An investigation into the peripheral substrates involved in the tactile modulation of cutaneous pain with emphasis on the C-tactile fibres

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• 作者：David A. Mahns (1) (2)
  Saad S. Nagi (1) (2)
  
• 关键词：C fibre ; Cutaneous pain ; Allodynia ; Hypertonic saline ; Vibration ; Intradermal anaesthesia
• 刊名：Experimental Brain Research
• 出版年：2013
• 出版时间：June 2013
• 年：2013
• 卷：227
• 期：4
• 页码：457-465
• 全文大小：440KB
• 参考文献：1. Andrew D (2010) Quantitative characterization of low-threshold mechanoreceptor inputs to lamina I spinoparabrachial neurons in the rat. J Physiol 588:117-24 CrossRef
  2. Andrews K, Baranowski A, Kinnman E (1999) Sensory threshold changes without initial pain or alterations in cutaneous blood flow, in the area of secondary hyperalgesia caused by topical application of capsaicin in humans. Neurosci Lett 266(1):45-8 CrossRef
  3. Arner S, Lindblom U, Meyerson B, Molander C (1990) Prolonged relief of neuralgia after regional anesthetic blocks. A call for further experimental and systematic clinical studies. Pain 43(3):287-97 CrossRef
  4. Ayles S, Graven-Nielsen T, Gibson W (2011) Vibration-induced afferent activity augments delayed onset muscle allodynia. J Pain 12(8):884-91 CrossRef
  5. Baron R (2009) Complex regional pain syndromes. In: Basbaum AI, Bushnell MC (eds) Science of pain. Elsevier, Oxford, pp 909-17
  6. Bessou P, Burgess PR, Perl ER, Taylor CB (1971) Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. J Neurophysiol 34(1):116-31
  7. Campbell JN, Raja SN, Meyer RA, Mackinnon SE (1988) Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32(1):89-4 CrossRef
  8. Cervero F, Laird J (1996) Mechanisms of touch-evoked pain (allodynia): a new model. Pain 68(1):13-3 CrossRef
  9. Cline M, Ochoa J, Torebj?rk H (1989) Chronic hyperalgesia and skin warming caused by sensitized C nociceptors. Brain 112(3):621-47 CrossRef
  10. Cole J, Bushnell MC, McGlone F, Elam M, Lamarre Y, Vallbo ?, Olausson H (2006) Unmyelinated tactile afferents underpin detection of low-force monofilaments. Muscle Nerve 34(1):105-07 CrossRef
  11. Dellon AL (1980) Clinical use of vibratory stimuli to evaluate peripheral nerve injury and compression neuropathy. Plast Reconstr Surg 65(4):466-76 CrossRef
  12. Douglas WW, Ritchie JM (1957) Non-medullated fibres in the saphenous nerve which signal touch. J Physiol 139(3):385-99
  13. Drake RL, Vogl W, Mitchell AWM (eds) (2005) Gray’s anatomy for students. Elsevier Churchill Livingstone, London
  14. Fillingim R, Fillingim L, Hollins M, Sigurdsson A, Maixner W (1998) Generalized vibrotactile allodynia in a patient with temporomandibular disorder. Pain 78(1):75-8 CrossRef
  15. Gracely R, Lynch S, Bennett G (1992) Painful neuropathy: altered central processing maintained dynamically by peripheral input. Pain 51(2):175-94 CrossRef
  16. Hallin RG, Torebj?rk HE (1976) Studies on cutaneous A and C fibre afferents, skin nerve blocks and perception. In: Zotterman Y (ed) Sensory functions of the skin in primates. Oxford University Press, London, pp 137-49
  17. Iggo A (1960) Cutaneous mechanoreceptors with afferent C fibres. J Physiol 152:337-53
  18. J?nig W (2011) Mechanical allodynia generated by stimulation of unmyelinated afferent nerve fibres. J Physiol 589(Pt 18):4407-408 CrossRef
  19. Johansson R, Trulsson M, Olsson K, Westberg K (1988) Mechanoreceptor activity from the human face and oral mucosa. Exp Brain Res 72(1):204-08 CrossRef
  20. Koltzenburg M, Torebj?rk H, Wahren L (1994) Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain 117(3):579-91 CrossRef
  21. Kumazawa T, Perl ER (1977) Primate cutaneous sensory units with unmyelinated (C) afferent fibers. J Neurophysiol 40(6):1325-338
  22. Landerholm ?H, Hansson PT (2011) Mechanisms of dynamic mechanical allodynia and dysesthesia in patients with peripheral and central neuropathic pain. Eur J Pain 15(5):498-03 CrossRef
  23. Li L, Rutlin M, Abraira Victoria E, Cassidy C, Kus L, Gong S, Jankowski Michael P, Luo W, Heintz N, Koerber HR, Woodbury CJ, Ginty David D (2011) The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147(7):1615-627 CrossRef
  24. Liljencrantz J, Bj?rnsdotter M, Morrison I, Bergstrand S, Ceko M, Seminowicz DA, Cole J, Bushnell MC, Olausson H (2013) Altered C-tactile processing in human dynamic tactile allodynia. Pain 154(2):227-34 CrossRef
  25. L?ken LS, Wessberg J, Morrison I, McGlone F, Olausson H (2009) Coding of pleasant touch by unmyelinated afferents in humans. Nat Neurosci 12(5):547-48 CrossRef
  26. L?ken LS, Evert M, Wessberg J (2011) Pleasantness of touch in human glabrous and hairy skin: order effects on affective ratings. Brain Res 1417:9-5 CrossRef
  27. Mackenzie RA, Burke D, Skuse NF, Lethlean AK (1975) Fibre function and perception during cutaneous nerve block. J Neurol Neurosurg Psychiatry 38(9):865-73 CrossRef
  28. Mahns DA, Perkins NM, Sahai V, Robinson L, Rowe MJ (2006) Vibrotactile frequency discrimination in human hairy skin. J Neurophysiol 95(3):1442-450 CrossRef
  29. Maih?fner C, Neund?rfer B, Stefan H, Handwerker H (2003) Cortical processing of brush-evoked allodynia. NeuroReport 14(6):785-89 CrossRef
  30. Maruhashi J, Mizuguchi K, Tasaki I (1952) Action currents in single afferent nerve fibres elicited by stimulation of the skin of the toad and the cat. J Physiol 117(2):129-51
  31. Melzack R (1975) Prolonged relief of pain by brief, intense transcutaneous somatic stimulation. Pain 1(4):357-73 CrossRef
  32. Melzack R, Wall P (1965) Pain mechanisms: a new theory. Science 150(3699):971-78 CrossRef
  33. Merskey H, Bogduk N (eds) (1994) Classification of chronic pain. Descriptions of chronic pain syndromes and definitions of pain terms, 2nd edn. IASP Press, Seattle
  34. Merzenich M, Harrington T (1969) The sense of flutter-vibration evoked by stimulation of the hairy skin of primates: comparison of human sensory capacity with the responses of mechanoreceptive afferents innervating the hairy skin of monkeys. Exp Brain Res 9(3):236-60 CrossRef
  35. Nagi SS, Mahns DA (2013) C-tactile fibers contribute to cutaneous allodynia after eccentric exercise. J Pain. doi:10.1016/j.jpain.2013.01.009
  36. Nagi SS, Rubin TK, Chelvanayagam DK, Macefield VG, Mahns DA (2011) Allodynia mediated by C-tactile afferents in human hairy skin. J Physiol 589(16):4065-075
  37. Nordin M (1990) Low-threshold mechanoreceptive and nociceptive units with unmyelinated (C) fibres in the human supraorbital nerve. J Physiol 426(1):229-40
  38. Ochoa J, Torebj?rk E (1989) Sensations evoked by intraneural microstimulation of C nociceptor fibres in human skin nerves. J Physiol 415(1):583-99
  39. Olausson H, Lamarre Y, Backlund H, Morin C, Wallin BG, Starck G, Ekholm S, Strigo I, Worsley K, Vallbo ?B, Bushnell MC (2002) Unmyelinated tactile afferents signal touch and project to insular cortex. Nat Neurosci 5(9):900-04 CrossRef
  40. Olausson H, Cole J, Rylander K, McGlone F, Lamarre Y, Wallin BG, Kr?mer H, Wessberg J, Elam M, Bushnell MC, Vallbo ? (2008) Functional role of unmyelinated tactile afferents in human hairy skin: sympathetic response and perceptual localization. Exp Brain Res 184(1):135-40 CrossRef
  41. Price D, Long S, Huitt C (1992) Sensory testing of pathophysiological mechanisms of pain in patients with reflex sympathetic dystrophy. Pain 49(2):163-73 CrossRef
  42. Richardson R, Arbit J, Siqueira E, Zagar R (1981) Transcutaneous electrical neurostimulation in functional pain. Spine 6(2):185-88 CrossRef
  43. Sahai V, Mahns D, Robinson L, Perkins N, Coleman G, Rowe M (2006) Processing of vibrotactile inputs from hairy skin by neurons of the dorsal column nuclei in the cat. J Neurophysiol 95(3):1451-464 CrossRef
  44. Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH (2009) Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 462:651-55 CrossRef
  45. Torebj?rk HE, Hallin RG (1973) Perceptual changes accompanying controlled preferential blocking of A and C fibre responses in intact human skin nerves. Exp Brain Res 16(3):321-32 CrossRef
  46. Torebj?rk HE, Lundberg LE, LaMotte RH (1992) Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J Physiol 448(1):765-80
  47. Treede R, Cole J (1993) Dissociated secondary hyperalgesia in a subject with a large-fibre sensory neuropathy. Pain 53(2):169-74 CrossRef
  48. Vallbo ?B, Olausson H, Wessberg J, Norrsell U (1993) A system of unmyelinated afferents for innocuous mechanoreception in the human skin. Brain Res 628(1-):301-04 CrossRef
  49. Vallbo ?B, Olausson H, Wessberg J (1999) Unmyelinated afferents constitute a second system coding tactile stimuli of the human hairy skin. J Neurophysiol 81(6):2753-763
  50. van Lieshout JJ, Wieling W, Karemaker JM, Eckberg DL (1991) The vasovagal response. Clin Sci 81(5):575-86
  51. Wasner G, Baron R, J?nig W (1999) Dynamic mechanical allodynia in humans is not mediated by a central presynaptic interaction of A beta-mechanoreceptive and nociceptive C-afferents. Pain 79(2-):113-19 CrossRef
  52. Weerakkody NS, Percival P, Hickey MW, Morgan DL, Gregory JE, Canny BJ, Proske U (2003) Effects of local pressure and vibration on muscle pain from eccentric exercise and hypertonic saline. Pain 105(3):425-35 CrossRef
  53. Wiklund Fernstr?m K (2004) Physiological properties of unmyelinated low-threshold tactile (CT) afferents in the human hairy skin. University of Gothenburg, Gothenburg
  54. Woolf C (1983) Evidence for a central component of post-injury pain hypersensitivity. Nature 306:686-88 CrossRef
  55. Woolf CJ, Salter MW (2000) Neuronal plasticity: increasing the gain in pain. Science 288:1765-768 CrossRef
  56. Woolf C, Thompson S (1991) The induction and maintenance of central sensitization is dependent on / N-methyl-d -aspartic acid receptor activation; implications for the treatment of post-injury pain hypersensitivity states. Pain 44(3):293-99 CrossRef
  57. Yarnitsky D, Ochoa JL (1991) Warm and cold specific somatosensory systems. Brain 114(4):1819-826 CrossRef
  58. Zar J (1984) Biostatistical analysis. Prentice-Hall International, NJ
  59. Zotterman Y (1939) Touch, pain and tickling: an electrophysiological investigation on cutaneous sensory nerves. J Physiol 95(1):1-8
  
• 作者单位：David A. Mahns (1) (2)
  Saad S. Nagi (1) (2)
  
  1. Department of Integrative Physiology, School of Medicine, University of Western Sydney, Penrith, Locked Bag 1797, Sydney, NSW, 2751, Australia
  2. Bioelectronics and Neuroscience Research Group, MARCS Institute, University of Western Sydney, Sydney, NSW, Australia
  
• ISSN：1432-1106

文摘

We recently demonstrated the emergence of touch-evoked pain (allodynia) during innocuous tactile stimulation of the skin overlying a painful muscle. This effect appeared to depend on a class of low-threshold unmyelinated mechanoafferents, termed C-tactile fibres (CT). In this study, we investigated the peripheral neurocircuitry of allodynia when pain originates in the skin. Psychophysical observations were carried out in 28 healthy subjects. Cutaneous pain was induced by infusing hypertonic saline (HS: 5?%) into the hairy skin overlying tibialis anterior muscle. An innocuous tactile stimulus (sinusoidal vibration: 200?Hz-200?μm) was concurrently applied to the hairy skin ~90?mm distal to the HS-infusion site. The contribution of different fibre classes to allodynia was determined by employing conduction blocks of myelinated (sciatic nerve compression) and unmyelinated (intradermal anaesthesia, Xylocaine 0.25?%) fibres. In absence of background nociceptive input, vibration was reported as non-painful. During cutaneous pain, vibration evoked a significant and reproducible increase in the overall pain intensity (allodynia). The blockade of myelinated fibres abolished the vibration sense, but the vibration-evoked allodynia persisted. Conversely, the blockade of unmyelinated cutaneous fibres abolished the allodynia (while the myelinated fibres were conducting or not). On the basis of these findings, in addition to our earlier work, we conclude that the allodynic effect of CT-fibre activation is not limited to nociceptive input arising from the muscle, but can be equally realized when pain originates in the skin. These results denote a broader role of CTs in pain modulation.