Advertisement

Dynamic Changes in Dorsal Horn Neurons

  • W. D. WillisJr.
Conference paper
Part of the NATO ASI Series book series (volume 79)

Abstract

The responses of dorsal horn neurons to somatosensory stimulation can be altered under a variety of circumstances. For example, somatosensory responses of spinal cord dorsal horn neurons can be decreased by 1) habituation following repeated stimulation of the excitatory receptive field;46 2) stimulation of an inhibitory receptive field;30 3) activity in descending inhibitory pathways81 and 4) pathological changes leading to loss of primary afferent fibers.13 Conversely, somatosensory responses can be increased by such manipulations as 1) repeated stimulation of fine calibre primary afferent fibers (“wind-up”);47 2) spatial summation of excitatory inputs from different parts of the receptive field;49 3) volleys in excitatory pathways descending from the brain;80 and 4) sensitization of primary afferent fibers37 or of dorsal horn neurons as a consequence of damage to peripheral tissue or peripheral nerves.19,57

Keywords

Receptive Field Dorsal Horn Intradermal Injection Dorsal Horn Neuron Spinal Cord Dorsal Horn 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Aniksztejn, L., Otani, S. and Ben-Ari, Y. (1992) Quisqualate metabotropic receptors modulate NMDA currents and facilitate induction of long-term potentiation through protein kinase C. Europ. J. Neurosci. 4, 500–505.CrossRefGoogle Scholar
  2. 2.
    Baba, A., Etoh, S. and Iawata, H. (1991) Inhibition of NMDA-induced protein kinase C translocation by a Zn2+ chelator: implication of intracellular Zn2+. Brain Res. 557, 103–108.PubMedCrossRefGoogle Scholar
  3. 3.
    Battaglia, G. and Rustioni, A. (1988) Coexistence of glutamate and substance P in dorsal root ganglion neurons of the rat and monkey. J. Comp. Neurol. 277, 302–312.PubMedCrossRefGoogle Scholar
  4. 4.
    Baumann, T.K., Simone, D.A., Shain, C.N. and Lamotte, R.H. (1991) Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J. Neurophysiol. 66, 212–227.PubMedGoogle Scholar
  5. 5.
    Ben-Ari, Y., Aniksztejn, L. and Bregestovski, P. (1992) Protein kinase C modulation of NMDA currents: an important link for LTP induction. TINS 15, 333–339.PubMedGoogle Scholar
  6. 6.
    Bessou, P. and Perl, E.R. (1969) Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol. 32, 1025–1043.PubMedGoogle Scholar
  7. 7.
    Bonica, J.J. The management of pain. (1990) 2nd ed. Lea & Febiger, Philadelphia.Google Scholar
  8. 8.
    Bredt, D.S. and Snyder, S.H. (1992) Nitric oxide, a novel neuronal messenger. Neuron 8, 3–11.PubMedCrossRefGoogle Scholar
  9. 9.
    Carlton, S.M., Lamotte, C.C., Honda, C.N., Surmeier, D.J., Delanerolle, N.C. and Willis, W.D. (1985) Ultrastructural analysis of substance P and other synaptic profiles innervating an identified primate spinothalamic tract neuron. Neurosci. Abstr. 11, 578.Google Scholar
  10. 10.
    Carlton, S.M., Westlund, K.N., Zhang, D., Sorkin, L.S. and Willis, W.D. (1990) Calcitonin gene-related peptide containing primary afferent fibers synapse on primate spinothalamic tract cells. Neurosci. Lett. 109, 76–81.PubMedCrossRefGoogle Scholar
  11. 11.
    Chen, L. and Huang, L.Y.M. (1991) Sustained potentiation of NMDA receptor-mediated glutamate responses through activation of protein kinase C by a µ opioid. Neuron 7, 319–326.PubMedCrossRefGoogle Scholar
  12. 12.
    Chung, J.M., Kenshalo, D.R., Jr., Gerhart, K.D. and Willis, W.D. (1979) Excitation of primate spinothalamic neurons by cutaneous C-fiber volleys. J. Neurophysiol. 42, 1354–1369.PubMedGoogle Scholar
  13. 13.
    Chung, J.M., Paik, K.S., Kim, J.S., Nam, S.C., Kim, K.J., Oh, U.T., Hasegawa, T., Chung, K. and Willis, W.D. (1993) Chronic effects of topical application of capsaicin to the sciatic nerve on responses of primate spinothalamic neurons. Pain (in press).Google Scholar
  14. 14.
    Chung, K., Lee, W.T. and Carlton, S.M. (1988) The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide- labeled terminals in the rat lumbar dorsal horn. Neurosci. Lett. 90, 27–32.PubMedCrossRefGoogle Scholar
  15. 15.
    Collingridge, G.L. and Lester, R.A.J. (1989) Excitatory amino acid receptors in the vertebrate central nervous system. Pharmacol. Rev. 40, 143–210.Google Scholar
  16. 16.
    Craig, A.D. and Kniffki, K.D. (1985) Spinothalamic lumbosacral lamina I cells responsive to skin and muscle stimulation in the cat. J. Physiol. 365, 197–221.PubMedGoogle Scholar
  17. 17.
    Curtis, D.R., Phillis, J.W. and Watkins, J.C. (1960) The chemical excitation of spinal neurones by certain acidic amino acids. J. Physiol. 150, 656–682.PubMedGoogle Scholar
  18. 18.
    De Biasi, S. and Rustioni, A. (1988) Glutamate and substance P coexist in primary afferent terminals in superficial laminae of spinal cord. Proc. Natl. Acad. Sci. USA 85, 7820–7824.PubMedCrossRefGoogle Scholar
  19. 19.
    Dougherty, P.M. and Willis, W.D. (1991) Enhancement of spinothalamic neuron responses to chemical and mechanical stimuli following combined micro-iontophoretic application of N-methyl-D-aspartic acid and substance P. Pain 47, 85–93.PubMedCrossRefGoogle Scholar
  20. 20.
    Dougherty, P.M. and Willis, W.D. (1992) Enhanced responses of spinothalamic tract neurons to excitatory amino acids accompany capsaicin-induced sensitization in the monkey. J. Neuroscience 12, 883–894.Google Scholar
  21. 21.
    Dougherty, P.M., Palecek, J., Paleckova, V., Sorkin, L.S. and Willis, W.D. (1992) The role of NMDA and non-NMDA excitatory amino acid receptors in the excitation of primate spinothalamic tract cells by mechanical, chemical, thermal and electrical stimuli. J. Neuroscience 12, 3025–3041.Google Scholar
  22. 22.
    Dougherty, P.M., Palecek, J., Zorn, S. and Willis, W.D. (1993) Combined application of excitatory amino acids and substance P produces long-lasting changes in responses of primate spinothalamic tract neurons. Brain Res. Rev., Accepted.Google Scholar
  23. 23.
    East, S.J. and Garthwaite, J. (1990) Nanomolar NG-nitroarginine inhibits NMDA-induced cyclic GMP formation in rat cerebellum. Eur. J. Pharmacol. 184, 311–313.PubMedCrossRefGoogle Scholar
  24. 24.
    Eccles, J.C. (1964) The physiology of synapses. Springer-Verlag, New York.CrossRefGoogle Scholar
  25. 25.
    Etoh, S., Baba, A. and Iwata, H. (1991) NMDA induces protein kinase C translocation in hippocampal slices of immature rat brain. Neurosci. Lett. 126, 119–122.PubMedCrossRefGoogle Scholar
  26. 26.
    Ferrington, D.G., Sorkin, L.S. and Willis, W.D. (1987) Responses of spinothalamic tract cells in the superficial dorsal horn of the primate lumbar spinal cord. J. Physiol. 388, 681–703.PubMedGoogle Scholar
  27. 27.
    Fitzgerald, M. (1983) Capsaicin and sensory neurones-a review. Pain 15, 109–130.PubMedCrossRefGoogle Scholar
  28. 28.
    Fitzgerald, M. and Lynn, B. (1977) The sensitization of high threshold mechanoreceptors with myelinated axons by repeated heating. J. Physiol. 265, 549–563.PubMedGoogle Scholar
  29. 29.
    Gerber, G., Cerne, R. and Randic, M. (1991) Participation of excitatory amino acid receptors in the slow excitatory synaptic transmission in rat spinal dorsal horn. Brain Res. 561, 236–251.PubMedCrossRefGoogle Scholar
  30. 30.
    Gerhart, K.D., Yezierski, R.P., Giesler, G.J. and Willis, W.D. (1981) Inhibitory receptive fields of primate spinothalamic tract cells. J. Neurophysiol. 46, 309–1325.Google Scholar
  31. 31.
    Giesler, G.J., Yezierski, R.P., Gerhart, K.D. and Willis, W.D. (1981) Spinothalamic tract neurons that project to medial and/or lateral thalamic nuclei: evidence for a physiologically novel population of spinal cord neurons. J. Neurophysiol. 46, 1285–1308.PubMedGoogle Scholar
  32. 32.
    Gu, Y.P. and Huang, L.Y.M. (1989) Effects of excitatory amino acids on neurons isolated from spinal trigeminal nuclei. Neurosci. Abstr. 15, 947.Google Scholar
  33. 33.
    Hardy, J.D., Wolff, H.G. and Goodell, H. (1952) Pain sensations and reactions. Williams & Wilkins, New York (reprinted by Hafner, New York, 1967 ).Google Scholar
  34. 34.
    Helke, C.J., Krause, J.E., Mantyh, P.W., Couture, R. and Bannon, M.J. (1990) Diversity in mammalian tachykinin peptidergic neurons: multiple peptides, receptors, and regulatory mechanisms. FASEB J. 4, 606–1615.Google Scholar
  35. 35.
    Henry, J.L. (1976) Effects of substance P on functionally identified units in cat spinal cord. Brain Res. Bull. 114, 439–451.Google Scholar
  36. 36.
    Hunt, S.P., Kelly, J.S., Emson, P.C., Kimmel, J.R., Miller, R.J. and Wu, J.Y. (1981) An immunohistochemical study of neuronal populations containing neuropeptides or γ-aminobutyrate within the superficial layers of the rat dorsal horn. Neuroscience 6, 1883–1898.PubMedCrossRefGoogle Scholar
  37. 7.
    Kenshalo, D.R., Jr., Leonard, R.B., Chung, J.M. and Willis, W.D. (1979) Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J. Neurophysiol. 42, 1370–1389.PubMedGoogle Scholar
  38. 38.
    Kenshalo, D.R., Jr., Leonard, R.B., Chung, J.M. and Willis, W.D. (1982) Facilitation of the responses of primate spinothalamic cells to cold and to tactile stimuli by noxious heating of the skin. Pain 12, 41–152.CrossRefGoogle Scholar
  39. 39.
    Knowles, R.G., Palacios, M., Palmer, R.M.J. and Moncada, S. (1989) Formation of nitric oxide from L-arginine in the central nervous system: A transduction mechanism for stimulation of the soluble guanylate cyclase. Proc. Natl. Acad. Sci. USA 86, 5159–5162.PubMedCrossRefGoogle Scholar
  40. 40.
    Lamotte, R.H., Lundberg, L.E.R. and Torebjörk, H.E. (1992) Pain, hyperalgesia and activity in nociceptive C units in humans after intradermal injection of capsaicin. J. Physiol. 448, 749–764.PubMedGoogle Scholar
  41. 41.
    Lamotte, R.H., Shain, C.N., Simone, D.A. and Tsai, E.F.P. (1991) Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J. Neurophysiol. 66, 190–211.PubMedGoogle Scholar
  42. 42.
    Lamotte, R.H., Thalhammer, J.G. and Robinson, C.J. (1983) Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: a comparison of neural events in monkey with sensory judgments in human. J. Neurophysiol. 50, 1–26.PubMedGoogle Scholar
  43. 43.
    Lewis, T. (1942) Pain. Macmillan, New York.Google Scholar
  44. 44.
    Lynn, B. (1990) Capsaicin: actions on nociceptive C-fibres and therapeutic potential. Pain 41, 61–69.PubMedCrossRefGoogle Scholar
  45. 45.
    Macdermott, A.B., Mayer, M.L., Westbrook, G.L., Smith, S.J. and Barker, J.L. (1986) NMDA-receptor activation increases cytoplasmic calcium concentration in cultured spinal cord neurones. Nature 321, 519–522.PubMedCrossRefGoogle Scholar
  46. 46.
    Maunz, R.A., Pitts, N.G. and Peterson, B.W. (1978) Cat spinoreticular neurons: locations, responses and changes in responses during repetitive stimulation. Brain Res. 148, 365–379.PubMedCrossRefGoogle Scholar
  47. 47.
    Mendell, L.M. (1966) Physiological properties of unmyelinated fiber projection to the spinal cord. Exp. Neurol. 16, 316–332.PubMedCrossRefGoogle Scholar
  48. 48.
    Meyer, R.A. and Campbell, J.N. (1981) Myelinated nociceptive afferents account for the hyperalgesia that follows a burn to the hand. Science 213, 1527–1529.PubMedCrossRefGoogle Scholar
  49. 49.
    Milne, R.J., Foreman, R.D., Giesler, G.J. and Willis, W.D. (1981) Convergence of cutaneous and pelvic visceral nociceptive inputs onto primate spinothalamic neurons. Pain 11, 163–183.PubMedCrossRefGoogle Scholar
  50. 50.
    Milne, R.J., Foreman, R.D. and Willis, W.D. (1982) Responses of primate spinothalamic neurons located in the sacral intermediomedial gray (Stilling’s nucleus) to proprioceptive input from the tail. Brain Res. 234, 227–236.PubMedCrossRefGoogle Scholar
  51. 51.
    Monaghan, D.T., Bridges, R.J. and Cotman, C.W. (1989) The excitatory amino acid receptors: their classes, pharmacology, and distinct properties in the function of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 29, 365–402.PubMedCrossRefGoogle Scholar
  52. 52.
    Murase, K., Ryu, P.D. and Randic, M. (1989) Excitatory and inhibitory amino acids and peptide-induced responses in acutely isolated rat spinal dorsal horn neurons. Neurosci. Lett. 103, 56–63.PubMedCrossRefGoogle Scholar
  53. 53.
    Murase, K., Ryu, P.D. and Randic, M. (1989) Tachykinins modulate multiple ionic conductances in voltage-clamped rat spinal dorsal horn neurons. J. Neurophysiol. 61, 854–865.PubMedGoogle Scholar
  54. 54.
    O’Dell, T.J., Hawkins, R.D., Kandel, E.R. and Arancio, O. (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. USA 88, 11285–11289.CrossRefGoogle Scholar
  55. 55.
    Osborne, N.N. and Ghazi, H. (1989) The effect of substance P and other tachykinins on inositol phospholipid hydrolysis in rabbit retina, superior colliculus and retinal cultures. Vision Res. 29, 757–764.PubMedCrossRefGoogle Scholar
  56. 56.
    Owens, C.M., Zhang, D. and Willis, W.D. (1992) Changes in the response states of primate spinothalamic tract cells caused by mechanical damage of the skin or activation of descending controls. J. Neurophysiol. 67, 1509–1527.PubMedGoogle Scholar
  57. 57.
    Palecek, J., Dougherty, P.M., Kim, S.H., Paleckova, V., Lekan, H., Chung, J.M., Carlton, S.M. and Willis, W.D. (1992) Responses of spinothalamic tract neurons to mechanical and thermal stimuli in an experimental model of peripheral neuropathy in primates. J. Neurophysiol. 68, 1951–1966.PubMedGoogle Scholar
  58. 58.
    Palecek, J., Palecková, V., Dougherty, P.M. and Willis, W.D. (1993) The effect of phorbol esters on the responses of primate spinothalamic neurons to mechanical and thermal stimuli. Submitted.Google Scholar
  59. 59.
    Palecek, J., Palecková, V., Dougherty, P.M. and Willis, W.D. (1993) The effect of trans-ACPD, a metabotropic excitatory amino acid agonist, on the responses of primate spinothalamic tract neurons. Submitted.Google Scholar
  60. 60.
    Palecková, V., Palecek, J., Mcadoo, D.J. and Willis, W.D. (1992) The non-NMDA antagonist CNQX prevents release of amino acids into the rat spinal cord dorsal horn evoked by sciatic nerve stimulation. Neurosci. Lett. 148, 19–22.PubMedCrossRefGoogle Scholar
  61. 61.
    Palecek, J., Palecková, V. and Willis, W.D. (1993) An inhibitor of nitric oxide synthase blocks sensitization of spinothalamic neurons after intradermal injection of capsaicin in primates. Submitted.Google Scholar
  62. 62.
    Randic, M., Hecimovic, H. and Ryu, P.D. (1990) Substance P modulates glutamate-induced currents in acutely isolated rat dorsal horn neurones. Neurosci. Lett. 117, 74–80.PubMedCrossRefGoogle Scholar
  63. 63.
    Randic, M., Ryu, P.D. and Urban, L. (1986) Effects of polyclonal and monoclonal antibodies to substance P on slow excitatory transmission in rat spinal dorsal horn. Brain Res. 383, 15–27.PubMedCrossRefGoogle Scholar
  64. 64.
    Schoepp, D.D. and Johnson, B.G. (1988) Excitatory amino acid agonist-antagonist interactions at 2-amino-4-phosphobutyric acid-sensitive quisqualate receptors coupled to phosphoinositide hydrolysis in slices of rat hippocampus. J. Neurochem. 50, 1605–1613.PubMedCrossRefGoogle Scholar
  65. 65.
    Simone, D.A., Sorkin, L.S., Oh, U., Chung, J.M., Owens, C., Lamotte, R.H. and Willis, W.D. (1991) Neurogenic hyperalgesia: central neural correlates in responses of spinothalamic tract neurons. J. Neurophysiol. 66, 228–246.PubMedGoogle Scholar
  66. 66.
    Sladeczek, F., Récasens, M. and Bockaert, J. (1988) A new mechanism for glutamate receptor action: phosphoinositide hydrolysis. TINS 11, 545–549.PubMedGoogle Scholar
  67. 67.
    Sugiyama, H., Ito, I. and Hirono, C. (1987) A new type of glutamate receptor linked to inositol phospholipid metabolism. Nature 325, 531–533.PubMedCrossRefGoogle Scholar
  68. 68.
    Tessler, A., Himes, B.T., Artymyshyn, R., Murray, M. and Goldberger, M.E. (1981) Spinal neurons mediate return of substance P following deafferentation of cat spinal cord. Brain Res. 230, 263–281.PubMedCrossRefGoogle Scholar
  69. 69.
    Torebjörk, H.E., Lundberg, L.E.R. and Lamotte, R.H. (1992) Central changes in processing of mechanoreceptive input in capsaicin-induced secondary hyperalgesia in humans. J. Physiol. 448, 765–780.PubMedGoogle Scholar
  70. 70.
    Trevino, D.L., Coulter, J.D. and Willis, W.D. (1973) Location of cells of origin of spinothalamic tract in lumbar enlargement of the monkey. J. Neurophysiol. 36, 750–761.PubMedGoogle Scholar
  71. 71.
    Urbán, L. and Dray, A. (1992) Synaptic activation of dorsal horn neurons by selective C-fibre excitation with capsaicin in the mouse spinal cord in vitro. Neuroscience 47, 693–702.PubMedCrossRefGoogle Scholar
  72. 72.
    Urbán, L. and Randic, M. (1984) Slow excitatory transmission in rat dorsal horn: possible mediation by peptides. Brain Res. 290, 336–341.PubMedCrossRefGoogle Scholar
  73. 73.
    Urbán, L., Willetts, J., Randic, M. and Papka, R.E. (1985) The acute and chronic effects of capsaicin on slow excitatory transmission in rat dorsal horn. Brain Res. 330, 390–396.PubMedCrossRefGoogle Scholar
  74. 74.
    Westlund, K.N., Carlton, S.M., Zhang, D. and Willis, W.D. (1992) Glutamate-immunoreactive terminals synapse on primate spinothalamic tract cells. J. Comp. Neurol. 322, 519–527.PubMedCrossRefGoogle Scholar
  75. 75.
    White, J.C. and Sweet, W.H. (1969) Pain and the neurosurgeon. Thomas. Springfield. 76. Willcockson, W.S., Chung, J.M., Hori, Y., Lee, K.H. and Willis, W.D. (1984) Effect of iontophoretically released peptides on primate spinothalamic tract cells. J. Neuroscience 4, 741–750.Google Scholar
  76. 77.
    Willis, W.D. (Ed.) (1992) Hyperalgesia andallodynia. Raven Press, New York.Google Scholar
  77. 78.
    Willis, W.D. and Coggeshall, R.E. (1991) Sensory mechanisms of the spinal cord. 2nd ed., Plenum Press, New York.Google Scholar
  78. 79.
    Willis, W.D., Palecek, J., Palecková, V., Ragland, J. and Dougherty, P.M. (1992) Neurokinin receptor antagonists modify the responses of primate STT neurons to cutaneous stimuli. Neurosci. Abstr. 18, 1023.Google Scholar
  79. 80.
    Yezierski, R.P., Gerhart, K.D., Schrock, B.J. and Willis, W.D. (1983) A further examination of effects of cortical stimulation on primate spinothalamic tract cells. J. Neurophysiol. 49, 424–441.PubMedGoogle Scholar
  80. 81.
    Zhang, D., Owens, C.M. and Willis, W.D. (1991) Two forms of inhibition of spinothalamic tract neurons produced by stimulation of the periaqueductal gray and the cerebral cortex. J. Neurophysiol. 65, 1567–1579.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1994

Authors and Affiliations

  • W. D. WillisJr.
    • 1
  1. 1.Department of Anatomy and Neurosciences and Marine Biomedical InstituteUniversity of Texas Medical BranchGalvestonUSA

Personalised recommendations