Interoception: the sense of the physiological condition of the body
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:
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of special interest
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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)
- et al.
Parabrachial nucleus projections to midline and intralaminar thalamic nuclei of the rat
J Comp Neurol
(2000) - et al.
Autonomic responses and efferent pathways from the insular cortex in the rat
J Comp Neurol
(1991) - Craig AD: New and old thoughts on the mechanisms of spinal cord injury pain. In Spinal Cord Injury Pain: Assessment,...
- James W: The Principles of Psychology. URL:...
- Damasio AR: Descartes’ Error: Emotion, Reason, and the Human Brain. New York: Putnam;...
- et al.
Subcortical and cortical brain activity during the feeling of self-generated emotions
Nat Neurosci
(2000) - et al.
Single trial fMRI reveals significant contralateral bias in responses to laser pain within thalamus and somatosensory cortices
Neuroimage
(2003) Mental self: the person within
Nature
(2003)How do you feel? Interoception: the sense of the physiological condition of the body
Nat Rev Neurosci
(2002)Pain mechanisms: labeled lines versus convergence in central processing
Annu Rev Neurosci
(2003)
Primary afferent projections from the upper respiratory tract in the muskrat
J Comp Neurol
The development of the rat spinal cord
Adv Anat Embryol Cell Biol
Propriospinal input to thoracolumbar sympathetic nuclei from cervical and lumbar lamina I neurons in the cat and the monkey
J Comp Neurol
Somatosympathetic reflexes: afferent fibers, central pathways, discharge characteristics
Physiol Rev
Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey
J Comp Neurol
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
The central autonomic nervous system: conscious visceral perception and autonomic pattern generation
Annu Rev Neurosci
Cerebral hemisphere regulation of motivated behavior
Brain Res
Baroreceptive and somatosensory convergent thalamic neurons project to the posterior insular cortex in the rat
Brain Res
The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex
Proc Natl Acad Sci USA
Effect of arterial occlusion on responses of group III and IV afferents to dynamic exercise
J Appl Physiol
Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin
J Neurophysiol
Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch
Nat Neurosci
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