Advertisement

The Touch Landscape

  • Rochelle AckerleyEmail author
  • Helena Backlund Wasling
  • Francis McGlone
Chapter

Abstract

Somatic sensation comprises four main modalities relaying tactile, thermal, painful, or pruritic (itch) information to the central nervous system. These input channels can be further classified as sub-serving sensory functions, such as spatial and temporal discrimination, and the provision of essential information for controlling and guiding exploratory manual behaviours, or affective functions that include the provision of the subjective experience of affective or emotional pleasurable touch. Signalling in fast-conducting myelinated peripheral nerve fibres (Aβ afferents) is important for the discriminative properties of tactile sensations, whereas signalling in unmyelinated peripheral nerve fibres, C-tactile (CT) afferents seems to be important for the rewarding, emotional properties of touch. CT afferents have specific biophysical, electrophysiological, neurobiological and anatomical properties to drive the temporally delayed affective somatic system. This chapter explores step by step the differences between the discriminative and affective touch systems, from the first stage of encoding touch in the skin to the neural pathways in the brain. The below quote from Bentley (Am J Psychol 11:405–425, 1900) reiterates the complexity of the skin and the wonder in the phenomenon of somatosensation:

‘The skin is burdened with offices. One of the surprises of physiology is the revelation of the multitude of functions performed by this apparently simple organ. As a rind it is not only the container, but the warder-off, and also the go-between for the organism and its world; tegument, buckler, interagent. It is small wonder that its work is represented in mental process; that many of our most worn and useful perceptions are made up of cutaneous sensations.’

Keywords

Affective touch Discriminative touch Somatosensation C-tactile Afferent Mechanoreceptor Somatosensory cortex Insula Myelinated Unmyelinated 

References

  1. Abraira VE, Ginty DD (2013) The sensory neurons of touch. Neuron 79:618–639. doi: 10.1016/j.neuron.2013.07.051 PubMedCrossRefGoogle Scholar
  2. Ackerley R, Backlund Wasling H, Liljencrantz J et al (2014a) Human C-tactile afferents are tuned to the temperature of a skin-stroking caress. J Neurosci 34:2879–2883. doi: 10.1523/JNEUROSCI.2847-13.2014 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ackerley R, Carlsson I, Wester H et al (2014b) Touch perceptions across skin sites: differences between sensitivity, direction discrimination and pleasantness. Front Behav Neurosci 8:54. doi: 10.3389/fnbeh.2014.00054 PubMedPubMedCentralGoogle Scholar
  4. Ackerley R, Eriksson E, Wessberg J (2013) Ultra-late EEG potential evoked by preferential activation of unmyelinated tactile afferents in human hairy skin. Neurosci Lett 535:62–66. doi: 10.1016/j.neulet.2013.01.004 PubMedCrossRefGoogle Scholar
  5. Ackerley R, Hassan E, Curran A et al (2012) An fMRI study on cortical responses during active self-touch and passive touch from others. Front Behav Neurosci 6:51. doi: 10.3389/fnbeh.2012.00051 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Ackerley R, Kavounoudias A (2015) The role of tactile afference in shaping motor behaviour and implications for prosthetic innovation. Neuropsychologia 79(Pt B):192–205. doi: 10.1016/j.neuropsychologia.2015.06.024.Google Scholar
  7. Ackerley R, Saar K, McGlone F, Backlund Wasling H (2014c) Quantifying the sensory and emotional perception of touch: differences between glabrous and hairy skin. Front Behav Neurosci 8:34. doi: 10.3389/fnbeh.2014.00034 PubMedPubMedCentralGoogle Scholar
  8. Adriaensen H, Gybels J, Handwerker H, Van Hees J (1983) Response properties of thin myelinated (A-delta) fibers in human skin nerves. J Neurophysiol 49:111–122PubMedGoogle Scholar
  9. Adrian E, Umrath K (1929) The impulse discharge from the pacinian corpuscle. J Physiol 68:139–154. doi: 10.1007/SpringerReference_183154 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Andrew D (2010) Quantitative characterization of low-threshold mechanoreceptor inputs to lamina I spinoparabrachial neurons in the rat. J Physiol 588:117–124. doi: 10.1113/jphysiol.2009.181511 PubMedCrossRefGoogle Scholar
  11. Azañón E, Longo MR, Soto-Faraco S, Haggard P (2010) The posterior parietal cortex remaps touch into external space. Curr Biol 20:1304–1309. doi: 10.1016/j.cub.2010.05.063 PubMedCrossRefGoogle Scholar
  12. Bentley I (1900) The synthetic experiment. Am J Psychol 11:405–425CrossRefGoogle Scholar
  13. Birznieks I, Macefield VG, Westling G, Johansson RS (2009) Slowly adapting mechanoreceptors in the borders of the human fingernail encode fingertip forces. J Neurosci 29:9370–9379. doi: 10.1523/JNEUROSCI.0143-09.2009 PubMedCrossRefGoogle Scholar
  14. Bolognini N, Rossetti A, Convento S, Vallar G (2013) Understanding others’ feelings: the role of the right primary somatosensory cortex in encoding the affective valence of others’ touch. J Neurosci 33:4201–4205. doi: 10.1523/JNEUROSCI.4498-12.2013 PubMedCrossRefGoogle Scholar
  15. Bostock H, Campero M, Serra J, Ochoa J (2003) Velocity recovery cycles of C fibres innervating human skin. J Physiol 553:649–663. doi: 10.1113/jphysiol.2003.046342 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brown A (1977) Cutaneous axons and sensory neurones in the spinal cord. Br Med Bull 33:109–112PubMedGoogle Scholar
  17. Brown A, Fyffe R, Noble R (1980) Projections from Pacinian corpuscles and rapidly adapting mechanoreceptors of glabrous skin to the cat’s spinal cord. J Physiol 307:385–400PubMedPubMedCentralCrossRefGoogle Scholar
  18. Büchel C, Geuter S, Sprenger C, Eippert F (2014) Placebo analgesia: a predictive coding perspective. Neuron 81:1223–1239. doi: 10.1016/j.neuron.2014.02.042 PubMedCrossRefGoogle Scholar
  19. Burgess PR, Petit D, Warren R (1968) Receptor types in cat hairy skin supplied by myelinated fibers. J Neurophysiol 31:833–848PubMedGoogle Scholar
  20. Chambers M, Andres K, Duering M, Iggo A (1972) The structure and function of the slowly adapting type II mechanoreceptor in hairy skin. Q J Exp Physiol 57:417–445PubMedCrossRefGoogle Scholar
  21. Chikenji T, Berger RA, Fujimiya M et al (2011) Distribution of nerve endings in human distal interphalangeal joint and surrounding structures. J Hand Surg Am 36:406–412. doi: 10.1016/j.jhsa.2010.11.050 PubMedCrossRefGoogle Scholar
  22. Chikenji T, Suzuki D, Fujimiya M et al (2010) Distribution of nerve endings in the human proximal interphalangeal joint and surrounding structures. J Hand Surg Am 35:1286–1293. doi: 10.1016/j.jhsa.2010.04.026 PubMedCrossRefGoogle Scholar
  23. Cole J, Bushnell MC, McGlone F et al (2006) Unmyelinated tactile afferents underpin detection of low-force monofilaments. Muscle Nerve 34:105–107. doi: 10.1002/mus.20534 PubMedCrossRefGoogle Scholar
  24. Coleman GT, Bahramali H, Zhang HQ, Rowe MJ (2001) Characterization of tactile afferent fibers in the hand of the marmoset monkey. J Neurophysiol 85:1793–1804PubMedGoogle Scholar
  25. Condon M, Birznieks I, Hudson K et al (2014) Differential sensitivity to surface compliance by tactile afferents in the human finger pad. J Neurophysiol 111:1308–1317. doi: 10.1152/jn.00589.2013 PubMedCrossRefGoogle Scholar
  26. Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505. doi: 10.1016/S0959-4388(03)00090-4 PubMedCrossRefGoogle Scholar
  27. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666. doi: 10.1038/nrn894 PubMedCrossRefGoogle Scholar
  28. Craig AD (2009) How do you feel--now? The anterior insula and human awareness. Nat Rev Neurosci 10:59–70. doi: 10.1038/nrn2555 PubMedCrossRefGoogle Scholar
  29. Douglas W, Ritchie J (1957) Non-medullated fibres in the saphenous nerve which signal touch. J Physiol 139:385–399PubMedPubMedCentralCrossRefGoogle Scholar
  30. Driskell RR, Giangreco A, Jensen KB et al (2009) Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 136:2815–2823. doi: 10.1242/dev.038620 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Edin BB (1992) Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J Neurophysiol 67:1105–1113PubMedGoogle Scholar
  32. Essick GK, James A, McGlone FP (1999) Psychophysical assessment of the affective components of non-painful touch. Neuroreport 10:2083–2087PubMedCrossRefGoogle Scholar
  33. Essick GK, McGlone F, Dancer C et al (2010) Quantitative assessment of pleasant touch. Neurosci Biobehav Rev 34:192–203. doi: 10.1016/j.neubiorev.2009.02.003 PubMedCrossRefGoogle Scholar
  34. Francis S, Rolls ET, Bowtell R et al (1999) The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. Neuroreport 10:453–459PubMedCrossRefGoogle Scholar
  35. Gairns F (1955) The sensory nerve endings of the human palate. Exp Physiol 40:40–48CrossRefGoogle Scholar
  36. Gazzola V, Spezio ML, Etzel JA et al (2012) Primary somatosensory cortex discriminates affective significance in social touch. Proc Natl Acad Sci U S A 109:E1657–E1666. doi: 10.1073/pnas.1113211109 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gordon I, Voos AC, Bennett RH et al (2013) Brain mechanisms for processing affective touch. Hum Brain Mapp 34:914–922. doi: 10.1002/hbm.21480 PubMedCrossRefGoogle Scholar
  38. Guest S, Dessirier JM, Mehrabyan A et al (2011) The development and validation of sensory and emotional scales of touch perception. Atten Percept Psychophys 73:531–550. doi: 10.3758/s13414-010-0037-y PubMedCrossRefGoogle Scholar
  39. Hagen MC, Pardo JV (2002) PET studies of somatosensory processing of light touch. Behav Brain Res 135:133–140PubMedCrossRefGoogle Scholar
  40. Halata Z (1993) Sensory innervation of the hairy skin (light- and electronmicroscopic study). J Invest Dermatol 101:75S–81SPubMedCrossRefGoogle Scholar
  41. Horch K, Tuckett R, Burgess P (1977) A key to the classification of cutaneous mechanoreceptors. J Invest Dermatol 69:75–82PubMedCrossRefGoogle Scholar
  42. Hsiao SS, Johnson KO, Twombly IA (1993) Roughness coding in the somatosensory system. Acta Psychol (Amst) 84:53–67CrossRefGoogle Scholar
  43. Hsiao SS, Lane J, Fitzgerald P (2002) Representation of orientation in the somatosensory system. Behav Brain Res 135:93–103PubMedCrossRefGoogle Scholar
  44. Hua Q-P, Zeng X-Z, Liu J-Y et al (2008) Dynamic changes in brain activations and functional connectivity during affectively different tactile stimuli. Cell Mol Neurobiol 28:57–70. doi: 10.1007/s10571-007-9228-z PubMedCrossRefGoogle Scholar
  45. Iggo A (1960) Cutaneous mechanoreceptors with afferent C fibres. J Physiol 152:337–353PubMedPubMedCentralCrossRefGoogle Scholar
  46. Iggo A, Kornhuber HH (1977) A quantitative study of C-mechanoreceptors in hairy skin of the cat. J Physiol 271:549–565PubMedPubMedCentralCrossRefGoogle Scholar
  47. Iggo A, Ogawa H (1977) Correlative physiological and morphological studies of rapidly adapting mechanoreceptors in cat’s glabrous skin. J Physiol 266:275–296PubMedPubMedCentralCrossRefGoogle Scholar
  48. Jaeger H (1944) Recherches histologiques sur les terminaisons nerveuses dans la peau normale des organes génitaux externs humains. Dermatology 90:49–74. doi: 10.1159/000255731 CrossRefGoogle Scholar
  49. Järvilehto T, Hämäläinen H, Soininen K (1981) Peripheral neural basis of tactile sensations in man: II. Characteristics of human mechanoreceptors in the hairy skin and correlations of their activity with tactile sensations. Brain Res 219:13–27PubMedCrossRefGoogle Scholar
  50. Johansson R, Trulsson M, Olsson KÅ, Westberg K-G (1988) Mechanoreceptor activity from the human face and oral mucosa. Exp Brain 72:204–208CrossRefGoogle Scholar
  51. Johansson RS (1978) Tactile sensibility in the human hand: receptive field characteristics of mechanoreceptive units in the glabrous skin area. J Physiol 281:101–125PubMedPubMedCentralCrossRefGoogle Scholar
  52. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7:170–177. doi: 10.1038/nn1177 PubMedCrossRefGoogle Scholar
  53. Johansson RS, Flanagan JR (2009) Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10:345–359. doi: 10.1038/nrn2621 PubMedCrossRefGoogle Scholar
  54. Johansson RS, Landström U, Lundström R (1982) Responses of mechanoreceptive afferent units in the glabrous skin of the human hand to sinusoidal skin displacements. Brain Res 244:17–25PubMedCrossRefGoogle Scholar
  55. Johansson RS, Vallbo AB (1979) Tactile sensibility in the human hand: relative and absolute densities of four types of mechanoreceptive units in glabrous skin. J Physiol 286:283–300PubMedPubMedCentralCrossRefGoogle Scholar
  56. Johansson RS, Vallbo AB (1980) Spatial properties of the population of mechanoreceptive units in the glabrous skin of the human hand. Brain Res 184:353–366PubMedCrossRefGoogle Scholar
  57. Johansson RS, Vallbo AB, Westling G (1980) Thresholds of mechanosensitive afferents in the human hand as measured with von Frey hairs. Brain Res 184:343–351PubMedCrossRefGoogle Scholar
  58. Johnson RD, Halata Z (1991) Topography and ultrastructure of sensory nerve endings in the glans penis of the rat. J Comp Neurol 312:299–310. doi: 10.1002/cne.903120212 PubMedCrossRefGoogle Scholar
  59. Johnson RD, Kitchell RL (1987) Mechanoreceptor response to mechanical and thermal stimuli in the glans penis of the dog. J Neurophysiol 57:1813–1836PubMedGoogle Scholar
  60. Jörntell H, Bengtsson F, Geborek P et al (2014) Segregation of tactile input features in neurons of the cuneate nucleus. Neuron 83:1444–1452. doi: 10.1016/j.neuron.2014.07.038 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kaas J, Nelson R, Sur M et al (1979) Multiple representations of the body within the primary somatosensory cortex of primates. Science 204(4392):521–523PubMedCrossRefGoogle Scholar
  62. Kaas JH, Nelson RJ, Sur M et al (1984) The somatotopic organization of the ventroposterior thalamus of the squirrel monkey, Saimiri sciureus. J Comp Neurol 226:111–140. doi: 10.1002/cne.902260109 PubMedCrossRefGoogle Scholar
  63. Keysers C, Kaas JH, Gazzola V (2010) Somatosensation in social perception. Nat Rev Neurosci 11:417–428. doi: 10.1038/nrn2833 PubMedCrossRefGoogle Scholar
  64. Klöcker A, Arnould C, Penta M, Thonnard J-L (2012) Rasch-built measure of pleasant touch through active fingertip exploration. Front Neurorobot 6:5. doi: 10.3389/fnbot.2012.00005 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kumazawa T, Perl ER (1977) Primate cutaneous sensory units with unmyelinated (C) afferent fibers. J Neurophysiol 40:1325–1338PubMedGoogle Scholar
  66. Lechner SG, Lewin GR (2013) Hairy sensation. Physiology (Bethesda) 28:142–150. doi: 10.1152/physiol.00059.2012 CrossRefGoogle Scholar
  67. Li L, Rutlin M, Abraira VE et al (2011) The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147:1615–1627. doi: 10.1016/j.cell.2011.11.027 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Light AR, Trevino DL, Perl ER (1979) Morphological features of functionally defined neurons in the marginal zone and substantia gelatinosa of the spinal dorsal horn. J Comp Neurol 186:151–171. doi: 10.1002/cne.901860204 PubMedCrossRefGoogle Scholar
  69. Löken LS, Evert M, Wessberg J (2011) Pleasantness of touch in human glabrous and hairy skin: order effects on affective ratings. Brain Res 1417:9–15. doi: 10.1016/j.brainres.2011.08.011 PubMedCrossRefGoogle Scholar
  70. Löken LS, Wessberg J, Morrison I et al (2009) Coding of pleasant touch by unmyelinated afferents in humans. Nat Neurosci 12:547–548. doi: 10.1038/nn.2312 PubMedCrossRefGoogle Scholar
  71. Lumpkin EA, Marshall KL, Nelson AM (2010) The cell biology of touch. J Cell Biol 191:237–248. doi: 10.1083/jcb.201006074 PubMedPubMedCentralCrossRefGoogle Scholar
  72. Mackevicius EL, Best MD, Saal HP, Bensmaia SJ (2012) Millisecond precision spike timing shapes tactile perception. J Neurosci 32:15309–15317. doi: 10.1523/JNEUROSCI.2161-12.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Maksimovic S, Nakatani M, Baba Y et al (2014) Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509:617–621. doi: 10.1038/nature13250 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Maricich SM, Morrison KM, Mathes EL, Brewer BM (2012) Rodents rely on Merkel cells for texture discrimination tasks. J Neurosci 32:3296–3300. doi: 10.1523/JNEUROSCI.5307-11.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  75. McCabe C, Rolls ET, Bilderbeck A, McGlone F (2008) Cognitive influences on the affective representation of touch and the sight of touch in the human brain. Soc Cogn Affect Neurosci 3:97–108. doi: 10.1093/scan/nsn005 PubMedPubMedCentralCrossRefGoogle Scholar
  76. McGlone F, Olausson H, Boyle JA et al (2012) Touching and feeling: differences in pleasant touch processing between glabrous and hairy skin in humans. Eur J Neurosci 35:1782–1788. doi: 10.1111/j.1460-9568.2012.08092.x PubMedCrossRefGoogle Scholar
  77. McGlone F, Wessberg J, Olausson H (2014) Discriminative and affective touch: sensing and feeling. Neuron 82:737–755. doi: 10.1016/j.neuron.2014.05.001 PubMedCrossRefGoogle Scholar
  78. Miller M, Ralston HI, Kasahara M (1958) The pattern of cutaneous innervation of the human hand. Am J Anat 102:183–217PubMedCrossRefGoogle Scholar
  79. Mountcastle VB (1957) Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 20:408–434PubMedGoogle Scholar
  80. Murray EA, Mishkin M (1984) Relative contributions of SII and area 5 to tactile discrimination in monkeys. Behav Brain Res 11:67–83PubMedCrossRefGoogle Scholar
  81. Murray GM, Zhang HQ, Kaye AN et al (1992) Parallel processing in rabbit first (SI) and second (SII) somatosensory cortical areas: effects of reversible inactivation by cooling of SI on responses in SII. J Neurophysiol 68:703–710PubMedGoogle Scholar
  82. Nordin M (1990) Low-threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve. J Physiol 426:229–240PubMedPubMedCentralCrossRefGoogle Scholar
  83. Ochoa J, Mair WG (1969) The normal sural nerve in man. I. Ultrastructure and numbers of fibres and cells. Acta Neuropathol 13:197–216PubMedCrossRefGoogle Scholar
  84. Ochoa J, Torebjörk E (1989) Sensations evoked by intraneural microstimulation of C nociceptor fibres in human skin nerves. J Physiol 415:583–599PubMedPubMedCentralCrossRefGoogle Scholar
  85. Olausson H, Lamarre Y, Backlund H et al (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5:900–904. doi: 10.1038/nn896 PubMedCrossRefGoogle Scholar
  86. Olausson HW, Cole J, Vallbo A et al (2008) Unmyelinated tactile afferents have opposite effects on insular and somatosensory cortical processing. Neurosci Lett 436:128–132. doi: 10.1016/j.neulet.2008.03.015 PubMedCrossRefGoogle Scholar
  87. Padberg J, Recanzone G, Engle J et al (2010) Lesions in posterior parietal area 5 in monkeys result in rapid behavioral and cortical plasticity. J Neurosci 30:12918–12935. doi: 10.1523/JNEUROSCI.1806-10.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  88. Paré M, Behets C, Cornu O (2003) Paucity of presumptive ruffini corpuscles in the index finger pad of humans. J Comp Neurol 456:260–266. doi: 10.1002/cne.10519 PubMedCrossRefGoogle Scholar
  89. Pasalar S, Ro T, Beauchamp MS (2010) TMS of posterior parietal cortex disrupts visual tactile multisensory integration. Eur J Neurosci 31:1783–1790. doi: 10.1111/j.1460-9568.2010.07193.x PubMedPubMedCentralCrossRefGoogle Scholar
  90. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443. doi: 10.1093/brain/60.4.389 CrossRefGoogle Scholar
  91. Petit D, Burgess PR (1968) Dorsal column projection of receptors in cat hairy skin supplied by myelinated fibers. J Neurophysiol 31:849–855PubMedGoogle Scholar
  92. Pruszynski JA, Johansson RS (2014) Edge-orientation processing in first-order tactile neurons. Nat Neurosci 17:1404–1409. doi: 10.1038/nn.3804 PubMedCrossRefGoogle Scholar
  93. Randolph M, Semmes J (1974) Behavioral consequences of selective subtotal ablations in the postcentral gyrus ofMacaca mulatta. Brain Res 70:55–70. doi: 10.1016/0006-8993(74)90211-X PubMedCrossRefGoogle Scholar
  94. Rasmussen T, Penfield W (1947) The human sensorimotor cortex as studied by electrical stimulation. Fed Proc 6:184PubMedGoogle Scholar
  95. Rolls ET, O’Doherty J, Kringelbach ML et al (2003) Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cereb Cortex 13:308–317PubMedCrossRefGoogle Scholar
  96. Romo R, Hernández A, Zainos A et al (2002a) Exploring the cortical evidence of a sensory-discrimination process. Philos Trans R Soc Lond B Biol Sci 357:1039–1051. doi: 10.1098/rstb.2002.1100 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Romo R, Hernández A, Zainos A et al (2002b) Neuronal correlates of decision-making in secondary somatosensory cortex. Nat Neurosci 5:1217–1225. doi: 10.1038/nn950 PubMedCrossRefGoogle Scholar
  98. Rowe MJ, Turman AB, Murray GM, Zhang HQ (1996) Parallel organization of somatosensory cortical areas I and II for tactile processing. Clin Exp Pharmacol Physiol 23:931–938PubMedCrossRefGoogle Scholar
  99. Sanchez-Panchuelo RM, Besle J, Beckett A et al (2012) Within-digit functional parcellation of Brodmann areas of the human primary somatosensory cortex using functional magnetic resonance imaging at 7 tesla. J Neurosci 32:15815–15822. doi: 10.1523/JNEUROSCI.2501-12.2012 PubMedCrossRefGoogle Scholar
  100. Schlake T (2007) Determination of hair structure and shape. Semin Cell Dev Biol 18:267–273. doi: 10.1016/j.semcdb.2007.01.005 PubMedCrossRefGoogle Scholar
  101. Schmidt R, Schmelz M, Forster C et al (1995) Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15:333–341PubMedGoogle Scholar
  102. Schwartz GG, Rosenblum LA (1981) Allometry of primate hair density and the evolution of human hairlessness. Am J Phys Anthropol 55:9–12. doi: 10.1002/ajpa.1330550103 PubMedCrossRefGoogle Scholar
  103. Semba K, Masarachia P, Malamed S et al (1985) An electron microscopic study of terminals of rapidly adapting mechanoreceptive afferent fibers in the cat spinal cord. J Comp Neurol 232:229–240. doi: 10.1002/cne.902320208 PubMedCrossRefGoogle Scholar
  104. Semba K, Masarachia P, Malamed S et al (1983) An electron microscopic study of primary afferent terminals from slowly adapting type I receptors in the cat. J Comp Neurol 221:466–481. doi: 10.1002/cne.902210409 PubMedCrossRefGoogle Scholar
  105. Semba K, Masarachia P, Malamed S et al (1984) Ultrastructure of pacinian corpuscle primary afferent terminals in the cat spinal cord. Brain Res 302:135–150PubMedCrossRefGoogle Scholar
  106. Serra J, Campero M, Ochoa J, Bostock H (1999) Activity-dependent slowing of conduction differentiates functional subtypes of C fibres innervating human skin. J Physiol 515:799–811PubMedPubMedCentralCrossRefGoogle Scholar
  107. St John Smith E, Purfürst B, Grigoryan T et al (2012) Specific paucity of unmyelinated C-fibers in cutaneous peripheral nerves of the African naked-mole rat: comparative analysis using six species of Bathyergidae. J Comp Neurol 520:2785–2803. doi: 10.1002/cne.23133 PubMedCrossRefGoogle Scholar
  108. Stark B, Carlstedt T, Hallin RG, Risling M (1998) Distribution of human pacinian corpuscles in the hand a cadaver study. J Hand Surg Am 23B:370–372CrossRefGoogle Scholar
  109. Sugiura Y (1996) Spinal organization of C-fiber afferents related with nociception or non-nociception. Prog Brain Res 113:320–339PubMedGoogle Scholar
  110. Trulsson M (2001) Mechanoreceptive afferents in the human sural nerve. Exp Brain Res 137:111–116. doi: 10.1007/s002210000649 PubMedCrossRefGoogle Scholar
  111. Trulsson M, Essick GK (1997) Low-threshold mechanoreceptive afferents in the human lingual nerve. J Neurophysiol 77:737–748PubMedGoogle Scholar
  112. Trulsson M, Essick GK (2010) Sensations evoked by microstimulation of single mechanoreceptive afferents innervating the human face and mouth. J Neurophysiol 103:1741–1747. doi: 10.1152/jn.01146.2009 PubMedCrossRefGoogle Scholar
  113. Usoskin D, Furlan A, Islam S et al (2014) Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat Neurosci 18:145–153. doi: 10.1038/nn.3881 PubMedCrossRefGoogle Scholar
  114. Vallbo Å, Hagbarth K (1968) Activity from skin mechanoreceptors recorded percutaneously in awake human subjects. Exp Neurol 289:270–289CrossRefGoogle Scholar
  115. Vallbo Å, Olausson H, Wessberg J (1999) Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J Neurophysiol 81:2753–2763PubMedGoogle Scholar
  116. Vallbo A, Olausson H, Wessberg J, Norrsell U (1993) A system of unmyelinated afferents for innocuous mechanoreception in the human skin. Brain Res 628:301–304PubMedCrossRefGoogle Scholar
  117. Vallbo AB, Hagbarth K-E, Wallin BG (2004) Microneurography: how the technique developed and its role in the investigation of the sympathetic nervous system. J Appl Physiol 96:1262–1269. doi: 10.1152/japplphysiol.00470.2003 PubMedCrossRefGoogle Scholar
  118. Vallbo AB, Johansson RS (1984) Properties of cutaneous mechanoreceptors in the human hand related to touch sensation. Hum Neurobiol 3:3–14PubMedGoogle Scholar
  119. Vallbo AB, Olausson H, Wessberg J, Kakuda N (1995) Receptive field characteristics of tactile units with myelinated afferents in hairy skin of human subjects. J Physiol 483:783–795PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wall PD (1970) The sensory and motor role of impulses travelling in the dorsal columns towards cerebral cortex. Brain 93:505–524PubMedCrossRefGoogle Scholar
  121. Wall PD, Noordenbos W (1977) Sensory functions which remain in man after complete transection of dorsal columns. Brain 100:641–653PubMedCrossRefGoogle Scholar
  122. Weber AI, Saal HP, Lieber JD et al (2013) Spatial and temporal codes mediate the tactile perception of natural textures. Proc Natl Acad Sci U S A 110:17107–17112. doi: 10.1073/pnas.1305509110 PubMedPubMedCentralCrossRefGoogle Scholar
  123. Weddell G, Pallie W, Palmer E (1954) The morphology of peripheral nerve terminations in the skin. Q J Microsc Sci 95:483–501Google Scholar
  124. Wegner K, Forss N, Salenius S (2000) Characteristics of the human contra-versus ipsilateral SII cortex. Clin Neurophysiol 111:894–900PubMedCrossRefGoogle Scholar
  125. Weidner C, Schmelz M, Schmidt R et al (1999) Functional attributes discriminating mechano-insensitive and mechano-responsive C nociceptors in human skin. J Neurosci 19:10184–10190PubMedGoogle Scholar
  126. Weinstein S (1968) Intensive and extensive aspects of tactile sensitivity as a function of body part, sex and laterality. In: Kenshalo D (ed) The skin senses. Charles C. Thomas, Springfield, pp 192–222Google Scholar
  127. Wessberg J, Olausson H, Fernström KW, Vallbo AB (2003) Receptive field properties of unmyelinated tactile afferents in the human skin. J Neurophysiol 89:1567–1575. doi: 10.1152/jn.00256.2002 PubMedCrossRefGoogle Scholar
  128. Woo S-H, Ranade S, Weyer AD et al (2014) Piezo2 is required for Merkel-cell mechanotransduction. Nature 509(7502):622–626. doi: 10.1038/nature13251 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zhang HQ, Murray GM, Turman AB et al (1996) Parallel processing in cerebral cortex of the marmoset monkey: effect of reversible SI inactivation on tactile responses in SII. J Neurophysiol 76:3633–3655PubMedGoogle Scholar
  130. Zhang HQ, Zachariah MK, Coleman GT, Rowe MJ (2001) Hierarchical equivalence of somatosensory areas I and II for tactile processing in the cerebral cortex of the marmoset monkey. J Neurophysiol 85:1823–1835PubMedGoogle Scholar
  131. Zimmerman A, Bai L, Ginty DD (2014) The gentle touch receptors of mammalian skin. Science 346(6212):950–954. doi: 10.1126/science.1254229 PubMedPubMedCentralCrossRefGoogle Scholar
  132. Zotterman Y (1939) Touch, pain and tickling: an electro-physiological investigation on cutaneous sensory nerves. J Physiol 95:1–28PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Rochelle Ackerley
    • 1
    Email author
  • Helena Backlund Wasling
    • 2
  • Francis McGlone
    • 3
    • 4
  1. 1.Department of PhysiologyUniversity of GothenburgGöteborgSweden
  2. 2.Department of Neuroscience and PhysiologySahlgrenska Academy, University of GothenburgGöteborgSweden
  3. 3.Research Centre for Brain & Behaviour, School of Natural Sciences and PsychologyLiverpool John Moores UniversityLiverpoolUK
  4. 4.Institute of Psychology, Health & SocietyUniversity of LiverpoolLiverpoolUK

Personalised recommendations