Elsevier

Cognitive Brain Research

Volume 25, Issue 3, December 2005, Pages 948-962
Cognitive Brain Research

Research Report
On the relationship between interoceptive awareness, emotional experience, and brain processes

https://doi.org/10.1016/j.cogbrainres.2005.09.019Get rights and content

Abstract

The perception of visceral signals plays a crucial role in many theories of emotions. The present study was designed to investigate the relationship between interoceptive awareness and emotion-related brain activity. 44 participants (16 male, 28 female) first underwent a heartbeat perception task and then were categorised either as good (n = 22) or poor heartbeat perceivers (n = 22). A total of 60 different pictures (pleasant, unpleasant, neutral) from the International Affective Picture System served as emotional stimuli. EEG (61 electrodes) and EOG were recorded during slide presentation. After each slide, the subjects had to rate emotional valence and arousal on a 9-point self-report scale. Good heartbeat perceivers scored the emotional slides significantly more arousing than poor heartbeat perceivers; no differences were found in the emotional valence ratings. The visually evoked potentials of good and poor heartbeat perceivers showed significant differences in the P300 and in the slow-wave latency ranges. Statistical analyses revealed significantly higher P300 mean amplitudes for good heartbeat perceivers (averaged across all 60 slides) than for poor heartbeat perceivers. In the slow-wave range, this effect was found for affective slides only. Heartbeat perception scores correlated significantly and positively with both the mean arousal rating as well as with the mean amplitudes in the P300 time window and the slow-wave window. Our results demonstrate a strong relationship between the perception of cardiac signals and the cortical processing of emotional stimuli, as would be postulated for example by the James–Lange theory of emotions.

Introduction

The perception of signals arising from the body plays an important role in many theories of emotions (so-called peripheral theories of emotions). Well-known examples are the theories by James [40], Schachter and Singer [70] and Damasio [29]. William James postulated 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” [40] The James theory is often referred to as the James–Lange theory due to the fact that Carl Lange, a Danish psychologist, proposed a similar theory in 1885[56]. However, Lange's theory used substantially more physiological reasoning as opposed to psychological reasoning. The theory of James is still under investigation today and continues to be a topic of debate [4], [30], [53], [66]. Schachter and Singer [70] agreed with James insofar as that visceral arousal is seen as a prerequisite for emotional experience. However, they emphasised the importance of cognitive attributions for the quality of the resulting emotional state. An example for a recent psychological theory incorporating the feedback from the peripheral nervous system (somatosensory and visceral) is the somatic marker hypothesis by Damasio and colleagues [1], [2], [6], [25], [26], [28], [82]. The authors speak of the obligatory body-relatedness of feeling: “the body is the main stage for emotions, either directly or via its representations in somatosensory structures of the brain” (p. 287, [27]). Furthermore, it is pointed out [27] that the described mechanisms to engage in emotional behaviour are compatible with James' view, thereby adding a new dimension by stating that “the emotional responses target both the body proper and the brain”.

James [40] stated that feelings originate from the perception of bodily states. Following this assumption, one may conclude that the extent of a person's sensitivity to bodily signals (“interoceptive awareness”, “visceral perception”) should be related to the experienced intensity of emotions. Individual differences in visceral perception have often been assessed by focussing on the cardiovascular system, and especially on the perception of heartbeats. Different heartbeat perception tasks have been developed and are widely used [11], [12], [57], [64], [71], [74], [83], [85], [89]. Substantial interindividual differences in heartbeat perception assessed under resting conditions have been shown in several studies [41], [45], [58], [64], [71], [72], [74], [86], [87], [91]. Subjects with good heartbeat perception – from the described viewpoint of peripheral theories of emotions – should experience emotions more intensely due to their heightened ability to perceive their bodily states. Most of the studies addressing this question found a positive relationship between heartbeat perception and emotional experience [22], [31], [58], [71], [89]. Blascovich et al. [8], however, found a negative relationship between a questionnaire measure of affect intensity and heartbeat detection.

A direct consequence of the increased emotional experience of persons with good heartbeat perception pertains to emotion-related brain processes. It has to be assumed that brain structures, which are related to the processing of emotional stimuli, will reveal an enhanced activity in persons with good heartbeat perception as compared to those with poor heartbeat perception. These structures should be of relevance for both heartbeat perception and emotional experience and thus serve as an interface between the perception of bodily signals and the processing of emotional stimuli on the input side, and emotional experience on the output side.

Research performed with PET and fMRI has shown that cerebral processing of emotions involves structures that are also dealing with the regulation of bodily states: Damasio et al. [28] found that during the feeling of self-generated emotions, the somatosensory cortices, the insula, the anterior and posterior cingulated cortex, and nuclei in the brainstem are activated. Their findings are consistent with anatomic evidence that these regions are direct or indirect recipients of signals from the internal milieu and viscera [60]. In the framework of Rolls [67], the orbitofrontal cortex, the somatosensory cortex and the amygdala are important structures for the processing of emotions. Some evidence exists for the right insula to play an important role in connecting emotional experience with interoceptive awareness [18], [22], [36], [38], [39], [49], [75]. In a recent fMRI study, Critchley et al. [22] could demonstrate that state anxiety was correlated with both interoceptive awareness as measured through a heartbeat perception task and the BOLD activity in the right insula. Taking these lines of research together, one might speculate that there are certain brain regions that both monitor the ongoing internal emotional state of the organism and are involved in the processing of emotions.

Event related potentials (ERPs) of the EEG allow the investigation of the topographic distribution of cortical activity and the time course of the brain responses following the perception of emotional stimuli. Brain electrical responses to emotional stimuli have frequently been studied by using affective pictures as stimuli (e.g., [10], [16], [23], [24], [34], [35], [48], [59], [77], [84]). One major finding is a greater magnitude of the P300 amplitude in response to pictures with emotional content as compared to neutral pictures. The P300 component is assumed to be an index of attention, processing capacity, motivational relevance, and task difficulty. It appears as a relatively large, distinct positive wave, peaking from approximately 300 ms to 600 ms post stimulus, depending on the specific experimental manipulations [43], [50], [63], [78]. Besides the P300, the so-called late-positive slow wave (a sustained late positive wave at 400 ms and beyond) shows sensitivity to emotional picture contents [24], [29], [48], [59]. It is assumed that the positive slow wave reflects the continued perceptual processing of emotional information [24], [50].

The enhanced brain electrical activity during viewing of pleasant and unpleasant pictures may indicate that emotional stimuli are processed preferentially [48], [55]. This assumption is in accordance to many theorists who claim that the affect system has evolved from a motivational basis [35]. Biphasic theories of emotions describe emotions on the two dimensions pleasantness, respectively, valence and arousal [35], [54], [55]. While pleasantness stands for the quality of emotions, emotional arousal refers to the intensity of mobilization or energy [35]. In many studies, both dimensions were assessed by self-report measures and physiological variables like evoked potentials, heart rate or skin conductance (see [24]). Generally, affective pictures are rated as more arousing than neutral ones (e.g. [54]). Concerning the interaction between evoked potentials and arousal, Polich and Kok [63] pointed out that the P300 is influenced by biological processes like the arousal state of subjects assessed by physiological performance or self-report measures. In accordance to this assumption Cuthbert et al. [24] showed that late positive potentials (e.g., 700–1000 ms post-stimulus) are specifically enhanced by pictures that are rated as more arousing. Also, Keil et al. [47] showed a modulation of late positive ERPs as a function of emotional arousal. Having in mind that former studies have shown an interaction between interoceptive awareness and the experienced intensity of emotions on the level of verbal report [22], [31], [58], [71], [89], one can assume that these observed differences in self-reported arousal correspond with analogous differences measured by evoked potentials. Especially the P300 component and the slow wave of the ERP, elicited by emotional stimuli, may be components sensitive for a modulation by interoceptive awareness.

The present study was designed primarily to investigate the cortical processes that are related to both interoceptive awareness and emotion-related brain activity. Thus, for good and poor heartbeat perceivers, visual evoked potentials elicited by emotional stimuli were analysed together with self-rated emotional experience.

In detail, the following hypotheses were examined:

  • (1)

    Subjects who perceive their heartbeats with high accuracy show higher arousal ratings to affective pictures.

  • (2)

    The heartbeat perception score and the subjective arousal rating are positively correlated.

  • (3)

    Good heartbeat perceivers display an enhancement in the P300 and slow wave components elicited by emotionally arousing pictures.

  • (4)

    The heartbeat perception score and the mean amplitude in the P300 time window as well as in the slow wave window are positively correlated.

Section snippets

Subjects

The sample consisted of 44 students (16 male, 28 female) from the University of Munich. Subjects received €30 (about $30) for their participation. The mean age was 25.5 (SD 4.5) years ranging from 18 to 36 years of age. Subjects were recruited in such a manner that both groups (good/poor heartbeat perceivers) were composed of 22 participants with an equal number of males (8) and females (14). Specifically, we used a screening test and assessed heartbeat perception in about 140 subjects.

Heartbeat perception

A heartbeat perception score was calculated as the mean score of eleven heartbeat perception intervals according to the following transformation:FORMULA:1/11Σ(1(|recordedheartbeatscountedheartbeats|)/recordedheartbeats)

The mean heartbeat perception score was 0.78 (SD 0.19; minimum 0.19; maximum 0.98). Female subjects had a mean heartbeat perception score of 0.77 (SD 0.21; minimum 0.13; maximum 0.98), male subjects of 0.80 (SD 0.14; minimum 0.52; maximum 0.96). There was no significant

Discussion

In this experiment, the VEPs to emotional stimuli were recorded and analysed focussing on the role of heartbeat perception on both emotion-related brain activity and experienced emotional arousal. In accordance with our hypotheses, the ability to perceive one's heartbeats accurately had a major influence both on the VEPs and the reported arousal. Moreover, we observed significant positive correlations between the heartbeat perception score and both the mean SAM arousal rating scores and the

Acknowledgment

This study was partly founded by a grant to Dr. Olga Pollatos by the Bavarian State Ministry of Sciences, Research and the Arts.

References (91)

  • P. Montoya et al.

    Heart-beat evoked potentials (HEP): topography and influence of cardiac awareness and focus of attention

    Electroencephalogr. Clin. Neurophysiol.

    (1993)
  • D. Palomba et al.

    Visual evoked potentials, heart rate responses and memory to emotional picturial stimuli

    Int. J. Psychophysiol.

    (1997)
  • K.L. Phan et al.

    Functional neuroanatomy of emotional activation studies in PET and fMRI

    NeuroImage

    (2002)
  • J. Polich et al.

    Cognitive and biological determinants of P300: an integrative review

    Biol. Psychol.

    (1995)
  • R. Schandry et al.

    Event-related brain potentials and the processing of cardiac activity

    Biol. Psychol.

    (1996)
  • B.D. Smith et al.

    The lateralized processing of affect in emotionally labile extraverts and introverts: central and autonomic effects

    Biol. Psychol.

    (1995)
  • G. Spangler et al.

    The specificity of infant emotional expression for emotion perception

    Int. J. Psychophysiol.

    (2001)
  • A.A. Stevens et al.

    Event-related fMRI of auditory and visual oddball tasks

    Magn. Reson. Imaging

    (2000)
  • I.M. Tarkka et al.

    Generaotrs for human P300 elicited by somatosensory stimuli using multiple dipole source analysis

    Neuroscience

    (1996)
  • S.R. Waldstein et al.

    Frontal electrocortical and cardiovascular reactivity during happiness and anger

    Biol. Psychol.

    (2000)
  • R. Adolphs et al.

    Fear and the human amygdala

    J. Neurosci.

    (1995)
  • R. Adolphs et al.

    A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping

    J. Neurosci.

    (2000)
  • P. Anderer et al.

    Electrical sources of P300 event-related brain potentials revealed by low resolution electromagnetic tomography

    Neuropsychobiology

    (1998)
  • J.M. Barbalet

    William James' theory of emotions: filling in the picture

    J. Theor. Soc. Behav.

    (1999)
  • A. Bechara et al.

    Deciding advantageously before knowing the advantageous strategy

    Science

    (1997)
  • A. Bechara et al.

    Emotion, decision making and the orbitofrontal cortex

    Cereb. Cortex

    (2000)
  • J. Blascovich et al.

    Affect intensity and cardiac arousal

    J. Pers. Soc. Psychol.

    (1992)
  • M.M. Bradley et al.

    Measuring emotions: the self-assessment manikin and the semantic differential

    J. Behav. Exp. Psychiatry

    (1994)
  • M.M. Bradley et al.

    Affective picture processing

  • J. Brener et al.

    Heartbeat detection: judgments of the simultaneity of external stimuli and heartbeats

    Psychophysiology

    (1988)
  • J. Brener et al.

    A method of constant stimuli for examining heartbeat detection: comparison with the Brener–Kluvitse and Whitehead methods

    Psychophysiology

    (1993)
  • T. Cacioppo et al.

    What is an emotion? The role of somatovisceral “illusions”

    Rev. Pers. Soc. Psychol.

    (1992)
  • O.G. Cameron

    Interoception: the inside story—A model for psychosomatic processes

    Psychosom. Med.

    (2001)
  • T. Canli et al.

    An fMRI study of personality influences on brain reactivity to emotional stimuli

    Behav. Neurosci.

    (2001)
  • The International Affective Picture System (IAPS): Technical Manual and Affective Ratings

    (1999)
  • A.D. Craig

    How do you feel? Interoception: the sense of the physiological condition of the body

    Nat. Rev., Neurosci.

    (2002)
  • H.D. Critchley et al.

    Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans

    J. Physiol.

    (2000)
  • H.D. Critchley et al.

    Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study

    J. Neurosci.

    (2000)
  • H.D. Critchley et al.

    Neuroanatomic basis for first- and second-order representations of bodily states

    Nat. Neurosci.

    (2001)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nat. Neurosci.

    (2004)
  • B.N. Cuthbert et al.

    Probing picture perception: activation and emotion

    Psychophysiology

    (1996)
  • A.R. Damasio. Descartes`Error: Emotion, Reason and the Human Brain. Grosset/Putman, New York,...
  • R. Damasio

    Emotion in the perspective of an integrated nervous system

    Brain Res. Rev.

    (1998)
  • A.R. Damasio

    The Feeling of What Happens: Body, Emotion and the Making of Consciousness

    (2000)
  • A.R. Damasio et al.

    Subcortical and cortical brain activity during the feeling of self-generated emotions

    Nat. Neurosci.

    (2000)
  • Cited by (242)

    • The neurobiology of interoception and affect

      2024, Trends in Cognitive Sciences
    • The renin-angiotensin system, emotional stress and anxiety

      2023, Angiotensin: From the Kidney to Coronavirus
    • Interoceptive attention facilitates emotion regulation strategy use

      2023, International Journal of Clinical and Health Psychology
    View all citing articles on Scopus
    View full text