Basic emotions are associated with distinct patterns of cardiorespiratory activity

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Abstract

The existence of specific somatic states associated with different emotions remains controversial. In this study, we investigated the profile of cardiorespiratory activity during the experience of fear, anger, sadness and happiness. ECG and respiratory activity was recorded in 43 healthy volunteers during the recall and experiential reliving of one or two potent emotional autobiographical episodes and a neutral episode. Univariate statistics indicated that the four emotions differed from each other and from the neutral control condition on several linear and spectral indices of cardiorespiratory activity. Dependent variables were further reduced to five physiologically meaningful factors using an exploratory principal component analysis (PCA). Multivariate analyses of variance and effect size estimates calculated on those factors confirmed the differences between the four emotion conditions. A stepwise discriminant analyses predicting emotions using the PCA factors led to a classification rate of 65.3% for the four emotions (chance = 25%; p = 0.001) and of 72.0–83.3% for pair-wise discrimination (chance = 50%; p's < 0.05). These findings may be considered preliminary in view of the small sample on which the multivariate approach has been applied. However, this study emphasizes the need to better characterize the multidimensional factors involved in cardio-respiratory regulation during emotion. These results are consistent with the notion that distinct patterns of peripheral physiological activity are associated with different emotions.

Introduction

There is a long history of debates surrounding the role of somatic states in emotions. William James proposed in 1894 (James, 1994) that the felt afferent signals from the viscera are essential for the unique experience associated with distinct emotions. In contrast, Cannon (1987) proposed that the slow, diffuse, and unspecific, visceral activity could not be the source for the qualities of felt emotions (also see Cannon, 1931). The contribution of cognitive factors was later emphasized in theories in which peripheral activity only contributed to the felt level of arousal and not to the quality of the emotion experienced (Schacter and Singer, 1962). One of the central questions raised by this debate is the role of somatic states, constituted by endocrine, visceral, musculoskeletal, and behavioral response, in the experience of emotions. Indeed, while James' original theoretical proposal requires that emotions be associated with distinct patterns of somato-visceral activity, the cognitive perspective implies that the peripheral activation associated with emotions can be reduced to a single dimension. Here, we revisited James' hypothesis using cardiorespiratory measures.

Previous studies have provided some evidence for James' view. Specific patterns of autonomic activity have been reported across individuals during the voluntary production of emotional facial expressions (Ekman et al., 1983; see also Levenson et al., 1990), and in response to visual (Collet et al., 1997), olfactory stimuli (Vernet-Maury et al., 1999), and film clips (Christie and Friedman, 2004). However, based on a meta-analysis of the studies investigating the physiological responses observed during basic emotions evoked using a variety of methods, Cacioppo and his colleagues concluded that the literature provided only equivocal evidence for the existence of distinct patterns of peripheral activity associated with basic emotions (Cacioppo et al., 2000). Although this conclusion may be regarded as particularly conservative in view of the evidence already available, it nonetheless suggested the need for additional investigations of somatic states associated with emotions.

There are at least two reasons for the limited success in uncovering distinctive physiological patterns associated with basic emotions: the inadequate experimental elicitation of the target emotions and the incomplete physiological characterization of the ensuing somatic states. The first limitation may be surmounted by acquiring and analyzing physiological data when subjects actually report feeling the emotions, rather than simply relying on stimulus or task-related criterion. Here, we use data obtained when subjects reported feeling a target emotion in a paradigm involving the autobiographical recall and on-line “reliving” of target emotions. This method has been effective in demonstrating some level of discrimination between basic emotions based on autonomic measurements in previous studies (e.g. Ekman et al., 1983). Improvements in the characterization of emotion-related physiological activity may be achieved by measuring additional physiological signals or by refining the analysis of commonly used physiological measures. In the present study, we took this latter approach and applied modern chronometric measurement techniques to assess cardiorespiratory activity during emotional states.

One of the conclusions of the meta-analysis of Cacioppo et al. (2000) was that a better characterization of sympathetic and parasympathetic responses may provide some discriminative power to distinguish patterns of visceral activity associated with basic emotions. A number of non-invasive computational techniques have been developed over the recent decades to characterize the autonomic processes involved in the chronometric regulation of cardiac function (e.g. Task force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, 1996, Berntson et al., 1993b, Malliani et al., 1991, Pagani et al., 1997). These techniques provide estimates of the relative contribution of the parasympathetic and sympathetic branches of the autonomic nervous system by assessing changes in heart rate variability (HRV). A continuous tachogram can be derived from the ECG by calculating the successive intervals between R-waves. From the resulting RR-tachogram, one can extract several indices of HRV based on linear calculations (time-domain measures such as the standard-deviation of RR intervals for a given epoch and the mean absolute difference between successive RR intervals). The RR-tachogram can also be analysed using Fast-Fourier Transform (FFT) methods to derive indices of HRV in specific frequency bands (frequency-domain measures such as the spectral power in the high frequency range).

Parasympathetic regulation is mediated by the vagus nerve and by the release of acetylcholine (Ach) at the neuro-muscular junction. This system is relatively rapid because the Ach is quickly degraded by acetylcholinesterase in the extracellular compartment (Talman and Kelkar, 1993). The dynamic regulation of vagal tone can therefore be indexed by a number of chronometric variables sensitive to high frequency changes in the RR interval. By contrast, sympathetic regulation relies upon the release and relatively slow re-uptake of adrenaline. The difference in the dynamics of parasympathetic and sympathetic systems implies that the rapid changes in heart rate are mediated by parasympathetic activity while slow changes can result from either sympathetic or parasympathetic activity. Rapid changes in heart rate are further coupled, in part, with changes in respiration because the increase in intra-abdominal pressure during inhaling activates the baroreceptor reflex and produces rapid increases in heart rate mediated by vagal mechanisms. The resulting respiratory sinus arrhythmia (RSA), typically observed in normal cardiac activity, can be characterized by the amplitude of changes in heart rate within each respiratory cycle, and generally contributes to the high frequency components of HRV. Based on these observations, several dependent measures, more or less sensitive and specific to various aspects of cardio-respiratory control, can be extracted from continuous recordings of cardiac and respiratory signals. These measurements reflect three component of autonomic regulation: (1) a sympathetic component; (2) a parasympathetic component coupled with respiration (RSA) and reactive to baroreceptor reflex activity; and (3) a parasympathetic component independent from respiration and possibly reflecting top-down neural influences on vagal output.

The experience of several basic emotions has been consistently associated with changes in heart rate (Cacioppo et al., 2000). By contrast, the contribution of heart rate variability to emotions has been documented mostly in fear. For example, panic attacks have been associated with higher heart rate levels coupled with robust decreases in HRV (Yeragani et al., 1991, Friedman and Thayer, 1998, Rao and Yeragani, 2001, George et al., 1989, Yeragani et al., 1994b). However, it is not clear whether those reductions in HRV are simply secondary to changes in respiration (e.g. hyperventilation) and thus reflect changes mediated by the baroreceptor reflex as the breathing pattern changes. Few studies have examined specifically the effect of other emotions on HRV. Exceptions include a study suggesting that the increase in heart rate during anger reflects mainly a sympathetic activation characterized by a relative increase in the low frequency range of HRV, while positive emotions may be associated with a shift towards the high frequency range (McCraty et al., 1995).

In the present study, we tested the contribution of cardiorespiratory activity to the production of distinct somatic states associated with the feeling of different emotions in normal human volunteers. We hypothesized that (1) cardiorespiratory activity associated with emotions can be characterized along the dimensions of sympathetic and parasympathetic influences, and that the latter factor can be further sub-divided into respiration-coupled and respiration-uncoupled components; and that (2) specific basic emotions can be predicted from the observed pattern of cardiorespiratory activity. In order to facilitate the observation of robust and sustained emotions, we relied on a self-induction paradigm in which subjects vividly recalled an autobiographical episode that elicited a strong emotion and we analyzed cardiac and respiratory activity recorded immediately after the subjects indicated starting to feel the emotion. This paradigm has demonstrated its effectiveness in producing robust and partly segregate patterns of brain activity associated with fear, anger, sadness and happiness (Damasio et al., 2000). We extracted several measures of heart rate, respiratory period and relative respiratory amplitude, as well as indices of variability in both heart rate and respiration. Since many of those measures were expected to be partly redundant, we applied an exploratory principal component analysis (PCA) to reduce the number of dependent variables and extract possible orthogonal factors. This analysis should be considered exploratory in view of the small sample size on which it is applied. The independent factors extracted form the PCA were used in discriminant analyses to test the possibility that the emotion experienced can be predicted by changes along those distinct dimensions of cardiorespiratory activity.

Section snippets

Subjects

Forty-three healthy volunteers were recruited from the University of Iowa Hospitals and Clinics and the University of Iowa students and staff. Subjects were first contacted by phone and were scheduled to participate in the experiment if they could vividly remember one or two autobiographical episodes where they experienced a strong emotion of fear, anger, sadness, or happiness. All procedures were approved by the Internal Review Board of the Human Subjects Office of the University of Iowa

Self-reports of emotions

Subjects reported experiencing the target emotion more intensely than any other emotion in all trials. The mean (sd) Likert-scale rating of the target emotion was 2.29 (0.64) for fear, 3.03 (0.86) for anger, 3.25 (0.70) for sadness, and 3.00 (0.67) for happiness. The target emotion was always felt more intensely than any emotion reported in the neutral condition for which the pooled mean rating of all the emotions reported was 0.40 (0.71) with a median and a mode of 0 (paired t-tests comparing

Discussion

This study provides some evidence that basic emotions are associated with distinctive patterns of cardiorespiratory activity. Different emotions were distinguished from the neutral control condition based on different subsets of dependent variables and multi-dimensional exploration of the data revealed complex patterns of activity that characterized each emotion. The exploratory PCA suggested that the variance in cardiorespiratory activity varied along five dimensions and discriminative

Conclusion

The hypothesis that the feeling of basic emotions is consistently associated with distinct patterns of somatic activity is receiving increasing support from psychophysiological research. The implication of our findings validates the recommendation of a growing number of independent investigators, according to which a multidimensional assessment of physiological activity is necessary to describe somatic states associated with basic emotions. Our results further indicate a contribution of dynamic

Acknowledgments

We thank Daniel Tranel for his advice on psychophysiological methods and analysis, Anne Virasith and Martin Bilodeau for their guidance in the application and interpretation of discriminant analyses, and Don C. Fowles for his constructive comments on the manuscript. Supported in part by grants from the Mathers Foundation and NIH (NINDS) Grant 5 PO 1 NS19632-23, by the Human Frontier Science Program (long-term fellowship to PR) and by the Quebec FRSQ (PR).

References (55)

  • W.T. Talman et al.

    Neural control of the heart: central and peripheral

    Neurol. Clin.

    (1993)
  • M. Toichi et al.

    A new method of assessing cardiac autonomic function and its comparison with spectral analysis and coefficient of variation of R–R interval

    J. Auton. Nerv. Syst.

    (1997)
  • E. Vernet-Maury et al.

    Basic emotions induced by odorants: a new approach based on autonomic pattern results

    J. Auton. Nerv. Syst.

    (1999)
  • C.J. Wientjes

    Respiration in psychophysiology: methods and applications

    Biol. Psychol.

    (1992)
  • V.K. Yeragani et al.

    Heart rate variability in patients with major depression

    Psychiatry Res.

    (1991)
  • V.K. Yeragani et al.

    Sodium lactate increases sympathovagal ratios in normal control subjects: spectral analysis of heart rate, blood pressure, and respiration

    Psychiatry Res.

    (1994)
  • V.K. Yeragani et al.

    Sodium lactate increases sympathovagal ratios in normal control subjects: spectral analysis of heart rate, blood pressure, and respiration

    Psychiatry Res.

    (1994)
  • A. Bechara et al.

    Listening to your heart: interoceptive awareness as a gateway to feeling

    Nat. Neurosci.

    (2004)
  • G.G. Berntson et al.

    ECG artifacts and heart period variability: don't miss a beat

    Psychophysiology

    (1998)
  • G.G. Berntson et al.

    Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications

    Psychophysiology

    (1993)
  • G.G. Berntson et al.

    Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications

    Psychophysiology

    (1993)
  • G.G. Berntson et al.

    Autonomic space and psychophysiological response

    Psychophysiology

    (1994)
  • G.C. Butler et al.

    Heart rate variability and fractal dimension during orthostatic challenges

    J. Appl. Physiol.

    (1993)
  • J.T. Cacioppo et al.

    The psychophysiology of emotion

  • W.B. Cannon

    Again the James–Lange and the thalamic theories of emotion

    Psychol. Rev.

    (1931)
  • W.B. Cannon

    The James–Lange theory of emotions: a critical examination and an alternative theory. By Walter B. Cannon, 1927

    Am. J. Psychol.

    (1987)
  • J. Cohen

    Statistical power analysis for the behavioral sciences

    (1988)
  • Cited by (0)

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