Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise

International Journal of Psychophysiology 65 (2007) 167 – 173 www.elsevier.com/locate/ijpsycho

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Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise Olga Pollatos a,⁎, Beate M. Herbert b , Christian Kaufmann c , Dorothee P. Auer d , Rainer Schandry a a

b

Department of Psychology, LMU University, Munich, Germany Department of Clinical and Cognitive Neuroscience, University of Heidelberg, Central Institute of Mental Health, Germany c Clinical Psychology, Department of Psychology, Humboldt-Universität zu Berlin, Germany d Academic Radiology, Queen's Medical Centre, University of Nottingham, United Kingdom Received 11 July 2006; received in revised form 9 February 2007; accepted 7 March 2007 Available online 14 March 2007

Abstract The present study was designed to investigate the relation between cardiovascular reactivity, trait anxiety and the interoceptive awareness. Eighteen male subjects underwent a heartbeat perception task and performed an isometric handgrip exercise. Subjects with high reactivity showed a higher degree of interoceptive awareness and trait anxiety suggesting that a habitually increased sympathetic outflow might be one variable contributing to the establishment of high interoceptive awareness and trait anxiety. © 2007 Elsevier B.V. All rights reserved. Keywords: Interoceptive awareness; Anxiety; Cardiovascular reactivity; Heart rate; Blood pressure; Handgrip; Sympathetic nervous system

1. Introduction The ability to perceive bodily changes – so-called interoceptive awareness – plays an important role in many theories of emotions such as proposed by James (James, 1884), Schachter and Singer (Schachter and Singer, 1962), or Damasio (Damasio, 1994; Damasio, 1999). William James was one of the first to postulate that viscero-afferent feedback is closely linked to emotional experience, stating that “bodily changes follow directly the perception of the exciting fact, and that our feelings of the same changes as they occur IS the emotion” (James, 1884). Despite its importance for emotions and many other processes, interoception is still an understudied area of sensory physiology (Cameron and Minoshima, 2002). Interoceptive awareness can be easily measured by using the ability to perceive one's heartbeats accurately (Cameron, 2001; Critchley et al., 2004; Jones et al., 1986; Pollatos et al., 2005a, 2006; Schandry et al., 1993). There is some evidence that heartbeat ⁎ Corresponding author. Leopoldstr. 13, 80802 Munich, Germany. Tel.: +49 89 2180 6356; fax: +49 89 2180 5233. E-mail address: [email protected] (O. Pollatos). 0167-8760/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.ijpsycho.2007.03.005

perception correlates with the ability to detect changes in other autonomically innervated organs (Whitehead and Drescher, 1980) and should therefore reflect a general sensitivity for visceral processes. There is confirming data on clinical populations known to have alterations in somatization and body perception like anxiety disorders, depression and eating disorders: Concerning anxiety disorders some studies showed an increased heartbeat perception (Ehlers et al., 1992, 2000; Pineles and Mineka, 2005; Van der Does et al., 2000; Wald and Taylor, 2005; White et al., 2006; Zoellner and Craske, 1999) while decreased heartbeat perception was found in depressive subjects (Dunn et al., in press). One common observation is the existence of substantial, interindividual differences in interoceptive awareness which may depend on different factors such as gender, percentage of body fat and physical fitness (Cameron, 2001; Cameron and Minoshima, 2002). Some studies suggest that also differences in cardiovascular parameters could contribute to observed differences in interoceptive awareness: Schandry and Bestler (Schandry and Bestler, 1995a) systematically manipulated cardiac activity by changing body position from supine to upright posture with a tilt-table in combination with bicycle

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ergometry to increase physical load and recorded myocardial performance by means of impedance cardiography. The authors found that during the various tilt and exercise phases, both changes in body position toward the horizontal and increases in physical load led to an improvement in interoceptive awareness. Similar results were demonstrated in an earlier study by Schandry et al. (Schandry et al., 1993), where different tilt/ exercise combinations induced changes in stroke volume significantly with interoceptive awareness assessed during the exercise conditions. O'Brien et al. (O'Brien et al., 1998) could show that increased systolic blood pressure facilitates detection of heartbeats. Additionally, a significantly greater proportion of the participants with higher systolic blood pressure was classified as subjects with high interoceptive awareness. These data imply that physiological characteristics of cardiac performance are essential determinants of interoceptive awareness. When physiological characteristics of cardiac reactivity as they appear e.g. during stressful situations facilitate the accurate detection of signals from the body by contributing to the consolidation of a habitually greater level of interoceptive awareness, then cardiovascular reactivity to emotional and physical stress should be positively related to interoceptive awareness. Some evidence exists confirming this hypothesis: Using emotional stimuli, psychophysiological arousal assessed by the P300 amplitude (Pollatos et al., 2007a; Pollatos and Schandry, 2004) and by heart rate reactivity (Pollatos et al., 2007b) to be positively related to interoceptive awareness. Further evidence for a possible relation between cardiovascular reactivity and interoceptive awareness stems from research on the pathophysiology of anxiety disorders (Cameron and Minoshima, 2002). Several studies (Ehlers, 1995; Ehlers et al., 2000; Pineles and Mineka, 2005; Roth et al., 1992; Van der Does et al., 2000; Wald and Taylor, 2005; White et al., 2006; Zoellner and Craske, 1999) have shown that interoceptive awareness is closely associated with anxiety disorders such as panic disorders or social phobia. Concerning panic disorders, Ehlers et al. (Ehlers et al., 2000) reported a higher degree of interoceptive awareness in panic patients. In a similar study with children, increased panic symptoms were associated with an enhanced ability to perceive internal physiological cues as measured by a heartbeat perception task (Eley et al., 2004). Interestingly, prior studies examining psychopathology and anxiety disorders have partly found increased cardiovascular reactivity to stressors (Friedman and Thayer, 1998; Gurguis et al., 1997; Monk et al., 2001; Richards and Bertram, 2000; Takahashi et al., 2005). For example Takahashi et al. (Takahashi et al., 2005) reported a positive relation between trait anxiety and autonomic reactivity during a social stress task. Results are yet not univocal, as e.g. Mauss et al. (Mauss et al., 2003) found comparable reactivity in high trait socially anxious and low trait socially anxious individuals during stressful speech tasks. Egloff and Schmukle (Egloff and Schmukle, 2002) suggested that implicit measures of anxiety which assess introspectively inaccessible processes that operate outside of awareness show a better relation to measures of cardiovascular reactivity than explicit test which assess introspectively accessible self-

descriptions. Confirming a close relation between interoceptive processes and trait anxiety, former work has shown that subjects with high interoceptive awareness also exhibit greater anxiety levels as measured by questionnaire (Critchley et al., 2004; Pollatos et al., 2007b, in press). Up to now it remains an open question whether cardiovascular reactivity to emotional or physical stress can predict interoceptive awareness and trait anxiety. Based on the data presented so far, one could hypothesize that cardiovascular reactivity is positively related to both interoceptive awareness and self-reported trait anxiety. Additionally, there should be a positive relation between these both personality variables. The primary purpose of the present study was to investigate the relations among cardiovascular reactivity (i.e. blood pressure, heart rate) induced by a physical stress task and both interoceptive awareness and trait anxiety in healthy subjects. Since the ventricular myocardium of primates is predominantly supplied by sympathetic fibers, increases of myocardial contractility usually occur during mental or physical stress (Lovallo et al., 1993; Matthews et al., 2003; Panknin et al., 2002). Static isometric exercise like sustained handgrip is known to induce an increase in heart rate and blood pressure (Rowell and Sheriff, 1988). The increase in blood pressure is a consequence of the activation of sympathetic vasoconstrictor neurons (Rowell and Sheriff, 1988) resulting in predominantly alpha-adrenergic activation. An increase in diastolic blood pressure and total peripheral resistance are the characteristics of this type of activation, along with moderate heart rate increases. In the light of the evidence presented so far, it was hypothesized that subjects with greater changes in cardiovascular and autonomic reactivity during physical load would exhibit higher levels of interoceptive awareness and trait anxiety. 2. Methods 2.1. Subjects 18 male subjects (mean age 25.2, SD 2.9, ranging from 21– 32 years) participated in the study. As gender may contribute to differences in interoceptive awareness (Cameron, 2001; Cameron and Minoshima, 2002), only male subjects were selected from an introductory course in psychology and received credit points for participation. All selected subjects had no history of psychiatric diseases or of heart diseases and gave informed written consent. The experiment was conducted in accordance with the Declaration of Helsinki. 2.2. Experimental design and procedure The study was performed in a quiet, comfortable environment at the Psychology Department of the University of Munich. Subjects filled in a questionnaire concerning personal data and the State-Trait-Anxiety Inventory (Spielberger et al., 1983) measuring state and trait anxiety (STAI). Subjects had to perform two experimental conditions: (1) A heartbeat perception task in which they were asked to count their heartbeats

O. Pollatos et al. / International Journal of Psychophysiology 65 (2007) 167–173

during four different time intervals and (2) a physical stress task in which they squeezed a handgrip at 30% of their maximum voluntary contraction with their left hand. The heartbeat perception task was performed in a sitting position and consisted of four heartbeat-counting phases (intervals lasting for 35, 25, 45, 60 s). During these intervals, participants were asked to count their own heartbeats silently. The beginning and end of the counting phases were signaled by a start and stop tone. During heartbeat-counting, subjects were instructed not to take their pulse or attempt to use other manipulations facilitating the counting of heartbeats. After the stop signal, subjects verbally reported the number of heartbeats counted. Subjects were neither informed about the length of the counting phases nor about their performance. Subsequently they rested semi-supine for 20 min in order to establish baseline haemodynamic conditions. After this resting phase baseline data was registered for five minutes. A light isometric exercise was performed using a handgrip task at about 30% of each subject's maximal voluntary contraction which had to be sustained for two minutes (Silke and McAuley, 1998). Cardiovascular measurements were made at baseline and during handgrip exercise. This stress condition was repeated after a ten minutes break. Haemodynamic variables were recorded at baseline and during exercise. The entire experiment lasted about 30 min. 2.3. Apparatus and physiological recordings All autonomic measures were averaged for baseline and physical exercise for each subject. As the physical stress task was repeated twice, autonomic measures were averaged across both periods. Finger arterial systolic and diastolic blood pressure was monitored continuously using the volume-clamp method, where the plethysmographic cuff was placed around the middle phalanx of the third finger of the left hand (Finapres 2300, Ohmeda, Louisville, USA). Heart rate and other cardiodynamic parameters were assessed using a non-invasive automated computerized impedance cardiography system (Cardioscreen; Medis, Ilmenau, Germany). Two pairs of disposable ECG Ag/AgCl electrodes were placed above the sternocleidomastoid region to the right and left of the volunteers' necks. Two more pairs of electrodes were placed in the medioclavicular line on each side of the lower thoracic aperture at the xiphoid level. The distance between two electrodes of one pair was 5 cm. This configuration also allows the registration of an electrocardiogram (ECG). Respiratory and other artefacts are automatically eliminated by signal-averaging algorithms. This impedance cardiography device has previously been shown to produce valid measures of haemodynamic processes (Scherhag et al., 1997). The Bernstein formula (Bernstein, 1986) was used to calculate stroke volume (SV) and derived indices. Cardiac output (CO) was computed as heart rate (HR) multiplied by stroke volume (CO = HR × SV). Total peripheral resistance (TPR) was computed as mean arterial blood pressure divided by cardiac output. Preejection period (PEP) was calculated.

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2.4. Interoceptive awareness A heartbeat perception score reflecting accuracy of interoceptive awareness was calculated as the mean score of four heartbeat perception intervals according to the following transformation: FORMULA: 1/4 Σ (1 − (|recorded heartbeats − counted heartbeats| / recorded heartbeats))

2.5. State and trait anxiety Mean state and trait anxiety scores were assessed as the mean subscore of the STAI questionnaire. 2.6. Data reduction and analyses The primary haemodynamic outcome measures were heart rate, systolic blood pressure, diastolic blood pressure, total peripheral resistance index, stroke volume, cardiac output and preejection period. Resting and exercising haemodynamic variables were evaluated using linear area-under-curve (AUC) analyses. Mean state and trait anxiety scores as well as mean interoceptive awareness scores were calculated. Investigating the effect of physical load on the haemodynamic variables, mean differences in haemodynamic outcome measures were analysed using one sample t-tests. Group differences between subjects with high and low cardiovascular reactivity concerning the variables interoceptive awareness and anxiety (state, trait anxiety) were assessed by submitting the data to three separate ANOVAs with the between subject factor cardiovascular reactivity (high/low). Where appropriate, degrees of freedom were adjusted after Greenhouse and Geiser. In the Results Section, uncorrected F-values are reported together with the Greenhouse–Geiser epsilon values and corrected probability levels. Pearson correlation analyses between the interoceptive awareness score and anxiety measures as well as partial correlations between mean haemodynamic changes and interoceptive awareness as well as trait anxiety were carried out. 3. Results 3.1. Haemodynamic responses to isometric exercise Haemodynamic responses to light isometric exercise are presented in Table 1. T-tests for dependent measures indicated that isometric handgrip exercise caused significant increases in heart rate, systolic blood pressure, diastolic blood pressure and total peripheral resistance index, whereas stroke volume, cardiac output and preejection time were significantly reduced. Based on their reactivity in each of these seven autonomic variables, a reactivity index was calculated by adding the subscores obtained in the variables in heart rate, systolic blood pressure, diastolic blood pressure, stroke volume and

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Table 1 Mean changes of haemodynamic variables from baseline to isometric handgrip exercise (N = 18; SEM = Standard Error of Means; ⁎⁎⁎: p b .001)

Heart rate (beats per minute) Systolic blood pressure (mm Hg) Diastolic blood pressure (mm Hg) Total peripheral resistance (mm Hg L− 1 min− 1) Stroke volume (ml) Cardiac output (L min− 1) Preejection period (ms)

Mean (SEM)

T (df = 17)

p

+5.8 (0.7) +10.6 (1.3) +5.3 (0.8) +174.2 (27.9)

5.8 8.4 6.5 6.3

⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎

− 14.1 (3.2) − 0.44 (0.08) − 29.7 (2.3)

− 4.4 − 5.5 − 13.0

⁎⁎⁎ ⁎⁎⁎ ⁎⁎⁎

preejection time (cardiac output and total peripheral resistance index were spared out as they are derived from the other measures) by using a median split categorization (scores 0 for low reactivity and score 1 for high reactivity) with total scores varying between 0 and 5. A median split procedure was applied to the total reactivity score. Nine subjects were assigned to the group with high reactivity (mean 3.8, SD 0.95) and were compared to nine subjects with low reactivity (mean 1.5, SD 0.70). Mean baseline values contrasting subjects with high and low reactivity is summarized in Table 2, the haemodynamic responses for both groups are depicted in Table 3. 3.2. Interoceptive awareness and anxiety in subjects with high vs. low cardiovascular reactivity The obtained mean scores in interoceptive awareness and anxiety are depicted in Table 4. Additionally, mean scores for both cardiovascular reactivity groups as well as the results of the statistical analyses are summarized in Table 4. 3.2.1. Interoceptive awareness As depicted in Table 4, the mean heartbeat perception score was .88 (SD .10, minimum .71, maximum .98) in the group with high cardiovascular reactivity compared to .76 (SD .06, minimum .66, maximum .90) in the low reactivity group. The observed difference in interoceptive awareness was statistical significant (F(1,16) = 15.15, p b .01, η2 = .49, ε = .90).

Table 3 Mean changes of haemodynamic variables from baseline to isometric handgrip exercise contrasting subjects with high (N = 9) and low cardiovascular reactivity (N = 9) High reactivity

Low reactivity

Heart rate (beats per minute) +7.9 Systolic blood pressure (mm Hg) +13.1 Diastolic blood pressure (mm Hg) +7.3 Total peripheral resistance (mm Hg L− 1 min− 1) +237.8 Stroke volume (ml) − 17.9 Cardiac output (L min− 1) − 0.55 Preejection period (ms) − 36.3

+3.7 +8.0 +3.4 +110.5 − 10.4 − 0.34 − 23.1

3.2.2. Anxiety There was no difference between subjects with high vs. low cardiovascular reactivity (mean 34.9 vs. 34.6; F(1,16) = 0.02, p = n.s., see Table 4) in state anxiety. Concerning trait anxiety, we observed a strong trend to higher trait anxiety scores in subjects with high cardiovascular reactivity (mean 39.2) compared to subjects with low reactivity (mean 34.5; (F (1,16) = 3.9, p = .065). 3.3. Correlation between interoceptive awareness and anxiety While there was no relation between state anxiety and interoceptive awareness (r = − .15, p = n.s.), we found a significant positive correlation of r = .47 between the heartbeat perception score and the mean trait anxiety score (p b .05). 3.4. Partial correlation analyses between haemodynamic responses to isometric exercise and interoceptive awareness and trait anxiety Because of the positive correlation between interoceptive awareness and trait anxiety, partial correlations were computed between these variables and the haemodynamic responses to isometric exercise. The results and the statistical significances are presented in Table 5.

Table 4 Mean scores in interoceptive awareness and anxiety for all subjects (N = 18) and for subjects with high (N = 9) and low cardiovascular reactivity (N = 9; ⁎: p b .05) Table 2 Mean baseline scores (N = 18; ⁎: p b .05, ⁎⁎: p b .01) contrasting subjects with high (N = 9) and low cardiovascular reactivity (N = 9)

Heart rate (beats per minute) Systolic blood pressure (mm Hg) Diastolic blood pressure (mm Hg) Total peripheral resistance (mm Hg L− 1 min− 1) Stroke volume (ml) Cardiac output (L min− 1) Preejection period (ms)

High reactivity

Low reactivity

T (df = 16)

p

68.2 118.2

67.1 124.6

− 0.3 1.3

n.s. n.s.

63.2

62.4

− 0.2

n.s.

902.2

832.0

− 0.5

n.s.

106.5 6.7 109

117.9 7.0 99.5

1.2 0.4 − 1.5

n.s. n.s. n.s.

Interoceptive awareness Mean (SD) Minimum Maximum State anxiety Mean (SD) Minimum Maximum Trait anxiety Mean (SD) Minimum Maximum

All subjects

High reactivity

Low reactivity

Statistical significance

.82 (.13) .66 .98

.88 (.10) .71 .98

.76 (.06) .66 .90

⁎

34.7 (4.6) 27 45

34.9 (5.3) 27 45

34.6 (4.0) 29 41

n.s.

36.8 (5.4) 27 48

39.2 (4.9) 27 48

34.5 (5.1) 30 45

n.s. (p = .065)

O. Pollatos et al. / International Journal of Psychophysiology 65 (2007) 167–173 Table 5 Partial correlation analyses between mean changes in haemodynamic variables (isometric handgrip exercise minus baseline; N = 18; ⁎: p b .05) and interoceptive awareness controlled for trait anxiety (df = 15) respectively trait anxiety controlled for interoceptive awareness (df = 15)

Δ Heart rate (beats per minute) Δ Systolic blood pressure (mm Hg) Δ Diastolic blood pressure (mm Hg) Δ Total peripheral resistance (mm Hg L− 1 min− 1) Δ Stroke volume (ml) Δ Cardiac output (L min− 1 m− 2) Δ Preejection period (ms)

Partial correlation with interoceptive awareness

Partial correlation with trait anxiety

.42⁎

.29

.52⁎

.35

.35

.23

.21

.46⁎

.22 .43⁎

.30 .02

.45⁎

.51⁎

Interoceptive awareness was significantly correlated with changes in heart rate, systolic blood pressure, cardiac output and preejection period (p b .05) whereas trait anxiety was significantly correlated with changes in total peripheral resistance and preejection period (p b .05). 4. Discussion Sustained isometric handgrip exercise caused significant increases in heart rate, blood pressure and total peripheral resistance, whereas stroke volume, cardiac output and preejection period were decreased. This is consistent with the fact that this task evokes a primarily alpha-adrenergic response pattern (Fontana et al., 2002; Prkachin et al., 2001). Categorizing the subjects depending on their cardiovascular response in high vs. low reactive was associated with differences in observed interoceptive awareness and trait anxiety. Both interoceptive awareness as well as trait anxiety were increased in the group with high cardiovascular reactivity. Additionally, a positive relation between interoceptive awareness and trait anxiety was obtained. The haemodynamic responses, especially heart rate, systolic blood pressure, cardiac output and preejection period, correlated significantly with interoceptive awareness, indicating a close relation between cardiovascular sympathetic responses to physical stress and interoceptive awareness. This result extends data from O'Brien et al. (O'Brien et al., 1998) who reported a relation between systolic blood pressure and the ability to detect one's heartbeats by showing that blood pressure increases during physical stress are also related to higher levels of interoceptive awareness. In line with former studies using exercise tasks with high physical effort (Schandry et al., 1993; Schandry and Bestler, 1995a), we assessed a correlation between contractility measures of the heart like stroke volume or cardiac output and interoceptive awareness. Due to the chosen experimental paradigm, relations to these variables were not as high like described by Schandry and Bestler (Schandry and Bestler, 1995b) who used an experimental procedure where physical load was manipulated in a stepwise way to a maximum level of physical effort. Additionally, we demonstrated for the

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first time that further measures of autonomic reactivity like changes in heart rate and in the preejection period are associated with interoceptive awareness. The present data broaden results with emotional stimuli showing that psychophysiological arousal is related to interoceptive awareness (Pollatos et al., 2005b, 2007a, 2007b, in press; Wiens et al., 2000). Our data suggest that the relation between augmented psychophysiological arousal and interoceptive awareness is not limited to affective stimuli but is also present in situations involving physical stress. We observed a positive relation between interoceptive awareness and trait anxiety which confirms former data showing that subjects with high interoceptive awareness exhibit greater anxiety levels (Critchley et al., 2004; Pollatos et al., 2007b, in press). This result does also fit into research about anxiety disorders where interoceptive awareness was found to be closely associated with many anxiety disorders (Ehlers et al., 2000; Pineles and Mineka, 2005; Roth et al., 1992; Van der Does et al., 2000; Wald and Taylor, 2005; White et al., 2006; Zoellner and Craske, 1999). Interestingly, enhanced cardiovascular reactivity was associated with both higher levels of interoceptive awareness and trait anxiety. Having in mind that many anxiety questionnaires like the used STAI assess introspectively accessible self-descriptions (Egloff and Schmukle, 2002) it is not astonishing that subjects with high interoceptive awareness do also score higher in anxiety measured in the described way. Concerning the present study, positive relations between haemodynamic changes and trait anxiety were assessed even when controlling for interoceptive awareness. Taken all results together we would suggest that besides of a high degree of common variation between interoceptive awareness and trait anxiety cardiovascular reactivity predicts an independent part of both variables. Further research with bigger sample sizes as well as with female subjects are necessary to make more precise predictions about the relationship between cardiovascular reactivity, interoceptive awareness and anxiety. Concerning the used heartbeat detection task, potential weaknesses must be taken in account when assessing interoception. Though this task is widely used (Ehlers et al., 2000; Leopold and Schandry, 2001; Pollatos et al., 2005a,b) there are several studies reporting that these kind of tracking tasks may be influenced by people's beliefs and expectancies about their heart rates (Knapp et al., 1997; Knapp-Kline and Kline, 2005; Wiens and Palmer, 2001; Windmann et al., 1999). Besides of the mentioned expectancies also other factors like attention or motivation may influence the outcome of any heartbeat perception task. Nevertheless, meanwhile there is a convincing body of evidence showing that though using different heartbeat perception tasks congruent results are observed concerning effects of interoception on emotions (Pollatos et al., 2005b, 2007a; Wiens et al., 2000) or localization of relevant brain structures activated during heartbeat perception (Critchley et al., 2004; Pollatos et al., 2005a), supporting the validity of these heartbeat perception tasks in detecting processes involved in interoception (Wiens, 2005). We conclude that cardiovascular reactivity to physical stress is associated with interoceptive awareness and trait anxiety.

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Several limitations of our study must be concerned when generalizing the observed results. First, a relative small sample size was used and only male subjects were investigated. Second, the physical stress level was not systematically manipulated e.g. by a task subsequently increasing physical load. Third, a task evoking a beta-adrenergic response pattern like a mental arithmetic task would provide further information. Fourth, the reliance on one measure of interoceptive awareness as assessed by the heartbeat perception task is a shortcoming of the present work. Future studies which are taking the mentioned limitations into account are required to address the mechanisms responsible for the observed increased cardiovascular reactivity in relation to interoceptive awareness and trait anxiety. Moreover, the potential consequences of excess cardiac sympathetic activity in subjects with high interoceptive awareness like panic patients require further consideration. Acknowledgments This work was partly founded by a grant to Dr. Olga Pollatos by the “Förderung im Rahmen des Hochschul-und Wissenschaftsprogramms (HWP)”. We want to thank Julia König and Katrin Holler for their participation in data managing, Jennifer Bruder, Jana Beil and Anna Nützel for editing the manuscript. References Bernstein, D.P., 1986. A new stroke volume equation for thoracic electrical bioimpedance: theory and rationale. Crit. Care Med. 14, 904–909. Cameron, O.G., 2001. Interoception: the inside story — a model for psychosomatic processes. Psychosom. Med. 63, 697–710. Cameron, O.G., Minoshima, S., 2002. Regional brain activation due to pharmacologically induced adrenergic interoceptive stimulation in humans. Psychosom. Med. 64, 851–861. Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A., Dolan, R.J., 2004. Neural systems supporting interoceptive awareness. Nat. Neurosci. 7, 189–195. Damasio, A.R., 1994. Descartes' Error: Emotion, Reason and the Human Brain. Grosset/Putman, New York. Damasio, A.R., 1999. The feeling of what happens: Body and Emotion in the Making of Consciousness. Harcourt Brace, New York. Dunn, B.D., Dalgleish, T., Ogilvie, A.D., Lawrence, A.D., in press. Heartbeat perception in depression. Behav. res. ther. doi:10.1016/j.brat.2006.09.008. Egloff, B., Schmukle, S.C., 2002. Predictive validity of an implicit association test for assessing anxiety. J. Pers. Soc. Psychol. 83, 1441–1455. Ehlers, A., 1995. A 1-year prospective study of panic attacks: clinical course and factors associated with maintenance. J. Abnorm. Psychology 104, 164–172. Ehlers, A., Margraf, J., Roth, W.T., 1992. Imipramine and alprazolam effects on stress test reactivity in panic disorder. Biol. Psychiatry 31, 35–51. Ehlers, A., Mayou, R.A., Sprigings, D.C., Birkhead, J., 2000. Psychological and perceptual factors associated with arrhythmias and benign palpitations. Psychosom. Med. 62, 693–702. 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. Behav. Res. Ther. 42, 439–448. Fontana, G.A., Pantaleo, T., Lavorini, F., Bongianni, F., Mannelli, M., Bridge, P.D., Pistolesi, M., 2002. Handgrip-induced airway dilation in asthmatic patients with bronchoconstriction induced by MCh inhalation. J. Appl. Physiol. 93, 1723–1730. Friedman, B.H., Thayer, J.F., 1998. Anxiety and autonomic flexibility: a cardiovascular approach. Biol. Psychol. 49, 303–323.

Gurguis, G.N.M., Vitton, B.J., Uhde, T.W., 1997. Behavioral, sympathetic and adrenocortical responses to yohimbine in panic disorder patients and normal controls. Psychiatry Res. 71, 27–39. James, W., 1884. What is an emotion? Mind 9, 188–205. Jones, G.E., Leonberger, T.F., Rouse, C.H., Caldwell, J.A., Jones, K.R., 1986. Preliminary data exploring the presence of an evoked potential associated with cardiac visceral activity. Psychophysiology 23. Knapp, K., Ring, C., Brener, J., 1997. Sensitivity to mechanical stimuli and the role of general sensory and perceptual processes in heartbeat detection. Psychophysiology 34, 467–473. Knapp-Kline, K., Kline, J.P., 2005. Heart rate, heart rate variability, and heartbeat detection with the method of constant stimuli: slow and steady wins the race. Biol. Psychol. 69, 387–396. Leopold, C., Schandry, R., 2001. The heartbeat-evoked brain potential in patients suffering from diabetic neuropathy and in healthy control persons. Clin. Neurophysiol. 112, 674–682. Lovallo, W.R., Pincomb, G.A., Sung, B.H., Wilson, M.F., 1993. Impedance cardiography used to assess patterns of cardiovascular response to behavioral stressors. Biol. Psychiatry 36, 97–105. Matthews, K.A., Salomon, K., Brady, S.S., Allen, M.T., 2003. Cardiovascular reactivity to stress predicts future blood pressure in adolescence. Psychosom. Med. 65, 410–415. Mauss, I.B., Wilhelm, F.H., Gross, J.J., 2003. Autonomic recovery and habituation in social anxiety. Psychophysiology 40, 648–653. Monk, C., Kovelenko, P., Ellman, L.M., Sloan, R.P., Bagiella, E., Gorman, J.M., Pine, D.S., 2001. Enhanced stress reactivity in paediatric anxiety disorders: implications for future cardiovascular health. Int. J. Neuropsychopharmacol. 4, 199–206. O'Brien, W.H., Reid, G.J., Jones, K.R., 1998. Differences in heartbeat awareness among males with higher and lower levels of systolic blood pressure. Int. J. Psychophysiol. 29, 53–63. Panknin, T.L., Dickensheets, S.L., Nixon, S.J., Lovallo, W.R., 2002. Attenuated heart rate responses to public speaking in individuals with alcohol dependence. Alcohol Clin. Exp. Res. 26, 841–847. Pineles, S.L., Mineka, S., 2005. Attentional biases to internal and external sources of potential threat in social anxiety. J. Abnorm. Psychology 114, 314–318. Pollatos, O., Schandry, R., 2004. Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology 41, 476–482. Pollatos, O., Kirsch, W., Schandry, R., 2005a. Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study. Hum. Brain Mapp. 26, 54–64. Pollatos, O., Kirsch, W., Schandry, R., 2005b. On the relationship between interoceptive awareness, emotional experience, and brain processes. Cogn. Brain Res. 25, 948–962. Pollatos, O., Gramann, K., Schandry, R., 2007a. Neural systems connecting interoceptive awareness and feelings. Hum. Brain Mapp. 28, 9–18. Pollatos, O., Herbert, B.M., Matthias, E., Schandry, R., 2007b. Heart rate response after emotional picture presentation is modulated by interoceptive awareness. Int. J. Psychophysiol. 63, 117–124. Pollatos, O., Traut-Mattausch, E., Schroeder, H., Schandry, R., in press. Interoceptive awareness mediates the relationship between anxiety and the intensity of unpleasant feelings. J. Anxiety Disord. doi:10.1016/j. janxdis.2006.12.004. Prkachin, K.M., Mills, D.E., Zwaal, C., Husted, J., 2001. Comparison of hemodynamic responses to social and nonsocial stress: Evaluation of an anger interview. Psychophysiology 38, 879–885. Richards, J.C., Bertram, S., 2000. Anxiety sensitivity, state and trait anxiety, and perception of change in sympathetic nervous system arousal. J. Anxiety Disord. 14, 413–427. Roth, W.T., Margraf, J., Ehlers, A., Taylor, G.J., Maddock, R.J., Davies, S., Agras, W.S., 1992. Stress test reactivity in panic disorder. Arch. Gen. Psychiatry 49, 301–310. Rowell, L.B., Sheriff, D.D., 1988. Are muscle “chemoreflexes” functionally important? News Physiol. Sci. 3, 250–253. Schachter, S., Singer, J.E., 1962. Cognitive, social and physiological determinants of emotional state. Psychol. Rev. 69, 379–399.

O. Pollatos et al. / International Journal of Psychophysiology 65 (2007) 167–173 Schandry, R., Bestler, M., 1995a. Cardiovascular function and heartbeat perception. In: Vaitl, D.S.R. (Ed.), Peter Lang, Frankfurt a. Main. Schandry, R., Bestler, M., 1995b. The association between parameters of cardiovascular functioning and heartbeat perception. Peter Lang, Frankfurt A.M. Schandry, R., Bestler, M., Montoya, P., 1993. On the relation between cardiodynamics and heartbeat perception. Psychophysiology 30, 467–474. Scherhag, A.W., Pfleger, S., deMey, C., Schreckenberger, A.B., Staedt, U., Heene, D.L., 1997. Continuous measurement of hemodynamic alterations during pharmacologic cardiovascular stress using automated impedance cardiography. J. Clin. Pharmacol. 37, 21–28. Silke, B., McAuley, D., 1998. Accuracy and precision of blood pressure determination with the Finapres: an overview using re-sampling statistics. J. Hum. Hypertens. 12, 403–409. Spielberger, C.D., Gorsuch, R.C., Lushene, R.E., Vagg, P.R., Jacobs, G.A., 1983. Manual for the State-Trait Anxiety Inventory. Consulting Psychologist Press, Palo-Alto, CA. Takahashi, T., Ikeda, K., Ishikawa, M., Kitamura, N., Tsukasaki, T., Nakama, D., Kameda, T., 2005. Anxiety, reactivity, and social stress-induced cortisol elevation in humans. Neuro Endocrinol. Lett. 26, 351–354. Van der Does, A.J.W., Antony, M.M., Ehlers, A., Barsky, A.J., 2000. Heartbeat perception in panic disorder: a reanalysis. Behav. Res. Ther. 38, 47–62.

173

Wald, J., Taylor, S.F., 2005. Interoceptive exposure therapy combined with trauma-related exposure therapy for post-traumatic stress disorder: a case report. Cogn. Behav. Ther. 34, 34–40. White, K.S., Brown, T.A., Somers, T.J., Barlow, D.H., 2006. Avoidance behavior in panic disorder: the moderating influence of perceived control. Behav. Res. Ther. 44, 147–157. Whitehead, W.E., Drescher, V.M., 1980. Perception of gastric contractions and self-control of gastric motility. Psychophysiology 17, 552–558. Wiens, S., 2005. Interoception in emotional experience. Curr. Opin. Neurol. 18, 442–447. Wiens, S., Palmer, S.N., 2001. Quadratic trend analysis and heartbeat detection. Biol. Psychol. 58, 159–175. Wiens, S., Mezzacappa, E.S., Katkin, E., 2000. Heartbeat detection and the experience of emotions. Cogn. Emot. 14, 417–427. Windmann, S., Schonecke, O.W., Fröhlig, G., Maldener, G., 1999. Dissociating beliefs about heart rates and actual heart rates in patients with cardiac pacemakers. Psychophysiology 36, 339–342. Zoellner, L.A., Craske, M.G., 1999. Interoceptive accuracy and panic. Behav. Res. Ther. 37, 1141–1158.