Functional properties of cutaneous A- and C-fibers 1-15 months after a nerve lesion

Journal of Neurophysiology

Volumn 102, Issue 6, 2009, Pages 3129-3141

  Gorodetskaya, Natalia ^a,b,c   Grossmann, Lydia ^a   Constantin, Cristina ^a,d   Jänig, Wilfrid ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b BOEHRINGER INGELHEIM PHARMA GMBH AND CO KG   (Germany)

^c PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

^d UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLD SENSITIVITY; CONTROLLED STUDY; CUTANEOUS A FIBER; CUTANEOUS C FIBER; FIBER; HEAT SENSITIVITY; MALE; MECHANICAL STIMULATION; NERVE CRUSH; NERVE ENDING; NERVE LESION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTIVE FIELD; REINNERVATION; SENSORY NERVE; SKIN STIMULATION; SURAL NERVE;

ANIMALS; BIOPHYSICS; CHI-SQUARE DISTRIBUTION; FOLLOW-UP STUDIES; MALE; NERVE FIBERS, MYELINATED; NERVE FIBERS, UNMYELINATED; PERIPHERAL NERVOUS SYSTEM DISEASES; PHYSICAL STIMULATION; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SENSORY THRESHOLDS; SKIN; SURAL NERVE; TIME FACTORS;

EID: 72749092637     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00203.2009     Document Type: Article

References (75)

1. Ali Z, Ringkamp M, Hartke TV, Chien HF, Flavahan NA, Campbell JN, Meyer RA. Uninjured C-fiber nociceptors develop spontaneous activity and alpha-adrenergic sensitivity following L6 spinal nerve ligation in monkey. J Neurophysiol 81: 455-466, 1999. (Pubitemid 29264493)
2. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41: 849-857, 2004. (Pubitemid 38429729)
3. Baron R, Jänig W, Kollmann W. Sympathetic and afferent somata projecting in hindlimb nerves and the anatomical organization of the lumbar sympathetic nervous system of the rat. J Comp Neurol 275: 460-468, 1988. (Pubitemid 18240167)
4. Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124: 1269-1282, 2006.
5. Belmonte C, Brock JA, Viana F. Converting cold into pain. Exp Brain Res 196: 13-30, 2009.
6. Belmonte C, Viana F. Molecular and cellular limits to somatosensory specificity (Abstract). Mol Pain 4: 14, 2008. (Pubitemid 351715887)
7. Blenk KH, Michaelis M, Vogel C, Jänig W. Thermosensitivity of acutely axotomized sensory nerve fibers. J Neurophysiol 76: 743-752, 1996. (Pubitemid 26284567)
8. Blumberg H, Jänig W. Discharge pattern of afferent fibers from a neuroma. Pain 20: 335-353, 1984. (Pubitemid 15176777)
9. Boring EG. Cutaneous sensation after nerve-division. Q J Exp Physiol 10: 1-95, 1916.
10. Brenan A, Jones L, Owain NR. The demonstration of the cutaneous distribution of saphenous nerve C-fibres using a plasma extravasation technique in the normal rat and following nerve injury. J Anat 157: 57-66, 1988. (Pubitemid 18108810)
11. Burgess PR, Horch KW. Specific regeneration of cutaneous fibers in the cat. J Neurophysiol 36: 101-114, 1973.
12. Caterina MJ. Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292: R64-R76, 2007. (Pubitemid 46098845)
13. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441, 1999. (Pubitemid 29180377)
14. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997. (Pubitemid 27462969)
15. Degn J, Tandrup T, Jakobsen J. Effect of nerve crush on perikaryal number and volume of neurons in adult rat dorsal root ganglion. J Comp Neurol 412: 186-192, 1999. (Pubitemid 29380334)
16. Diamond J, Coughlin M, Macintyre L, Holmes M, Visheau B. Evidence that endogenous beta nerve growth factor is responsible for the collateral sprouting, but not the regeneration, of nociceptive axons in adult rats. Proc Natl Acad Sci USA 84: 6596-6600, 1987.
17. Diamond J, Foerster A, Holmes M, Coughlin M. Sensory nerves in adult rats regenerate and restore sensory function to the skin independently of endogenous NGF. J Neurosci 12: 1467-1476, 1992.
18. Diamond J, Holmes M, Coughlin M. Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat. J Neurosci 12: 1454-1466, 1992.
19. Forster C, Handwerker HO. Automatic classification and analysis of microneurographic spike data using a PC/AT. J Neurosci Methods 31: 109-118, 1990. (Pubitemid 20044166)
20. Gorodetskaya N, Constantin C, Jänig W. Ectopic activity in cutaneous regenerating afferent nerve fibers following nerve lesion in the rat. Eur J Neurosci 18: 2487-2497, 2003. (Pubitemid 37452665)
21. Grossmann L, Gorodetskaya N, Baron R, Jänig W. Enhancement of spontaneous and evoked ectopic discharge in regenerating A- and C-fibers by inflammatory mediators. J Neurophysiol 101: 2762-2774, 2009b.
22. Grossmann L, Gorodetskaya N, Teliban A, Baron R, Jänig W. Regenerating cutaneous afferent C-fibers show two types of cold-sensitivity. Eur J Pain 13: 682-690, 2009a.
23. Head H, Sherren J. The consequences of injury to the peripheral nerves in man. Brain 28: 116-338, 1905.
24. Hoffmann P, Buck-Gramcko D, Lubahn JD. The Hoffmann-Tinel sign. 1915. J Hand Surg (Br) 18: 800-805, 1993.
25. Hökfelt T, Zhang X, Wiesenfeld-Hallin Z. Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci 17: 22-30, 1994. (Pubitemid 24024322)
26. Horch K. Guidance of regrowing sensory axons after cutaneous nerve lesions in the cat. J Neurophysiol 42: 1437-1449, 1979. (Pubitemid 10229775)
27. Horch KW, Lisney SJ. On the number and nature of regenerating myelinated axons after lesions of cutaneous nerves in the cat. J Physiol 313: 275-286, 1981.
28. Hu J, Milenkovic N, Lewin GR. The high threshold mechanotransducer: a status report. Pain 120: 3-7, 2006. (Pubitemid 43077164)
29. Hu P, McLachlan EM. Selective reactions of cutaneous and muscle afferent neurons to peripheral nerve transection in rats. J Neurosci 23: 10559-10567, 2003. (Pubitemid 37485269)
30. Jänig W, Grossmann L, Gorodetskaya N. Mechano- and thermosensitivity of regenerating cutaneous afferent nerve fibers. Exp Brain Res 196: 101-114, 2009.
31. Jänig W, McLachlan E. On the fate of sympathetic and sensory neurons projecting into a neuroma of the superficial peroneal nerve in the cat. J Comp Neurol 225: 302-311, 1984. (Pubitemid 14111849)
32. Jankowski MP, Lawson JJ, McIlwrath SL, Rau KK, Anderson CE, Albers KM, Koerber HR. Sensitization of cutaneous nociceptor after nerve transection and regeneration: possible role of target-derived neurotrophic factor signaling. J Neurosci 29: 1636-1647, 2009.
33. Jenq CB, Coggeshall RE. Regeneration of axons in tributary nerves. Brain Res 310: 107-121, 1984.
34. Johnson RD, Munson JB. Regenerating sprouts of axotomized cat muscle afferents express characteristic firing patterns to mechanical stimulation. J Neurophysiol 66: 2155-2158, 1991.
35. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427: 260-265, 2004. (Pubitemid 38112043)
36. Julius D, McCleskey EW. Cellular and molecular properties of primary afferent neurons. In: Wall and Melzack's Textbook of Pain (5th ed.), edited by McMahon SB, Koltzenburg M. Edinburgh: Elsevier Churchill Livingstone, 2006, p. 35-48.
37. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, Voets T. TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci USA 106: 1273-1278, 2009.
38. Koschorke GM, Meyer RA, Tillman DB, Campbell JN. Ectopic excitability of injured nerves in monkey: entrained responses to vibratory stimuli. J Neurophysiol 65: 693-701, 1991.
39. Kress M, Koltzenburg M, Reeh PW, Handwerker HO. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68: 581-595, 1992.
40. Kruger L, Silverman JD, Mantyh PW, Sternini C, Brecha NC. Peripheral patterns of calcitonin-gene-related peptide general somatic sensory innervation: cutaneous and deep terminations. J Comp Neurol 280: 291-302, 1989. (Pubitemid 19042138)
41. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50: 277-289, 2006.
42. Lawson JJ, McIlwrath SL, Woodbury CJ, Davis BM, Koerber HR. TRPV1 unlike TRPV2 is restricted to a subset of mechanically insensitive cutaneous nociceptors responding to heat. J Pain 9: 298-308, 2008.
43. Lawson SN. The peripheral sensory nervous system: dorsal root ganglion neurons. In: Peripheral Neuropathy (4th ed.), edited by Dyck P, Thomas PK. Amsterdam: Elsevier/Saunders, 2005, p. 163-202.
44. Leem JW, Willis WD, Chung JM. Cutaneous sensory receptors in the rat foot. J Neurophysiol 69: 1684-1699, 1993.
45. Lekan HA, Chung K, Yoon YW, Chung JM, Coggeshall RE. Loss of dorsal root ganglion cells concomitant with dorsal root axon sprouting following segmental nerve lesions. Neuroscience 81: 527-534, 1997. (Pubitemid 27382005)
46. Lewin GR, McMahon SB. Physiological properties of primary sensory neurons appropriately and inappropriately innervating skin in the adult rat. J Neurophysiol 66: 1205-1217, 1991.
47. Lewin GR, Moshourab R. Mechanosensation and pain. J Neurobiol 61: 30-44, 2004.
48. Lisney SJ. Regeneration of unmyelinated axons after injury of mammalian peripheral nerve. Q J Exp Physiol 74: 757-784, 1989. (Pubitemid 20078486)
49. McKemy DD, Neuhausser WM, Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416: 52-58, 2002. (Pubitemid 34215395)
50. McLachlan EM, Keast JR, Bauer M. SP- and CGRP-immunoreactive axons differ in their ability to reinnervate the skin of the rat tail. Neurosci Lett 176: 147-151, 1994. (Pubitemid 24241843)
51. Michaelis M, Blenk KH, Jänig W, Vogel C. Development of spontaneous activity and mechanosensitivity in axotomized afferent nerve fibers during the first hours after nerve transection in rats. J Neurophysiol 74: 1020-1027, 1995.
52. Michaelis M, Blenk KH, Vogel C, Jänig W. Distribution of sensory properties among axotomized cutaneous C-fibres in adult rats. Neuroscience 94: 7-10, 1999. (Pubitemid 29457590)
53. Navarro X, Vivo M, Valero-Cabre A. Neural plasticity after peripheral nerve injury and regeneration. Prog Neurobiol 82: 163-201, 2007. (Pubitemid 47088051)
54. Nealen ML, Gold MS, Thut PD, Caterina MJ. TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90: 515-520, 2003.
55. Proske U, Iggo A, Luff AR. Mechanical sensitivity of regenerating myelinated skin and muscle afferents in the cat. Exp Brain Res 104: 89-98, 1995.
56. Rajan B, Polydefkis M, Hauer P, Griffin JW, McArthur JC. Epidermal reinnervation after intracutaneous axotomy in man. J Comp Neurol 457: 24-36, 2003. (Pubitemid 36172570)
57. Reid G. ThermoTRP channels and cold sensing: what are they really up to? Pflügers Arch 451: 250-263, 2005. (Pubitemid 41424930)
58. Reid G, Babes A, Pluteanu F. A cold- and menthol-activated current in rat dorsal root ganglion neurones: properties and role in cold transduction. J Physiol 545: 595-614, 2002. (Pubitemid 36004391)
59. Rivera L, Gallar J, Pozo MA, Belmonte C. Responses of nerve fibres of the rat saphenous nerve neuroma to mechanical and chemical stimulation: an in vitro study. J Physiol 527: 305-313, 2000. (Pubitemid 30705957)
60. Rivers WHR, Head H. A human experiment in nerve division. Brain 31: 323-450, 1908.
61. Roza C, Belmonte C, Viana F. Cold sensitivity in axotomized fibers of experimental neuromas in mice. Pain 120: 24-35, 2006. (Pubitemid 43078588)
62. Sansone JM, Gatzke AM, Aslinia F, Rolak LA, Yale SH. Jules Tinel (1879-1952) and Paul Hoffman (1884 -1962). Clin Med Res 4: 85-89, 2006.
63. Scadding JW, Koltzenburg M. Painful peripheral neuropathies. In: Wall and Melzack's Textbook of Pain (5th ed.), edited by McMahon SB, Koltzenburg M. Edinburgh: Elsevier Churchill Livingstone, 2006, p. 973-999.
64. Schafer ES. Recovery after severance of cutaneous nerves. Brain 50: 538-545, 1927.
65. Shea VK, Perl ER. Regeneration of cutaneous afferent unmyelinated (C) fibers after transection. J Neurophysiol 54: 502-512, 1985. (Pubitemid 16217243)
66. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112: 819-829, 2003. (Pubitemid 36378884)
67. Sunderland S. Nerves and Nerve Injuries. Edinburgh: Churchill Livingstone, 1978.
68. Sunderland S. Nerve Injuries and Their Repair. A Critical Appraisal. Edinburgh: Churchill Livingstone, 1991.
69. Tandrup T, Woolf CJ, Coggeshall RE. Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. J Comp Neurol 422: 172-180, 2000. (Pubitemid 30390162)
70. Thut PD, Wrigley D, Gold MS. Cold transduction in rat trigeminal ganglia neurons in vitro. Neuroscience 119: 1071-1083, 2003. (Pubitemid 36776456)
71. Tinel J. "Tingling" signs with peripheral nerve injuries. La Presse Medicale 47: 388-389, 1915.
72. Trotter W, Davies HM. Experimental studies in the innervation of the skin. J Physiol 38: 134-246, 1909.
73. Woodbury CJ, Zwick M, Wang S, Lawson JJ, Caterina MJ, Koltzenburg M, Albers KM, Koerber HR, Davis BM. Nociceptors lacking TRPV1 and TRPV2 have normal heat responses. J Neurosci 24: 6410-6415, 2004. (Pubitemid 38944232)
74. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA. Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 21: RC140, 2001.
75. 2+. Nat Neurosci 10: 277-279, 2007.