Skip to main content

Advertisement

SpringerLink
Log in

Origins of antidromic activity in sensory afferent fibers and neurogenic inflammation

  • Review
  • Published:
Seminars in Immunopathology Aims and scope Submit manuscript

Abstract

Neurogenic inflammation results from the release of biologically active agents from the peripheral primary afferent terminal. This release reflects the presence of releasable pools of active product and depolarization-exocytotic coupling mechanisms in the distal afferent terminal and serves to alter the physiologic function of innervated organ systems ranging from the skin and meninges to muscle, bone, and viscera. Aside from direct stimulation, this biologically important release from the peripheral afferent terminal can be initiated by antidromic activity arising from five anatomically distinct points of origin: (i) afferent collaterals at the peripheral-target organ level, (ii) afferent collaterals arising proximal to the target organ, (iii) from mid-axon where afferents lacking myelin sheaths (C fibers and others following demyelinating injuries) may display crosstalk and respond to local irritation, (iv) the dorsal root ganglion itself, and (v) the central terminals of the afferent in the dorsal horn where local circuits and bulbospinal projections can initiate the so-called dorsal root reflexes, i.e., antidromic traffic in the sensory afferent.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Spitzer MJ, Reeh PW, Sauer SK (2008) Mechanisms of potassium- and capsaicin-induced axonal calcitonin gene-related peptide release: involvement of L- and T-type calcium channels and TRPV1 but not sodium channels. Neuroscience 151(3):836–842. https://doi.org/10.1016/j.neuroscience.2007.10.030

    Article  PubMed  CAS  Google Scholar 

  2. Kvamme E (1998) Synthesis of glutamate and its regulation. Prog Brain Res 116:73–85. https://doi.org/10.1016/S0079-6123(08)60431-8

    Article  PubMed  CAS  Google Scholar 

  3. Jimenez-Diaz L, Geranton SM, Passmore GM, Leith JL, Fisher AS, Berliocchi L, Sivasubramaniam AK, Sheasby A, Lumb BM, Hunt SP (2008) Local translation in primary afferent fibers regulates nociception. PLoS One 3(4):e1961. https://doi.org/10.1371/journal.pone.0001961

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Du J, Koltzenburg M, Carlton SM (2001) Glutamate-induced excitation and sensitization of nociceptors in rat glabrous skin. Pain 89(2):187–198. https://doi.org/10.1016/S0304-3959(00)00362-6

    Article  PubMed  CAS  Google Scholar 

  5. Zhou S, Komak S, Du J, Carlton SM (2001) Metabotropic glutamate 1alpha receptors on peripheral primary afferent fibers: their role in nociception. Brain Res 913(1):18–26. https://doi.org/10.1016/S0006-8993(01)02747-0

    Article  PubMed  CAS  Google Scholar 

  6. Hucho T, Levine JD (2007) Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 55(3):365–376. https://doi.org/10.1016/j.neuron.2007.07.008

    Article  PubMed  CAS  Google Scholar 

  7. Pellett S, Yaksh TL, Ramachandran R (2015) Current status and future directions of botulinum neurotoxins for targeting pain processing. Toxins (Basel) 7(11):4519–4563. https://doi.org/10.3390/toxins7114519

    Article  CAS  Google Scholar 

  8. Zamponi GW, Lewis RJ, Todorovic SM, Arneric SP, Snutch TP (2009) Role of voltage-gated calcium channels in ascending pain pathways. Brain Res Rev 60(1):84–89. https://doi.org/10.1016/j.brainresrev.2008.12.021

    Article  PubMed  CAS  Google Scholar 

  9. Kress M, Izydorczyk I, Kuhn A (2001) N- and L- but not P/Q-type calcium channels contribute to neuropeptide release from rat skin in vitro. Neuroreport 12(4):867–870. https://doi.org/10.1097/00001756-200103260-00048

    Article  PubMed  CAS  Google Scholar 

  10. Saxena VK, de Deyn PP, Schoups AA, Coen EP, de Potter WP (1989) Relationship between external calcium concentration and noradrenaline- and neuropeptide Y-evoked release from perfused dog spleen. Brain Res 486(2):310–315. https://doi.org/10.1016/0006-8993(89)90517-9

    Article  PubMed  CAS  Google Scholar 

  11. Just S, Heppelmann B (2002) Frequency dependent changes in mechanosensitivity of rat knee joint afferents after antidromic saphenous nerve stimulation. Neuroscience 112(4):783–789. https://doi.org/10.1016/S0306-4522(02)00125-2

    Article  PubMed  CAS  Google Scholar 

  12. Zhang X, Chen Y, Wang C, Huang LY (2007) Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. Proc Natl Acad Sci U S A 104(23):9864–9869. https://doi.org/10.1073/pnas.0611048104

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Gee MD, Lynn B, Cotsell B (1997) The relationship between cutaneous C fibre type and antidromic vasodilatation in the rabbit and the rat. J Physiol 503(Pt 1):31–44. https://doi.org/10.1111/j.1469-7793.1997.031bi.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Carpenter SE, Lynn B (1981) Vascular and sensory responses of human skin to mild injury after topical treatment with capsaicin. Br J Pharmacol 73(3):755–758. https://doi.org/10.1111/j.1476-5381.1981.tb16812.x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  15. Ferrell WR, Russell NJ (1986) Extravasation in the knee induced by antidromic stimulation of articular C fibre afferents of the anaesthetized cat. J Physiol 379(1):407–416. https://doi.org/10.1113/jphysiol.1986.sp016260

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Levine JD, Coderre TJ, Covinsky K, Basbaum AI (1990) Neural influences on synovial mast cell density in rat. J Neurosci Res 26(3):301–307. https://doi.org/10.1002/jnr.490260306

    Article  PubMed  CAS  Google Scholar 

  17. Lundberg JM, Brodin E, Hua X, Saria A (1984) Vascular permeability changes and smooth muscle contraction in relation to capsaicin-sensitive substance P afferents in the guinea-pig. Acta Physiol Scand 120(2):217–227. https://doi.org/10.1111/j.1748-1716.1984.tb00127.x

    Article  PubMed  CAS  Google Scholar 

  18. Michaelis M, Habler HJ, Jaenig W (1996) Silent afferents: a separate class of primary afferents? Clin Exp Pharmacol Physiol 23(2):99–105. https://doi.org/10.1111/j.1440-1681.1996.tb02579.x

    Article  PubMed  CAS  Google Scholar 

  19. Schmelz M, Michael K, Weidner C, Schmidt R, Torebjork HE, Handwerker HO (2000) Which nerve fibers mediate the axon reflex flare in human skin? Neuroreport 11(3):645–648. https://doi.org/10.1097/00001756-200002280-00041

    Article  PubMed  CAS  Google Scholar 

  20. Chiu IM, Heesters BA, Ghasemlou N, Von Hehn CA, Zhao F, Tran J, Wainger B, Strominger A, Muralidharan S, Horswill AR, Bubeck Wardenburg J, Hwang SW, Carroll MC, Woolf CJ (2013) Bacteria activate sensory neurons that modulate pain and inflammation. Nature 501(7465):52–57. https://doi.org/10.1038/nature12479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Pinter E, Helyes Z, Nemeth J, Porszasz R, Petho G, Than M, Keri G, Horvath A, Jakab B, Szolcsanyi J (2002) Pharmacological characterisation of the somatostatin analogue TT-232: effects on neurogenic and non-neurogenic inflammation and neuropathic hyperalgesia. Naunyn Schmiedeberg's Arch Pharmacol 366(2):142–150. https://doi.org/10.1007/s00210-002-0563-9

    Article  CAS  Google Scholar 

  22. Meyer RA, Davis KD, Cohen RH, Treede RD, Campbell JN (1991) Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res 561(2):252–261. https://doi.org/10.1016/0006-8993(91)91601-V

    Article  PubMed  CAS  Google Scholar 

  23. Malykhina AP, Qin C, Greenwood-van Meerveld B, Foreman RD, Lupu F, Akbarali HI (2006) Hyperexcitability of convergent colon and bladder dorsal root ganglion neurons after colonic inflammation: mechanism for pelvic organ cross-talk. Neurogastroenterol Motil 18(10):936–948. https://doi.org/10.1111/j.1365-2982.2006.00807.x

    Article  PubMed  CAS  Google Scholar 

  24. Sameda H, Takahashi Y, Takahashi K, Chiba T, Ohtori S, Moriya H (2001) Primary sensory neurons with dichotomizing axons projecting to the facet joint and the sciatic nerve in rats. Spine (Phila Pa 1976) 26(10):1105–1109. https://doi.org/10.1097/00007632-200105150-00003

    Article  CAS  Google Scholar 

  25. Ohtori S, Takahashi K, Chiba T, Yamagata M, Sameda H, Moriya H (2003) Calcitonin gene-related peptide immunoreactive neurons with dichotomizing axons projecting to the lumbar muscle and knee in rats. Eur Spine J 12(6):576–580. https://doi.org/10.1007/s00586-003-0573-4

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sameda H, Takahashi Y, Takahashi K, Chiba T, Ohtori S, Moriya H (2003) Dorsal root ganglion neurones with dichotomising afferent fibres to both the lumbar disc and the groin skin. A possible neuronal mechanism underlying referred groin pain in lower lumbar disc diseases. J Bone Joint Surg Br 85(4):600–603. https://doi.org/10.1302/0301-620X.85B4.13306

    Article  PubMed  CAS  Google Scholar 

  27. Langford LA, Coggeshall RE (1981) Branching of sensory axons in the peripheral nerve of the rat. J Comp Neurol 203(4):745–750. https://doi.org/10.1002/cne.902030411

    Article  PubMed  CAS  Google Scholar 

  28. Chung K, Coggeshall RE (1984) The ratio of dorsal root ganglion cells to dorsal root axons in sacral segments of the cat. J Comp Neurol 225(1):24–30. https://doi.org/10.1002/cne.902250104

    Article  PubMed  CAS  Google Scholar 

  29. McCarthy PW, Prabhakar E, Lawson SN (1995) Evidence to support the peripheral branching of primary afferent C-fibres in the rat: an in vitro intracellular electrophysiological study. Brain Res 704(1):79–84. https://doi.org/10.1016/0006-8993(95)01107-2

    Article  PubMed  CAS  Google Scholar 

  30. Ramer MS, Thompson SW, McMahon SB (1999) Causes and consequences of sympathetic basket formation in dorsal root ganglia. Pain Suppl 6:S111–S120

    Article  PubMed  CAS  Google Scholar 

  31. Xu Q, Yaksh TL (2011) A brief comparison of the pathophysiology of inflammatory versus neuropathic pain. Curr Opin Anaesthesiol 24(4):400–407. https://doi.org/10.1097/ACO.0b013e32834871df

    Article  PubMed  PubMed Central  Google Scholar 

  32. Hanani M (2012) Intercellular communication in sensory ganglia by purinergic receptors and gap junctions: implications for chronic pain. Brain Res 1487:183–191. https://doi.org/10.1016/j.brainres.2012.03.070

    Article  PubMed  CAS  Google Scholar 

  33. Waxman SG, Zamponi GW (2014) Regulating excitability of peripheral afferents: emerging ion channel targets. Nat Neurosci 17(2):153–163. https://doi.org/10.1038/nn.3602

    Article  PubMed  CAS  Google Scholar 

  34. Gouin O, L’Herondelle K, Lebonvallet N, Le Gall-Ianotto C, Sakka M, Buhe V, Plee-Gautier E, Carre JL, Lefeuvre L, Misery L, Le Garrec R (2017) TRPV1 and TRPA1 in cutaneous neurogenic and chronic inflammation: pro-inflammatory response induced by their activation and their sensitization. Protein Cell 8(9):644–661. https://doi.org/10.1007/s13238-017-0395-5

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Warwick RA, Hanani M (2013) The contribution of satellite glial cells to chemotherapy-induced neuropathic pain. Eur J Pain 17(4):571–580. https://doi.org/10.1002/j.1532-2149.2012.00219.x

    Article  PubMed  CAS  Google Scholar 

  36. Dublin P, Hanani M (2007) Satellite glial cells in sensory ganglia: their possible contribution to inflammatory pain. Brain Behav Immun 21(5):592–598. https://doi.org/10.1016/j.bbi.2006.11.011

    Article  PubMed  CAS  Google Scholar 

  37. Huang TY, Hanani M (2005) Morphological and electrophysiological changes in mouse dorsal root ganglia after partial colonic obstruction. Am J Physiol Gastrointest Liver Physiol 289(4):G670–G678. https://doi.org/10.1152/ajpgi.00028.2005

    Article  PubMed  CAS  Google Scholar 

  38. Zhang H, Mei X, Zhang P, Ma C, White FA, Donnelly DF, Lamotte RH (2009) Altered functional properties of satellite glial cells in compressed spinal ganglia. Glia 57(15):1588–1599. https://doi.org/10.1002/glia.20872

    Article  PubMed  PubMed Central  Google Scholar 

  39. Huang TY, Belzer V, Hanani M (2010) Gap junctions in dorsal root ganglia: possible contribution to visceral pain. Eur J Pain 14(49):e1–11

    Google Scholar 

  40. Hu P, Bembrick AL, Keay KA, McLachlan EM (2007) Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve. Brain Behav Immun 21(5):599–616. https://doi.org/10.1016/j.bbi.2006.10.013

    Article  PubMed  CAS  Google Scholar 

  41. McLachlan EM, Hu P (1998) Axonal sprouts containing calcitonin gene-related peptide and substance P form pericellular baskets around large diameter neurons after sciatic nerve transection in the rat. Neuroscience 84(4):961–965. https://doi.org/10.1016/S0306-4522(97)00680-5

    Article  PubMed  CAS  Google Scholar 

  42. McLachlan EM, Janig W, Devor M, Michaelis M (1993) Peripheral nerve injury triggers noradrenergic sprouting within dorsal root ganglia. Nature 363(6429):543–546. https://doi.org/10.1038/363543a0

    Article  PubMed  CAS  Google Scholar 

  43. Chung K, Yoon YW, Chung JM (1997) Sprouting sympathetic fibers form synaptic varicosities in the dorsal root ganglion of the rat with neuropathic injury. Brain Res 751(2):275–280. https://doi.org/10.1016/S0006-8993(96)01408-4

    Article  PubMed  CAS  Google Scholar 

  44. Xie WR, Deng H, Li H, Bowen TL, Strong JA, Zhang JM (2006) Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia. Neuroscience 142(3):809–822. https://doi.org/10.1016/j.neuroscience.2006.06.045

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Ramer MS, Bisby MA (1997) Rapid sprouting of sympathetic axons in dorsal root ganglia of rats with a chronic constriction injury. Pain 70(2):237–244. https://doi.org/10.1016/S0304-3959(97)03331-9

    Article  PubMed  CAS  Google Scholar 

  46. Murinson BB, Griffin JW (2004) C-fiber structure varies with location in peripheral nerve. J Neuropathol Exp Neurol 63(3):246–254. https://doi.org/10.1093/jnen/63.3.246

    Article  PubMed  Google Scholar 

  47. Griffin JW, Thompson WJ (2008) Biology and pathology of nonmyelinating Schwann cells. Glia 56(14):1518–1531. https://doi.org/10.1002/glia.20778

    Article  PubMed  Google Scholar 

  48. Murinson BB, Hoffman PN, Banihashemi MR, Meyer RA, Griffin JW (2005) C-fiber (Remak) bundles contain both isolectin B4-binding and calcitonin gene-related peptide-positive axons. J Comp Neurol 484(4):392–402. https://doi.org/10.1002/cne.20506

    Article  PubMed  CAS  Google Scholar 

  49. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, LaMotte RH (2003) Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89(3):1588–1602. https://doi.org/10.1152/jn.00855.2002

    Article  PubMed  Google Scholar 

  50. Xie Y, Zhang J, Petersen M, LaMotte RH (1995) Functional changes in dorsal root ganglion cells after chronic nerve constriction in the rat. J Neurophysiol 73(5):1811–1820. https://doi.org/10.1152/jn.1995.73.5.1811

    Article  PubMed  CAS  Google Scholar 

  51. Kajander K, Waikaka S, Bennett G (1992) Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat. Neurosci Lett 138(2):225–228. https://doi.org/10.1016/0304-3940(92)90920-3

    Article  PubMed  CAS  Google Scholar 

  52. Seltzer Z, Devor M (1979) Ephaptic transmission in chronically damaged peripheral nerves. Neurology 29(7):1061–1064. https://doi.org/10.1212/WNL.29.7.1061

    Article  PubMed  CAS  Google Scholar 

  53. Rasminsky M (1980) Ephaptic transmission between single nerve fibres in the spinal nerve roots of dystrophic mice. J Physiol 305(1):151–169. https://doi.org/10.1113/jphysiol.1980.sp013356

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Wu G, Ringkamp M, Murinson BB, Pogatzki EM, Hartke TV, Weerahandi HM, Campbell JN, Griffin JW, Meyer RA (2002) Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J Neurosci 22(17):7746–7753

    Article  PubMed  CAS  Google Scholar 

  55. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA (2001) Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. J Neurosci 21:RC140

    Article  PubMed  CAS  Google Scholar 

  56. Myers RR, Heckman HM, Rodriguez M (1996) Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice. Exp Neurol 141(1):94–101. https://doi.org/10.1006/exnr.1996.0142

    Article  PubMed  CAS  Google Scholar 

  57. Sorkin LS, Xiao WH, Wagner R, Myers RR (1997) Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 81(1):255–262. https://doi.org/10.1016/S0306-4522(97)00147-4

    Article  PubMed  CAS  Google Scholar 

  58. Moalem G, Grafe P, Tracey DJ (2005) Chemical mediators enhance the excitability of unmyelinated sensory axons in normal and injured peripheral nerve of the rat. Neuroscience 134(4):1399–1411. https://doi.org/10.1016/j.neuroscience.2005.05.046

    Article  PubMed  CAS  Google Scholar 

  59. Zelenka M, Schafers M, Sommer C (2005) Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116(3):257–263. https://doi.org/10.1016/j.pain.2005.04.018

    Article  PubMed  CAS  Google Scholar 

  60. Sorkin L, Doom C (2000) Epineurial application of TNF elecits an acute mechanical hyperalgesia in the awake rat. J Peripheral Nervous Sys 5(2):96–1000. https://doi.org/10.1046/j.1529-8027.2000.00012.x

    Article  CAS  Google Scholar 

  61. Bove GM, Leem J-G (2002) Mid-axonal tumor necrosis factor-alpha induces ectopic activity in a subset of slowly conducting cutaneous and deep afferent neurons. J Pain 3:45

    Article  PubMed  Google Scholar 

  62. Hoffmann T, Sauer SK, Horch RE, Reeh PW (2008) Sensory transduction in peripheral nerve axons elicits ectopic action potentials. J Neurosci 28(24):6281–6284. https://doi.org/10.1523/JNEUROSCI.1627-08.2008

    Article  PubMed  CAS  Google Scholar 

  63. Chung JM, Lee KH, Hori Y, Willis WD (1985) Effects of capsaicin applied to a peripheral nerve on the responses of primate spinothalamic tract cells. Brain Res 329(1-2):27–38. https://doi.org/10.1016/0006-8993(85)90509-8

    Article  PubMed  CAS  Google Scholar 

  64. Sauer SK, Reeh PW, Bove GM (2001) Noxious heat-induced CGRP release from rat sciatic nerve axons in vitro. Eur J Neurosci 14(8):1203–1208. https://doi.org/10.1046/j.0953-816x.2001.01741.x

    Article  PubMed  CAS  Google Scholar 

  65. Hoffmann T, Sauer SK, Horch RE, Reeh PW (2009) Projected pain from noxious heat stimulation of an exposed peripheral nerve--a case report. Eur J Pain 13(1):35–37. https://doi.org/10.1016/j.ejpain.2008.09.014

    Article  PubMed  CAS  Google Scholar 

  66. Bove GM, Ransil BJ, Lin HC, Leem JG (2003) Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. J Neurophysiol 90(3):1949–1955. https://doi.org/10.1152/jn.00175.2003

    Article  PubMed  Google Scholar 

  67. Toennies JF (1938) Reflex discharge from the spinal cord over the dorsal roots. J Neurophysiol 1(4):378–390. https://doi.org/10.1152/jn.1938.1.4.378

    Article  Google Scholar 

  68. Alvarez FJ, Kavookjian AM, Light AR (1992) Synaptic interactions between GABA-immunoreactive profiles and the terminals of functionally defined myelinated nociceptors in the monkey and cat spinal cord. J Neurosci 12(8):2901–2917

    Article  PubMed  CAS  Google Scholar 

  69. Singer E, Placheta P (1980) Reduction of [3H]muscimol binding sites in rat dorsal spinal cord after neonatal capsaicin treatment. Brain Res 202(2):484–487. https://doi.org/10.1016/0006-8993(80)90160-2

    Article  PubMed  CAS  Google Scholar 

  70. Carlton SM, Hayes ES (1990) Light microscopic and ultrastructural analysis of GABA-immunoreactive profiles in the monkey spinal cord. J Comp Neurol 300(2):162–182. https://doi.org/10.1002/cne.903000203

    Article  PubMed  CAS  Google Scholar 

  71. Todd AJ, Lochhead V (1990) GABA-like immunoreactivity in type I glomeruli of rat substantia gelatinosa. Brain Res 514(1):171–174. https://doi.org/10.1016/0006-8993(90)90454-J

    Article  PubMed  CAS  Google Scholar 

  72. Todd AJ (2015) Plasticity of inhibition in the spinal cord. Handb Exp Pharmacol 227:171–190. https://doi.org/10.1007/978-3-662-46450-2_9

    Article  PubMed  CAS  Google Scholar 

  73. Schmidt RF (1971) Presynaptic inhibition in the vertebrate nervous system. Rev Physiol Biochem Pharm 63:21–101

    Google Scholar 

  74. Jimenez I, Rudomin P, Solodkin M (1987) Mechanisms involved in the depolarization of cutaneous afferents produced by segmental and descending inputs in the cat spinal cord. Exp Brain Res 69(1):195–207

    Article  PubMed  CAS  Google Scholar 

  75. Willis WD Jr (1999) Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 124(4):395–421. https://doi.org/10.1007/s002210050637

    Article  PubMed  CAS  Google Scholar 

  76. Fitzgerald M, Woolf CJ (1981) Effects of cutaneous nerve and intraspinal conditioning of C-fibre afferent terminal excitability in decerebrate spinal rats. J Physiol 318(1):25–39. https://doi.org/10.1113/jphysiol.1981.sp013848

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  77. Lin Q, Zou X, Willis WD (2000) Adelta and C primary afferents convey dorsal root reflexes after intradermal injection of capsaicin in rats. J Neurophysiol 84(5):2695–2698. https://doi.org/10.1152/jn.2000.84.5.2695

    Article  PubMed  CAS  Google Scholar 

  78. Sluka KA, Rees H, Westlund KN, Willis WD (1995) Fiber types contributing to dorsal root reflexes induced by joint inflammation in cats and monkeys. J Neurophysiol 74(3):981–989. https://doi.org/10.1152/jn.1995.74.3.981

    Article  PubMed  CAS  Google Scholar 

  79. Cervero F, Laird JM (1996) Mechanisms of allodynia: interactions between sensitive mechanoreceptors and nociceptors. Neuroreport 7(2):526–528. https://doi.org/10.1097/00001756-199601310-00036

    Article  PubMed  CAS  Google Scholar 

  80. Cervero F, Laird JM (1996) Mechanisms of touch-evoked pain (allodynia): a new model. Pain 68(1):13–23. https://doi.org/10.1016/S0304-3959(96)03165-X

    Article  PubMed  CAS  Google Scholar 

  81. Rees H, Sluka KA, Westlund KN, Willis WD (1995) The role of glutamate and GABA receptors in the generation of dorsal root reflexes by acute arthritis in the anaesthetized rat. J Physiol Lond 484(2):437–445. https://doi.org/10.1113/jphysiol.1995.sp020676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Sluka KA, Westlund KN (1993) Centrally administered non-NMDA but not NMDA receptor antagonists block peripheral knee joint inflammation. Pain 55(2):217–225. https://doi.org/10.1016/0304-3959(93)90150-N

    Article  PubMed  CAS  Google Scholar 

  83. Sluka KA, Jordan HH, Westlund KN (1994) Reduction in joint swelling and hyperalgesia following post-treatment with a non-NMDA glutamate receptor antagonist. Pain 59(1):95–100. https://doi.org/10.1016/0304-3959(94)90052-3

    Article  PubMed  CAS  Google Scholar 

  84. Garcia-Ramirez DL, Calvo JR, Hochman S, Quevedo JN (2014) Serotonin, dopamine and noradrenaline adjust actions of myelinated afferents via modulation of presynaptic inhibition in the mouse spinal cord. PLoS One 9(2):e89999. https://doi.org/10.1371/journal.pone.0089999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Martin RF, Haber LH, Willis WD (1979) Primary afferent depolarization of identified cutaneous fibers following stimulation in medial brain stem. J Neurophysiol 42(3):779–790. https://doi.org/10.1152/jn.1979.42.3.779

    Article  PubMed  CAS  Google Scholar 

  86. Vinay L, Brocard F, Fellippa-Marques S, Clarac F (1999) Antidromic discharges of dorsal root afferents in the neonatal rat. J Physiol Paris 93(4):359–367. https://doi.org/10.1016/S0928-4257(00)80063-7

    Article  PubMed  CAS  Google Scholar 

  87. Owen MP, Hodge CJ Jr (1973) Positive dorsal root potentials evoked by stimulation of the brain stem reticular formation. Brain Res 54:305–308. https://doi.org/10.1016/0006-8993(73)90051-6

    Article  PubMed  CAS  Google Scholar 

  88. Lovick TA (1981) Primary afferent depolarization of tooth pulp afferents by stimulation in nucleus raphe magnus and the adjacent reticular formation in the cat: effects of bicuculline. Neurosci Lett 25(2):173–178. https://doi.org/10.1016/0304-3940(81)90327-X

    Article  PubMed  CAS  Google Scholar 

  89. Peng YB, Wu J, Willis WD, Kenshalo DR (2001) GABA(a) and 5-HT(3) receptors are involved in dorsal root reflexes: possible role in periaqueductal gray descending inhibition. J Neurophysiol 86(1):49–58. https://doi.org/10.1152/jn.2001.86.1.49

    Article  PubMed  CAS  Google Scholar 

  90. Lovick TA (1983) The role of 5-HT, GABA and opioid peptides in presynaptic inhibition of tooth pulp input from the medial brainstem. Brain Res 289(1-2):135–142. https://doi.org/10.1016/0006-8993(83)90014-8

    Article  PubMed  CAS  Google Scholar 

  91. Zeitz KP, Guy N, Malmberg AB, Dirajlal S, Martin WJ, Sun L, Bonhaus DW, Stucky CL, Julius D, Basbaum AI (2002) The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J Neurosci 22(3):1010–1019

    Article  PubMed  CAS  Google Scholar 

  92. Khasabov SG, Lopez-Garcia JA, Asghar AU, King AE (1999) Modulation of afferent-evoked neurotransmission by 5-HT3 receptors in young rat dorsal horn neurones in vitro: a putative mechanism of 5-HT3 induced anti-nociception. Br J Pharmacol 127(4):843–852. https://doi.org/10.1038/sj.bjp.0702592

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Levine JD, Dardick SJ, Basbaum AI, Scipio E (1985) Reflex neurogenic inflammation. I. Contribution of the peripheral nervous system to spatially remote inflammatory responses that follow injury. J Neurosci 5(5):1380–1386

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anesthesiology, University of California, San Diego, San Diego, CA, USA

    Linda S. Sorkin, Kelly A. Eddinger, Sarah A. Woller & Tony L. Yaksh

Authors
  1. Linda S. Sorkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kelly A. Eddinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sarah A. Woller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tony L. Yaksh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Linda S. Sorkin.

Additional information

This article is a contribution to the special issue on Neurogenic Inflammation - Guest Editors: Tony Yaksh and Anna Di Nardo

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sorkin, L.S., Eddinger, K.A., Woller, S.A. et al. Origins of antidromic activity in sensory afferent fibers and neurogenic inflammation. Semin Immunopathol 40, 237–247 (2018). https://doi.org/10.1007/s00281-017-0669-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00281-017-0669-2

Keywords

Search

Navigation