Abstract
There is dual tactile innervation of the human hairy skin: in addition to fast-conducting myelinated afferent fibers, there is a system of slow-conducting unmyelinated (C) afferents that respond to light touch. In a unique patient lacking large myelinated afferents, we found that activation of C tactile (CT) afferents produced a faint sensation of pleasant touch. Functional magnetic resonance imaging (fMRI) analysis during CT stimulation showed activation of the insular region, but not of somatosensory areas S1 and S2. These findings identify CT as a system for limbic touch that may underlie emotional, hormonal and affiliative responses to caress-like, skin-to-skin contact between individuals.
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References
Kandel, E.R., Schwartz, J.H. & Jessell, T.M. Principles of Neural Science (McGraw-Hill, Health Professions Division, New York, 2000).
Zotterman, Y. Touch, pain and tickling: an electrophysiological investigation on cutaneous sensory nerves. J. Physiol. (Lond.) 95, 1–28 (1939).
Vallbo, Å., Olausson, H., Wessberg, J. & Norrsell, U. A system of unmyelinated afferents for innocuous mechanoreception in the human skin. Brain Res. 628, 301–304 (1993).
Nordin, M. Low-threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve. J. Physiol. (Lond.) 426, 229–240 (1990).
Vallbo, Å.B., Olausson, H. & Wessberg, J. Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J. Neurophysiol. 81, 2753–2763 (1999).
Edin, B. Cutaneous afferents provide information about knee joint movements in humans. J. Physiol. (Lond.) 531, 289–297 (2001).
Douglas, W.W. & Ritchie, J.M. Non-medullated fibres in the saphenous nerve which signal touch. J. Physiol. (Lond.) 139, 385–399 (1957).
Kumazawa, T. & Perl, E.R. Primate cutaneous sensory units with unmyelinated (C) afferent fibers. J. Neurophysiol. 40, 1325–1338 (1977).
Georgopoulos, A.P. Functional properties of primary afferent units probably related to pain mechanisms in primate glabrous skin. J Neurophysiol. 39, 71–83 (1976).
Bessou, P., Burgess, P.R., Perl, E.R. & Taylor, C.B. Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. J. Neurophysiol. 34, 116–131 (1971).
Johansson, R.S. & Vallbo, Å.B. Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J. Physiol. (Lond.) 286, 283–300 (1979).
Kakuda, N. Conduction velocity of low-threshold mechanoreceptive afferent fibers in the glabrous and hairy skin of human hands measured with microneurography and spike-triggered averaging. Neurosci. Res. 15, 179–188 (1992).
Iggo, A. Cutaneous mechanoreceptors with afferent C fibres. J. Physiol. (Lond.) 152, 337–353 (1960).
Kumazawa, T. & Perl, E.R. Primate cutaneous receptors with unmyelinated (C) fibres and their projection to the substantia gelatinosa. J. Physiol. (Paris) 73, 287–304 (1977).
Light, A.R., Trevino, D.L. & Perl, E.R. Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J. Comp. Neurol. 186, 151–171 (1979).
Sugiura, Y., Lee, C.L. & Perl, E.R. Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin. Science 234, 358–361 (1986).
Light, A.R. & Willcockson, H.H. Spinal laminae I–II neurons in rat recorded in vivo in whole cell, tight seal configuration: properties and opioid responses. J. Neurophysiol. 82, 3316–3326 (1999).
MacKenzie, R.A., Burke, D., Skuse, N.F. & Lethlean, A.K. Fibre function and perception during cutaneous nerve block. J. Neurol. Neurosurg. Psychiatry 38, 865–873 (1975).
Essick, G.K., James, A. & McGlone, F.P. Psychophysical assessment of the affective components of non-painful touch. Neuroreport 10, 2083–2087 (1999).
Forget, R. & Lamarre, Y. Postural adjustments associated with different unloadings of the forearm: effects of proprioceptive and cutaneous afferent deprivation. Can. J. Physiol. Pharmacol. 73, 285–294 (1995).
Olausson, H., Norrsell, U., Göthner, K. & Wallin, B.G. Directional sensibility for quantification of tactile dysfunction. Muscle Nerve 20, 1414–1421 (1997).
Robinson, C.J. & Burton, H. Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis. J. Comp. Neurol. 192, 69–92 (1980).
Augustine, J.R. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Rev. 22, 229–244 (1996).
Järvilehto, T., Hämäläinen, H. & Laurinen, P. Characteristics of single mechanoreceptive fibres innervating hairy skin of the human hand. Exp. Brain Res. 25, 45–61 (1976).
Konietzny, F. & Hensel, H. Response of rapidly and slowly adapting mechanoreceptors and vibratory sensitivity in human hairy skin. Pflügers Arch. 368, 39–44 (1977).
Burgess, P.R., Petit, D. & Warren, R.M. Receptor types in cat hairy skin supplied by myelinated fibers. J. Neurophysiol. 31, 833–848 (1968).
Perl, E.R. Myelinated afferent fibres innervating the primate skin and their response to noxious stimuli. J. Physiol. (Lond.) 197, 593–615 (1968).
Vallbo, Å.B., Olausson, H., Wessberg, J. & Kakuda, N. Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. J. Physiol. (Lond.) 483, 783–795 (1995).
Uvnäs-Moberg, K. Oxytocin may mediate the benefits of positive social interaction and emotions. Psychoneuroendocrinology 23, 819–835 (1998).
Harlow, H.F. The nature of love. Am. Psychol. 13, 673–685 (1958).
Friedman, D.P., Murray, E.A., O'Neill, J.B. & Mishkin, M. Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a corticolimbic pathway for touch. J. Comp. Neurol. 252, 323–347 (1986).
Disbrow, E., Buonocore, M., Antognini, J., Carstens, E. & Rowley, H.A. Somatosensory cortex: a comparison of the response to noxious thermal, mechanical, and electrical stimuli using functional magnetic resonance imaging. Hum. Brain Mapp. 6, 150–159 (1998).
Coghill, R.C. et al. Distributed processing of pain and vibration by the human brain. J. Neurosci. 14, 4095–4108 (1994).
Brooks, J.C., Nurmikko, T.J., Bimson, W.E., Singh, K.D. & Roberts, N. fMRI of thermal pain: effects of stimulus laterality and attention. Neuroimage 15, 293–301 (2002).
Drzezga, A. et al. Central activation by histamine-induced itch: analogies to pain processing: a correlational analysis of O-15 H2O positron emission tomography studies. Pain 92, 295–305 (2001).
Craig, A.D., Chen, K., Bandy, D. & Reiman, E.M. Thermosensory activation of insular cortex. Nat. Neurosci. 3, 184–190 (2000).
Bartels, A. & Zeki, S. The neural basis of romantic love. Neuroreport 11, 3829–3834 (2000).
Stoleru, S. et al. Neuroanatomical correlates of visually evoked sexual arousal in human males. Arch. Sex. Behav. 28, 1–21 (1999).
Craig, A.D. in Progress in Brain Research (eds. Holstege, G., Bandler, R. & Saper, C. B.) 225–242 (Elsevier Science BV, Ireland, 1996).
Craig, A.D. & Andrew, D. Responses of spinothalamic lamina I neurons to repeated brief contact heat stimulation in the cat. J. Neurophysiol. 87, 1902–1914 (2002).
White, J.C. & Sweet, W.H. Pain and the Neurosurgeon: a Forty-year Experience (C. C. Thomas, Springfield, Illinois, 1969).
Craig, A.D. Spinal location of ascending lamina I axons in the Macaque monkey. J. Pain 1, 33–45 (2000).
Damasio, A.R. The Feeling of What Happens: Body and Emotion in the Making of Consciousness (Harcourt Brace, New York, 1999).
Melzack, R. & Wall, P.D. Pain mechanisms: a new theory. Science 150, 971–979 (1965).
Yarnitsky, D., Sprecher, E., Zaslansky, R. & Hemli, J.A. Heat pain thresholds: normative data and repeatability. Pain 60, 329–332 (1995).
Worsley, K.J. et al. A general statistical analysis for fMRI data. Neuroimage 15, 1–15 (2002).
Olausson, H. et al. Cortical activation by tactile and painful stimuli in hemispherectomized patients. Brain 124, 916–927 (2001).
Collins, D.L., Neelin, P., Peters, T.M. & Evans, A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 18, 192–205 (1994).
Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain (G. Thieme, Stuttgart, 1988).
Acknowledgements
This study was supported by the Canadian and Swedish Medical Research Councils (grants 3546, 12170 and 3548), and the Ingabritt and Arne Lundberg Research Foundation.
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Olausson, H., Lamarre, Y., Backlund, H. et al. Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5, 900–904 (2002). https://doi.org/10.1038/nn896
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DOI: https://doi.org/10.1038/nn896
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