Review
The cutaneous sensory system

https://doi.org/10.1016/j.neubiorev.2009.08.004Get rights and content

Abstract

The cutaneous senses are traditionally thought to comprise four recognized submodalities that relay tactile, thermal, painful and pruritic (itch) information to the central nervous system, but there is growing evidence for the presence of a fifth modality that conveys positive affective (pleasant) properties of touch. Cutaneous sensory channels can be further classified as serving predominantly either discriminative or affective functions. The former provides information about the spatial and temporal localisation of events on the body surface, e.g., the presence of an insect or the temperature of a cold wind; and the latter, although widely recognised as providing the afferent neural input driving the negative emotional experience of pain, is here posited to provide the afferent neural input driving the positive emotional experience of affiliative touch as well. A distinction is made between the properties of fast conducting myelinated afferents and those of slowly conducting unmyelinated afferents, with the former subserving a sensory-discriminative role, and the latter an affective-motivational one. Here we review the basic elements of the somatosensory system and outline evidence for the inclusion of the ‘fifth’ sub-modality, conveyed by low-threshold C-fiber mechanoreceptors as the counterpart of high-threshold C-fiber nociceptors with both C-fiber systems serving opposing aspects of affective touch, yet underpining a common mechanism for the preservation of self and species.

Section snippets

Introduction to the somatosensory system

The primary sensory modality subserving the body senses is collectively described as the somatosensory system. It comprises all those peripheral afferent nerve fibers, and specialised receptors, subserving proprioceptive (joint, muscle) and cutaneous sensitivity. The former processes information about limb position and muscle forces which the central nervous system uses to monitor and control limb movements and to ensure that a planned action or movement is executed fluently via elegant

The peripheral nervous system

The skin is the most extensive and versatile of the body's organs and in a fully grown adult covers a surface area approaching 2 m2. Apart from its role as a sensory organ the skin contains in excess of 2 million sweat glands and 5 million hairs, that may be either fine vellous types covering all surfaces apart from the soles of the feet and the palms of the hands (glabrous skin). Skin consists of an outer stratified squamous epithelium of ectodermal origin – the epidermis – and an inner,

The central projections

The submodalties of skin sensory receptors and nerves that convey information to the brain about mechanical, thermal, and painful/pruritic stimulation of the skin are grouped into three different pathways in the spinal cord and project to different target areas in the brain. They differ in their receptors, pathways, and targets, and also in the level of decussation (crossing over) within the CNS. Most sensory systems en route to the cerebral cortex decussate at some point, as projections are

Conclusion

This overview of the cutaneous senses provides a landscape view of the system's structure and function, with the following review papers in this Special Issue highlighting specific aspects and properties of the skin senses and their roles in sensation, affect and cognition. Cutaneous sensitivity is central to human functional, emotional and social life, as is evidenced by it being the most developed sensory modality at birth, contributing to brain and cognitive development throughout infancy

References (95)

  • K. Inoue et al.

    Functional vanilloid receptors in cultured normal human keratinocytes

    Biochem. Biophys. Res. Com.

    (2002)
  • E.G. Jones

    A pain in the thalamus

    Pain

    (2002)
  • J.A. Maldjian et al.

    The sensory somatotopic map of the human hand demonstrated at 4T

    NeuroImage

    (1999)
  • F.P. McGlone et al.

    Functional neuroimaging studies of human somatosensory cortex

    Behav. Brain Res.

    (2002)
  • S.L. McIlwrath et al.

    The sensory mechanotransduction ion channel ASIC2 acid sensitive ion channel 2 is regulated by neutrophin availability

    Neuroscience

    (2005)
  • R. Melzack

    The McGill pain questionnaire: major properties and scoring methods

    Pain

    (1975)
  • C. Montell et al.

    The TRP channels, a remarkably functional family

    Cell

    (2002)
  • R.J. Schneider et al.

    A modality specific somatosensory area within the insula of the rhesus monkey

    Brain Res.

    (1993)
  • A.B. Vallbo et al.

    A system of unmyelinated afferents for innocuous mechanoreception in the human skin

    Brain Res.

    (1993)
  • D. Andrew et al.

    Spinothalamic lamina 1 neurons selectively sensitive to histamine: a central neural pathway for itch

    Nat. Neurosci.

    (2001)
  • A.E. Applebaum et al.

    Organization and receptive fields of primate spinothalamic tract neurons

    J. Neurophysiol.

    (1975)
  • C.C. Askwith et al.

    DEG/EnaC ion channels involved in sensory transduction are modulated by cold temperature

    PNAS

    (2001)
  • I.M. Bentley

    The synthetic experiment

    Am. J. Psychol.

    (1900)
  • M. Bessou et al.

    Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli

    J. Neurophysiol.

    (1969)
  • S.J. Bolanowski et al.

    Four channels mediate the mechanical aspects of touch

    J. Acoust. Soc. Am.

    (1988)
  • J.N. Campbell et al.

    Peripheral neural mechanisms of nociception

  • M. Campero et al.

    C-polymodal nociceptors activated by noxious low temperature in human skin

    J. Physiol.

    (1996)
  • M. Campero et al.

    Slowly conducting afferents activated by innocuous low temperature in human skin

    J. Physiol.

    (2001)
  • C.M. Canessa et al.

    Epithelial sodium channel related to proteins involved in neurodegeneration

    Nature

    (1993)
  • M.J. Caterina et al.

    The capsaicin receptor: a heat-activated ion channel in the pain pathway

    Nature

    (1997)
  • M.J. Caterina et al.

    Impaired nociception and pain sensation in mice lacking the capsaicin receptor

    Science

    (2000)
  • D.E. Clapham

    TRP channels as cellular sensors

    Nature

    (2003)
  • R.C. Coghill et al.

    Distributed processing of pain and vibration by the human brain

    J. Neurosci.

    (1994)
  • B. Craig

    How do you feel—now? The anterior insula and human awareness

    Nat. Neurosci. Rev.

    (2009)
  • I. Darian-Smith

    The sense of touch: performance and peripheral neural processes

  • I. Darian-Smith

    Thermal sensibility

  • J.B. Davis et al.

    Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia

    Nature

    (2000)
  • M. Denda et al.

    Epidermal keratinocytes as the forefront of the sensory system

    Exp. Dermatol.

    (2007)
  • M. Driscoll et al.

    Closing in on a mammalian touch receptor

    Nat. Neurosci.

    (2000)
  • R. Duclaux et al.

    Conduction velocity along afferent vagal dendrites: a new type of fiber

    J. Physiol.

    (1976)
  • G.J. Ebenezer et al.

    Denervation of skin in neuropathies: the sequence of axonal and Schwann cell changes in skin biopsies

    Brain

    (2007)
  • G.K. Essick et al.

    Receptor encoding of moving tactile stimuli in humans. II. The mean response of individual low-threshold mechanoreceptors to motion across the receptive field

    J. Neurosci.

    (1995)
  • G. Essick et al.

    Psychophysical assessment of the affective components of non-painful touch

    NeuroReport

    (1999)
  • S.T. Francis et al.

    The representation of pleasant touch in the brain and its relationship with taste and olfactory areas

    NeuroReport

    (1999)
  • G.A. Gescheider et al.

    Some characteristics of tactile channels

    Behav. Brain Res.

    (2003)
  • G.A. Gescheider et al.

    Prediction of vibrotactile masking functions

    J. Acoust. Soc. Am.

    (1982)
  • Cited by (303)

    View all citing articles on Scopus
    View full text