Elsevier

Brain Research

Volume 1141, 13 April 2007, Pages 178-187
Brain Research

Research Report
Brain structures mediating cardiovascular arousal and interoceptive awareness

https://doi.org/10.1016/j.brainres.2007.01.026Get rights and content

Abstract

Different emotions are accompanied by different bodily states and it is unclear which brain structures are involved in both, the cerebral representation of the bodily change and the representation of its perception. Structures connecting bodily signals and interoceptive awareness could trigger, in a feedforward manner, behavioral responses appropriate to maintain a desired state of the cardiovascular system. The present functional magnetic resonance imaging study aimed at identifying brain structures that are mutually activated during interoceptive awareness of heartbeats and during cardiovascular arousal. Additionally, we searched for brain regions connecting interoception with feelings. During the interoceptive task (directing attention towards heartbeats in relation to an exteroceptive task) the thalamus, the insula, the medial frontal/dorsal cingulate and the inferior frontal gyrus, as well as the somatomotor cortex were activated. The conjunction of the interoceptive awareness of heartbeats and cardiovascular arousal revealed structures presumably connecting both conditions, i.e. the right thalamus, insula, somatomotor cortex, and the dorsal cingulate as well as medial frontal gyrus. Furthermore, the degree of interoceptive awareness predicted the degree of activation of both the insula and the medial frontal/dorsal cingulate gyrus. Negative feelings correlated with the BOLD response of the interoceptive awareness condition in the dorsal cingulate gyrus extending into the dorsomedial prefrontal cortex. We provide evidence that the insula, the dorsal cingulate gyrus, and the dorsomedial prefrontal cortex are specifically involved in processing cardiac sensations. The dorsal cingulate gyrus and the dorsomedial prefrontal cortex presumably represent the neural substrates of experiencing negative emotions.

Introduction

The perception of signals arising from the body plays an important role in many theories of emotions (Damasio, 1999, James, 1884, Costa and McCrae, 1989, Schachter and Singer, 1962). William James (1884) was one of the first to present a psychological theory linking viscero-afferent feedback to emotional experience. James suggested that an emotional stimulus initiates particular visceral, vascular or somatic activities, like changes of blood pressure and heart rate, and that perception of these bodily reactions may be the crucial component for mediating the emotional experience. This implies that different emotions are accompanied by different bodily states. The hypothesis was confirmed by studies using visual emotional stimuli (Critchley et al., 2005, Collet et al., 1997, Surakka and Hietanen, 1998, Levenson et al., 1990). But interoceptive awareness, which is the ability to perceive bodily changes, differs substantially across individuals (Jones, 1994). Thus, according to James' theory emotional reactivity should vary between individuals depending on the level of interoceptive awareness.

The latter trait is often quantified by measuring a person's ability to perceive one's heartbeats accurately (Critchley et al., 2004, Cameron, 2001, Pollatos et al., 2005, Schandry and Bestler, 1995, Jones, 1994). Brain structures which are activated during interoception induced by focussing attention to one's heartbeats are the insula, the cingulate cortex, the somatomotor and the prefrontal cortices, as has been shown in two recent studies: The accuracy of heartbeat perception did correlate with the BOLD response at the right insula (Critchley et al., 2004), and the dipole strength at the right insula and dorsal cingulate cortex (Pollatos et al., 2005). As it follows from James' theory, the perceived intensity of arousal, induced by an emotional stimulus, should influence the strength of an experienced emotion. It was recently demonstrated that heart rate increases when looking at pictures with emotional facial expressions, covaried with the level of brain activity in several interconnected brain regions including the amygdala, the insula, the cingulate cortex, and the brainstem (Critchley et al., 2005). Another line of research investigated brain structures activated by cardiovascular arousal, often by using non-emotional stimuli like physical or mental stress tasks (Critchley et al., 2001, King et al., 1999, Williamson et al., 2002).

However, it is still unclear which brain structures are involved in both, the cerebral representation of the bodily change and the representation of its perception. Structures connecting bodily signals and interoceptive awareness could trigger, in a feedforward manner, behavioral responses appropriate to maintain a desired state of the cardiovascular system. Cardiovascular control mechanisms including afferent pathways participating in feedforward control are of a great complexity and variability (Mullen et al., 1997, Nollo et al., 2005, Ursino and Magosso, 2003). In a recent fMRI study by Critchley et al. (2003), it could be shown that – among others – the dorsal cingulate gyrus is related to sympathetic modulation of heart rate and the modulation of different bodily arousal states. Patients with focal damage involving this brain region showed abnormalities in autonomic cardiovascular responses to mental stress (Critchley et al., 2003). Other studies have shown a correlation between midbrain lesions and cardiovascular autonomic dysfunction (Macey et al., 2006, Saari et al., 2004). Moreover, enhancement of contingent negative variation (CNV)-related activity, which is regarded as a measure of anticipatory response activity, in anterior and midcingulate, somatomotor, supplementary motor area as well as insular cortices, was found to be associated with decreases in peripheral sympathetic arousal (Nagai et al., 2004).

As a neuroanatomical construct of James' theory of emotional experience, one can conjecture that brain regions must exist with dual representation of both conscious awareness of visceral sensation and emotional perception. Former research suggests that the right insula and the cingulate gyrus are candidate regions for connecting interoceptive awareness with feelings. For the right insula a correlation has been shown between the intensity of negative emotions and the BOLD response during interoception (Critchley et al., 2004), and it was postulated that the right insula is crucial for conscious awareness of subjective feelings (Craig, 2004). Related research suggests that the insula might be responsible for visceral awareness, but proposes that the cingulate and prefrontal cortex are of key importance for the perception of feelings (Lane et al., 1998): The activity in the cingulate cortex has been shown to be relevant for the accurate detection of emotional signals which were perceived either interoceptively or exteroceptively. In another study it was demonstrated that conscious self-regulation of emotions involved the right cingulate cortex and the right superior frontal gyrus (Beauregard et al., 2001). Interestingly, tracing studies (An et al., 1998, Öngür et al., 1998) could demonstrate that there are strong connection between the insula and areas in the medial prefrontal brain including parts of the cingulate cortex of which posterior and ventral regions are of special importance for processing visceral signals (Devinsky et al., 1995, Vogt and Laureys, 2005, Vogt, 2005, Vogt et al., 1992). Confirming the proposed role of these structures in linking visceral sensation with emotions, a network for vascular responses to emotional stress was suggested comprising the infralimbic cortex, cingulate areas, the hypothalamus and the medulla (Saper, 2002).

The insula as well as the prefrontal and cingulate cortex do also play an essential role in the somatic marker theory of Damasio (Bechara and Naqvi, 2004, Damasio, 1994, Damasio, 1999). Here, it is stated that an emotional object, either derived from the environment or recalled from memory, causes activation in so-called emotion trigger sites (ventromedial prefrontal cortex, amygdala, brain stem nuclei, hypothalamus and basal forebrain) which induce changes towards the body and other brain regions. Both the organism with its ongoing visceral sensations and the object interacting with sensory and motor structures are mapped as neural patterns in so-called first-order mapping structures (e.g. insula, somatosensory cortices). The right insula is therefore important for mapping visceral states and bringing interoceptive signals to conscious perception (Bechara and Naqvi, 2004). Concerning the described role of the insula, it is suggested that, especially within the right anterior insula, a meta-representation of the state of the body is re-represented which is associated with the subjective awareness of the ‘feeling self’ and the degree of emotional awareness (Craig, 2003, Craig, 2004, Craig, 2005). However, additional regions – so-called second-order regions such as the cingulate cortex and regions in the prefrontal cortex – are required for the integration of information about the body with information about the world (Damasio, 1999, Bechara and Naqvi, 2004); also it is yet unclear how these putative structures interact.

The aim of the present study was twofold: Up to now brain structures being commonly involved in the processing of interoceptive signals and cardiovascular arousal have not been investigated. Such regions would be important interfaces for a feedforward system of cardiovascular control. We therefore measured BOLD activity both during a heartbeat perception task and during cardiovascular arousal due to enhanced physical load. In order to investigate whether brain regions mediating cardiovascular arousal and interoception are modulated by emotion also different personality traits were assessed.

Section snippets

Functional imaging data

Interoceptive attention (heartbeat detection) compared to exteroceptive attention (tone detection) was associated with enhanced brain activation in bilateral regions of the insula and inferior/middle frontal gyrus, medial frontal/dorsal cingulate gyrus, right inferior parietal lobule, and thalamic nuclei (see Table 1 and Fig. 1). Increased activity during tone detection could be observed in bilateral acoustic cortices (see Table 1). Next, we tested for activity-mediating interoceptive

Discussion

Regional brain activity was studied by means of functional magnetic resonance imaging during an interoceptive attention task and during enhanced physical load. Interoceptive attention activated several brain regions: the insula, the cingulate, medial and inferior frontal gyrus, the somatomotor cortex, and the thalamus. This network of activity is highly congruent with the anatomical structures identified by Critchley et al. (2004). Since in the latter study a different heartbeat perception task

Subjects and questionnaires

20 right-handed male subjects (age mean = 26.8, S.D. = 3.7, ranging from 21 to 34 years) participated in the study. All subjects gave informed written consent. They completed two questionnaires indexing state and trait anxiety (State Trait Anxiety Inventory (Spielberger et al., 1983) as well as adult personality (NEO–Five Factor Inventory (Costa and McCrae, 1989). The mean scores were used for correlation analyses with heartbeat accuracy and regional brain activity. Heart rate was monitored using a

Acknowledgments

We want to thank the Max Planck Institute of Psychiatry in Munich, Renate Wehrle who took care of the psychophysiological recording of the ECG, the technical staff, especially Rosa Hemauer of the MRI group who supported us in the data processing, Katrin Holler and Anna Nützel who took part in data processing and editing the manuscript and Dr. Martin Wiesmann for his helpful comments on the manuscript.

References (78)

  • Y. Nagai et al.

    Brain activity relating to the contingent negative variation: an fMRI investigation

    NeuroImage

    (2004)
  • W.J.H. Nauta

    The problem of the frontal lobe: a reinterpretation

    J. Psychiatr. Res.

    (1971)
  • T. Nichols et al.

    Valid conjunction inference with the minimum statistic

    NeuroImage

    (2005)
  • K.L. Phan et al.

    Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI

    NeuroImage

    (2002)
  • D.A. Pizzagalli et al.

    Brain electrical tomography in depression: the importance of symptom severity, anxiety, and melancholic features

    Biol. Psychiatry

    (2002)
  • J. Pujol et al.

    Anatomical variability of the anterior cingulate gyrus and basic dimensions of human personality

    NeuroImage

    (2002)
  • B.D. Rusch et al.

    Hippocampal morphometry in depressed patients and control subjects: relations to anxiety symptoms

    Biol. Psychiatry

    (2001)
  • A. Saari et al.

    Cardiovascular autonomic dysfunction correlates with brain MRI lesion load in MS

    Clin. Neurophysiol.

    (2004)
  • M. Sugiura et al.

    Correlation between human personality and neural activity in cerebral cortex

    NeuroImage

    (2000)
  • V. Surakka et al.

    Facial and emotional reactions to Duchenne and non-Duchenne smiles

    Int. J. Psychophysiol.

    (1998)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    NeuroImage

    (2002)
  • B.A. Vogt et al.

    Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness

    Prog. Brain Res.

    (2005)
  • J. Wrase et al.

    Gender differences in the processing of standardized emotional visual stimuli in humans: a functional magnetic resonance imaging study

    Neurosci. Lett.

    (2003)
  • G.L. Ahern et al.

    Heart rate and heart rate variability changes in the intracarotid sodium amobarbital test

    Epilepsia

    (2001)
  • X. An et al.

    Prefrontal cortical projections to longitudinal columns in the midbrain periaqueductal gray in Macaque monkeys

    J. Comp. Neurol.

    (1998)
  • E. Azim et al.

    Sex differences in brain activation elicited by humor

    PNAS

    (2005)
  • M. Beauregard et al.

    Neural correlates of conscious self-regulation of emotion

    J. Neurosci.

    (2001)
  • A. Bechara et al.

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

    Nat. Neurosci.

    (2004)
  • M. Brett et al.

    The problem of functional localization in the human brain

    Nat. Rev., Neurosci.

    (2002)
  • T. Butler et al.

    Fear-related activity in subgenual anterior cingulate differs between men and women

    NeuroReport

    (2005)
  • L. Cahill et al.

    Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an fMRI investigation

    Learn. Mem.

    (2004)
  • O.G. Cameron

    Interoception: the inside story—A model for psychosomatic processes

    Psychosom. Med.

    (2001)
  • S.T. Carmichael et al.

    Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys

    J. Comp. Neurol.

    (1996)
  • M. Corbetta et al.

    Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography

    J. Neurosci.

    (1991)
  • P.T. Costa et al.

    The NEO PI/FFI Manual Supplement

    (1989)
  • A.D. Craig

    Interoception: the sense of the physiological condition of the body

    Curr. Opin. Neurobiol.

    (2003)
  • 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.

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

    Nat. Neurosci.

    (2001)
  • H.D. Critchley et al.

    Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence

    Brain

    (2003)
  • Cited by (265)

    View all citing articles on Scopus
    View full text