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Journal of Molecular Neuroscience

, Volume 31, Issue 3, pp 289–296 | Cite as

Age alters the ability of substance P to sensitize joint nociceptors in Guinea pigs

Original Article
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Abstract

Pain perception is altered during senescence and it is thought that this could in part be due to changes in peripheral pain sensing processes. The present study examined the effect of substance P (SP) (10−10−10−8 mol; 0.1 mL bolus close intraarterial) on knee joint afferent mechanosensitivity in young (2- to 5-mo-old) and aged (17- to 36-mo-old) Dunkin-Hartley guinea pigs. Single unit electrophysiological recordings were made from knee joint primary afferent nerves in response to normal (nonnoxious) and painful (noxious) rotation of the joint. In young and old animals, local application of SP had a sensitizing effect on joint afferents in response to movements made in the normal working range of the knee. With noxious hyper-rotation of the joint, SP was able to increase afferent firing rate in young but not in old animals. These data demonstrate a lack of SP-mediated sensitization of joint nociceptors during senescence and suggest a peripheral deficiency in joint nociception with respect to age.

Index Entries

Age electrophysiology knee joint mechanosensory nerves neuropeptides nociception 

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References

  1. Bendele A. M. and Hulman J. F. (1988) Spontaneous cartilage degeneration in guinea pigs. Arthritis Rheum. 31, 561–565.PubMedCrossRefGoogle Scholar
  2. Berg B. N., Wolf A., and Simmshs (1962) Degenerative lesions of spinal roots and peripheral nerves in aging rats. Gerontologia 6, 72–80.PubMedCrossRefGoogle Scholar
  3. Bergman E., Johnson H., Zhang X., Hokfelt T., and Ulfhake B. (1996) Neuropeptides and neurotrophin receptor mRNAs in primary sensory neurons of aged rats. J. Comp. Neurol. 375, 303–319.PubMedCrossRefGoogle Scholar
  4. Carlton S. M., Zhou S., and Coggeshall R. E. (1996) Localization and activation of substance P receptors in unmyelinated axons of rat glabrous skin. Brain Res. 734, 103–108.PubMedCrossRefGoogle Scholar
  5. Cruce W. L., Lovell J. A., Crisp T., and Stuesse S. L. (2001) Effect of aging on the substance P receptor, NK-1, in the spinal cord of rats with peripheral nerve injury. Somatosens. Mot. Res. 18, 66–75.PubMedCrossRefGoogle Scholar
  6. de Paulis A., Marino I., Ciccarelli A., et al. (1996) Human synovial mast cells. I. Ultrastructural in situ and in vitro immunologic characterization. Arthritis Rheum. 39, 1222–1233.PubMedCrossRefGoogle Scholar
  7. Dhall U., Cowen T., Haven A. J., and Burnstock G. (1986) Perivascular noradrenergic and peptide-containing nerves show different patterns of changes during development and ageing in the guinea-pig. J. Auton. Nerv. Sys. 16, 109–126.CrossRefGoogle Scholar
  8. Felson D. T. (1995) The epidemiology of osteoarthritis: prevalence and risk factors, in Osteoarthritic Disorders (Kuettner K. E. and Goldberg C. H., eds). American Academy of Orthopaedic Surgeons, Rosemont, IL: pp 13–24.Google Scholar
  9. Gibson S. J. and Farrell M. (2004) A review of age differences in the neurophysiology of nociception and the perceptual experience of pain. Clin. J. Pain 20, 227–239.PubMedCrossRefGoogle Scholar
  10. Grigg P., Schaible H. G., and Schmidt R. F. (1986) Mechanical sensitivity of group III and IV afferents from posterior articular nerve in normal and inflamed cat knee. J. Neurophysiol. 55, 635–643.PubMedGoogle Scholar
  11. Guilbaud G., Iggo A., and Tegner R. (1985) Sensory receptors in ankle joint capsules of normal and arthritic rats. Exp. Brain Res. 58, 29–40.PubMedCrossRefGoogle Scholar
  12. Hanesch U., Pawlak M., and McDougall J. J. (2003) Gabapentin reduces the mechanosensitivity of fine afferent nerve fibres in normal and inflamed rat knee joints. Pain 104, 363–366.PubMedCrossRefGoogle Scholar
  13. Hannan M. T., Felson D. T., and Pincus T. (2000) Analysis of the discordance between radiographic changes and knee pain in osteoarthritis of the knee. J. Rheumatol. 27, 1513–1517.PubMedGoogle Scholar
  14. Harkins S. W. and Chapman C. R. (1976) Detection and decision factors in pain perception in young and elderly men. Pain 2, 253–264.PubMedCrossRefGoogle Scholar
  15. Harkins S. W. and Chapman C. R. (1977) The perception of induced dental pain in young and elderly women. J. Gerontol. 32, 428–435.PubMedGoogle Scholar
  16. Heppelmann B. and Pawlak M. (1997) Sensitisation of articular afferents in normal and inflamed knee joints by substance P in the rat. Neurosci. Lett. 223, 97–100.PubMedCrossRefGoogle Scholar
  17. Heppelmann B. and McDougall J. J. (2005) Inhibitory effect of amiloride and gadolinium on fine afferent nerves in the rat knee. Evidence of mechanogated ion channels in joints. Exp. Brain Res. 167, 114–118.PubMedCrossRefGoogle Scholar
  18. Heppelmann B., Messlinger K., Neiss W. F., and Schmidt R. F. (1995) Fine sensory innervation of the knee joint capsule by group III and group IV nerve fibers in the cat. J. Comp. Neurol. 351, 415–428.PubMedCrossRefGoogle Scholar
  19. Huebner J. L., Hanes M. A., Beekman B., TeKoppele J. M., and Kraus V. B. (2002) A comparative analysis of bone and cartilage metabolism in two strains of guinea-pig with varying degrees of naturally occurring osteoarthritis. Osteoarthritis Cart. 10, 758–767.CrossRefGoogle Scholar
  20. Hukkanen M., Grönblad M., Rees R., et al. (1991) Regional distribution of mast cells and peptide containing nerves in normal and adjuvant arthritic rat synovium. J. Rheumatol. 18, 177–183.PubMedGoogle Scholar
  21. Jinks C., Jordan K., and Croft P. (2002) Measuring the population impact of knee pain and disability with the Western Ontario and McMaster Universities Osteoarthritis Index (WOMAC). Pain 100, 55–64.PubMedCrossRefGoogle Scholar
  22. Kitagawa J., Kanda K., Sugiura M., et al. (2005) Effect of chronic inflammation on dorsal horn nociceptive neurons in aged rats. J. Neurophysiol. 93, 3594–3604.PubMedCrossRefGoogle Scholar
  23. Lawrence R. C., Helmick C. G., Arnett F. C., et al. (1998) Estimates of the prevalence of arthritis and selected musculoskeletal disorders in the United States. Arthritis Rheum. 41, 778–799.PubMedCrossRefGoogle Scholar
  24. McDougall J. J., Pawlak M., Hanesch U., and Schmidt R. F. (2000) Peripheral modulation of rat knee joint afferent mechanosensitivity by nociceptin/orphanin FQ. Neurosci. Lett. 288, 123–126.PubMedCrossRefGoogle Scholar
  25. McDougall J. J., Hanesch U., Pawlak M., and Schmidt R. F. (2001) Participation of NK1 receptors in nociceptin-induced modulation of rat knee joint mechanosensitivity. Exp. Brain Res. 137, 249–253.PubMedCrossRefGoogle Scholar
  26. Pawlak M., Schmidt R. F., Heppelmann B., and Hanesch U. (2001) The neurokinin-1 receptor antagonist RP 67580 reduces the sensitization of primary afferents by substance P in the rat. Eur. J. Pain 5, 69–79.PubMedCrossRefGoogle Scholar
  27. Piotrowski W. and Foreman J. C. (1985) On the actions of substance P, somatostatin, and vasoactive intestinal polypeptide on rat peritoneal mast cells and in human skin. Naunyn-Schmiedeberg’s Arch. Pharmacol. 331, 364–368.CrossRefGoogle Scholar
  28. Sakai K., Matsuno H., Tsuji H., and Tohyama M. (1998) Substance P receptor (NK1) gene expression in synovial tissue in rheumatoid arthritis and osteoarthritis. Scand. J. Rheumatol. 27, 135–141.PubMedCrossRefGoogle Scholar
  29. Samorajski T. (1974) Age differences in the morphology of posterior tibial nerves of mice. J. Comp. Neurol. 157, 439–445.PubMedCrossRefGoogle Scholar
  30. Schaible H. G. and Schmidt R. F. (1983a) Responses of fine medial articular nerve afferents to passive movements of knee joints. J. Neurophysiol. 49, 1118–1126.PubMedGoogle Scholar
  31. Schaible H. G. and Schmidt R. F. (1983b) Activation of groups III and IV sensory units in medial articular nerve by local mechanical stimulation of knee joint. J. Neurophysiol. 49, 35–44.PubMedGoogle Scholar
  32. Schaible H. G. and Schmidt R. F. (1985) Effects of an experimental arthritis on the sensory properties of fine articular afferent units. J. Neurophysiol. 54, 1109–1122.PubMedGoogle Scholar
  33. Schepelmann K., Messlinger K., Schaible H. G., and Schmidt R. F. (1992) Inflammatory mediators and nociception in the joint: excitation and sensitization of slowly conducting afferent fibers of cat’s knee by prostaglandin 12. Neurosci. 50, 237–247.CrossRefGoogle Scholar
  34. Schuelert N. and McDougall J. J. (2006) Electrophysiological evidence that the vasoactive intestinal peptide receptor antagonist VIP(6–28) reduces nociception in an animal model of osteoarthritis. Osteoarthritis Cart. 14, 1155–1162.CrossRefGoogle Scholar
  35. Sharma A. K., Bajada S., and Thomas P. K. (1980) Age changes in the tibial and plantar nerves of the rat. J. Anat. 130, 417–428.PubMedGoogle Scholar
  36. Skofitsch G., Donnerer J., Petronijevic S., Saria A., and Lembeck F. (1983) Release of histamine by neuropeptides from the perfused rat hindquarter. Naunyn-Schmiedeberg’s Arch. Pharmacol. 322, 153–157.CrossRefGoogle Scholar

Copyright information

© Humana Press Inc 2007

Authors and Affiliations

  1. 1.Department of Physiology and BiophysicsUniversity of CalgaryCalgaryCanada

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