Interoception: the sense of the physiological condition of the body

https://doi.org/10.1016/S0959-4388(03)00090-4Get rights and content

Abstract

Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and ‘air hunger’. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.

Introduction

Humans perceive ‘feelings’ from the body that provide a sense of their physical condition and underlie mood and emotional state. However, in the conventional view, the well-discriminated feelings of temperature, itch and pain are associated with an ‘exteroceptive’ somatosensory system, whereas the less distinct visceral feelings of vasomotor activity, hunger, thirst and internal sensations are associated with a separate ‘interoceptive’ system. That categorization obscures several fundamental discrepancies, such as the lack of effect of stimulation or lesions of somatosensory cortices on temperature or pain sensation, and the inherent emotional (affective/motivational) qualities and reflexive autonomic effects that all feelings from the body share. Recent findings that compel a conceptual shift resolve these issues by showing that all feelings from the body are represented in a phylogenetically new system in primates. This system has evolved from the afferent limb of the evolutionarily ancient, hierarchical homeostatic system that maintains the integrity of the body. These feelings represent a sense of the physiological condition of the entire body, redefining the category ‘interoception’. The present article summarizes this new view; more detailed reviews are available elsewhere 1.••, 2..

Section snippets

Anatomical characteristics

Cannon [3] recognized that the neural processes (autonomic, neuroendocrine and behavioral) that maintain optimal physiological balance in the body, or homeostasis, must receive afferent inputs that report the condition of the tissues of the body. ‘Parasympathetic’ (vagal and glossopharyngeal) afferents to the nucleus of the solitary tract (NTS) have long been recognized, but an afferent pathway that parallels sympathetic efferents has only recently been identified. Small-diameter (Aδ and C)

Input to VMpo

In primates, lamina I neurons project topographically to a relay nucleus in the posterolateral thalamus, the posterior ventral medial nucleus (VMpo) 1.••, 26.. Their axons ascend in the lateral spinothalamic tract, precisely where lesions selectively interrupt the feelings from the body [27]. The VMpo is organized antero-posteriorly, orthogonal to the medio-lateral topography of the somatosensory ventral posterior (VP) nuclei, which it is connected to at the point at which the mouth is

Conclusions

Recent findings have identified a homeostatic afferent path that represents the physiological condition of all tissues of the body. The direct ‘encephalized’ inputs in humans provide the substrate for homeostatic emotions involving distinct sensations, engendered in interoceptive and anterior insular cortex (the feeling self), as well as affective motivations, engendered in the ACC (the behavioral agent). These findings explain the distinct nature of pain, temperature, itch, sensual touch and

Update

Since this review was submitted several interesting and relevant studies have been published in this area. New imaging results relevant to interoception and the feeling self are rapidly accumulating, such as the fMRI study from Bingel et al. [51] confirming that laser-evoked pain distinguishes activation of interoceptive cortex from the neighboring somatosensory cortex. Critchley et al. [52] contribute a review of the imaging literature on emotion in which the concepts of interoception and the

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

  • of special interest

  • ••

    of outstanding interest

Acknowledgements

I would like to thank the many collaborators, colleagues, friends and associates who have worked on these projects and discussed these ideas with me. My laboratory is supported by National Institutes of Health grants NS40413 and 41287 and the Barrow Neurological Foundation.

References (55)

  • Cannon WB: The Wisdom of the Body. New York: Norton & Company;...
  • W.M. Panneton

    Primary afferent projections from the upper respiratory tract in the muskrat

    J Comp Neurol

    (1991)
  • J. Altman et al.

    The development of the rat spinal cord

    Adv Anat Embryol Cell Biol

    (1984)
  • A.D. Craig

    Propriospinal input to thoracolumbar sympathetic nuclei from cervical and lumbar lamina I neurons in the cat and the monkey

    J Comp Neurol

    (1993)
  • Holstege G: Direct and indirect pathways to lamina I in the medulla oblongata and spinal cord of the cat. In Progress...
  • A. Sato et al.

    Somatosympathetic reflexes: afferent fibers, central pathways, discharge characteristics

    Physiol Rev

    (1973)
  • A.D. Craig

    Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey

    J Comp Neurol

    (1995)
  • B. Pan et al.

    Central afferent pathways conveying nociceptive input to the hypothalamic paraventricular nucleus as revealed by a combination of retrograde labeling and c-fos activation

    J Comp Neurol

    (1999)
  • C.B. Saper

    The central autonomic nervous system: conscious visceral perception and autonomic pattern generation

    Annu Rev Neurosci

    (2002)
  • L.W. Swanson

    Cerebral hemisphere regulation of motivated behavior

    Brain Res

    (2000)
  • Z.H. Zhang et al.

    Baroreceptive and somatosensory convergent thalamic neurons project to the posterior insular cortex in the rat

    Brain Res

    (2000)
  • J.P. Johansen et al.

    The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex

    Proc Natl Acad Sci USA

    (2001)
  • Darwin C: The Expression of the Emotions in Man and Animals. Chicago: University of Chicago Press (1965 reprint);...
  • C.M. Adreani et al.

    Effect of arterial occlusion on responses of group III and IV afferents to dynamic exercise

    J Appl Physiol

    (1998)
  • Å.B. Vallbo et al.

    Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin

    J Neurophysiol

    (1999)
  • Light AR: The Initial Processing of Pain and Its Descending Control: Spinal and Trigeminal Systems. Basel: Karger;...
  • D. Andrew et al.

    Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch

    Nat Neurosci

    (2001)
  • Cited by (1862)

    • The role of touch in osteopathic clinical encounters – A scoping review

      2024, International Journal of Osteopathic Medicine
    View all citing articles on Scopus
    View full text