. P., & Schandry, R. (2007b). Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise. International Journal of Psychophysiology, 65, 167–173. doi:10.1016/j.ijpsycho.2007.03.005 Pollatos, O., Herbert, B. M., Matthias, E., & Schandry, R. (2007c). Heart rate response after emotional picture presentation is modulated by interoceptive awareness. International Journal of Psychophysiology, 63, 117–124. doi:10.1016/j.ijpsycho.2006.09. 003 Pollatos, O., Kirsch, W., & Schandry, R. (2005). On the relationship between interoceptive awareness, emotional experience, and brain processes. Cognitive Brain Research, 25, 948–962. doi:10. 1016/j.cogbrainres.2005.09.019 Pollatos, O., & Schandry, R. (2008). Emotional processing and emotional memory are modulated by interoceptive awareness. Cognition and Emotion, 22, 272–287. doi:10.1080/02699930701 357535 Pollatos, O., Traut-Mattausch, E., & Schandry, R. (2009). Differential effects of anxiety and depression on interoceptive accuracy. Depression and Anxiety, 26, 167–173. doi:10.1002/da.20504 Rouse, C. H., Jones, G. E., & Jones, K. R. (1988). The effect of body composition and gender on cardiac awareness. Psychophysiology, 25, 400–407. doi:10.1111/j.1469-8986.1988.tb01876.x Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18, 483–488. doi:10.1111/j.1469-8986.1981. tb02486.x

123

Schandry, R. (1983). On the relationship between improvement of cardiac perception and the increase of emotional experience. Psychophysiology, 20, 468–469. doi:10.1111/j.1469-8986.1983. tb00923.x Schandry, R., & Bestler, M. (1995). Cardiovascular function and heartbeat perception. In D. S. R. Vaitl & R. Schandry (Eds.), From the heart to the brain (pp. 224–250). Frankfurt a. M.: Peter Lang. Schandry, R., Bestler, M., & Montoya, P. (1993). On the relation between cardiodynamics and heartbeat perception. Psychophysiology, 30, 467–474. doi:10.1111/j.1469-8986.1993.tb02010.x Schandry, R., Sparrer, B., & Weitkunat, R. (1986). Brain-electrical correlates of the heart-beat signal. Psychophysiology, 23, 459. doi:10.1111/j.1469-8986.1986.tb00655.x Steyer, R., Schwenkmezger, P., Notz, P., & Eid, M. (1997). Der Mehrdimensionale Befindlichkeitsfragebogen (MDBF)—Multidimensional Mood Questionnaire. Go¨ttingen: Hogrefe. Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201–216. doi:10.1016/S01650327(00)00338-4 Vaitl, D. (1996). Interoception. Biological Psychology, 42, 1–27. doi:10.1016/0301-0511(95)05144-9 Van der Does, W. A. J., Antony, M. M., Ehlers, A., & Barsky, A. J. (2010). Heartbeat perception in panic disorder: A reanalysis. Behaviour Research and Therapy, 38, 47–62. doi:10.1016/ S0005-7967(98)00184-3 Werner, N. S., Duschek, S., Mattern, M., & Schandry, R. (2009a). Interoceptive sensitivity modulates anxiety during public speaking. Journal of Psychophysiology, 23, 85–94. doi:10.1027/02698803.23.2.85 Werner, N. S., Duschek, S., Mattern, M., & Schandry, R. (2009b). The relationship between pain perception and interoception. Journal of Psychophysiology, 23, 35–42. doi:10.1027/0269-8803.23.1.35 Werner, N. S., Jung, K., Duschek, S., & Schandry, R. (2009c). Enhanced cardiac perception is associated with benefits in decision-making. Psychophysiology, 46, 1123–1129. doi:10. 1111/j.1469-8986.2009.00855.x Werner, N. S., Kerschreiter, R., Kindermann, N. K., & Duschek, S. (2013). Interoceptive awareness as a moderator of affective responses to social exclusion. Journal of Psychophysiology, 27, 39–50. doi:10.1027/0269-8803/a000086 Werner, N. S., Mannhart, T., Reyes del Paso, G. A., & Duschek, S. (2014). Attention interference for emotional stimuli in cardiac interoceptive awareness. Psychophysiology. doi:10.1111/psyp. 12200. Werner, N. S., Peres, I., Duschek, S., & Schandry, R. (2010). Implicit memory for emotional words is modulated by cardiac perception. Biological Psychology, 85, 370–376. doi:10.1016/j. biopsycho.2010.08.008 Whitehead, W. E., Drescher, V. M., Heiman, P., & Blackwell, B. (1977). Relation of heart rate control to heartbeat perception. Biofeedback and Self-Regulation, 2, 371–392. doi:10.1007/ BF00998623 Wiens, S., Mezzacappa, E. S., & Katkin, E. S. (2000). Heartbeat detection and the experience of emotions. Cognition and Emotion, 14, 417–427. doi:10.1080/026999300378905 Wilken, J. A., Smith, B. D., Tola, K., & Mann, M. (2000). Trait anxiety and prior exposure to non-stressful stimuli: Effects on psychophysiological arousal and anxiety. International Journal of Psychophysiology, 37, 233–242. doi:10.1016/S01678760(00)00082-9 Wittchen, H.-U., & Perkonig, A. (1996). DIA-X SSQ. Frankfurt: Swets Test Services.