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Modulatory Effects of Descending Systems on Spinal Dorsal Horn Neurons

  • G. F. Gebhart

Abstract

It is well established that suprasegmental modulation of spinal reflexes and spinal neuronal responses can be demonstrated from widespread areas of the brain, including the brainstem, diencephalon, and cortex. Indeed, many of these spinal reflexes and neurons are tonically modulated from supraspinal sites. Early investigators employed lesions and intracerebral electrical stimulation to locate the site(s) of origin of descending control of flexion reflexes. Although these efforts were directed primarily toward understanding mechanisms of motor control, they also contributed significantly to our knowledge of sensory mechanisms and the suprasegmental modulation of nociception. Focal electrical brain stimulation and intracerebral drug microinjections are widely employed today to examine descending modulatory influences on spinal dorsal horn neurons and nociceptive reflexes, focusing often on “intrinsic” systems of pain control. This chapter considers descending inhibitory modulation of nociceptive transmission in the spinal cord, but it is important to recognize that centrifugal influences on somatosensory pathways can be either inhibitory or excitatory. The substrates for these spinopetal effects have been discussed further in the chapters by Hammond (Chapter 15), Ruda (Chapter 7), and LaMotte (Chapter 5).

Keywords

Dorsal Horn Spinal Dorsal Horn Dorsal Horn Neuron Spinal Dorsal Horn Neuron Nucleus Raphe Magnus 
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References

  1. Basbaum, A. I., and Fields, H. L. Endogenous pain control mechanisms: Review and hypothesis. Ann. Neurol. 4:451–461, 1978.PubMedCrossRefGoogle Scholar
  2. Beck, P. W., Handwerker, H. O., and Zimmermann, M. Nervous outflow from the cat’s foot during noxious heat stimulation. Brain Res. 67:373–386, 1974.PubMedCrossRefGoogle Scholar
  3. Beitz, A. J., Mullett, M. A., and Weiner, L. L. The periaqueductal gray projections to the rat spinal trigeminal, raphe magnus, gigantocellular pars alpha and paragigantocellular nuclei arise from separate neurons. Brain Res. 288:307–314, 1983.PubMedCrossRefGoogle Scholar
  4. Belcher, G., Ryall, R. W., and Schaffner, R. The differential effects of 5-hydroxytryptamine, noradrenaline and raphe stimulation on nociceptive and nonnociceptive dorsal horn interneurones in the cat. Brain Res. 151:307–321, 1978.PubMedCrossRefGoogle Scholar
  5. Bennett, G. J., and Mayer, D. J. Inhibition of spinal cord interneurons by narcotic microinjection and focal electrical stimulation in the periaqueductal central gray matter. Brain Res. 172:243–257, 1979.PubMedCrossRefGoogle Scholar
  6. Besson, J. M., Oliveras, J. C., Chaolch, A., and Rivot, J. P. Role of the raphe nuclei in stimulation producing analgesia. Adv. Exp. Biol. Med. 133:153–176, 1981.CrossRefGoogle Scholar
  7. Carpenter, C. J., Engberg, I., and Lundberg, A. Primary afferent depolarization evoked from the brain stem and cerebellum. Arch. Ital. Biol. 104:73–85, 1966.PubMedGoogle Scholar
  8. Carstens, E. Inhibition of spinal dorsal horn neuronal responses to noxious skin heating by medial hypothalamic stimulation in the cat. J. Neurophysiol. 41:808–822, 1982.Google Scholar
  9. Carstens, E., Yokota, T., and Zimmermann, M. Inhibition of spinal responses to noxious skin heating by stimulation of mesencephalic periaqueductal gray in the cat. J. Neurophysiol. 42:558–568, 1979.PubMedGoogle Scholar
  10. Carstens, E., Klumpp, D., and Zimmermann, M. Differential inhibitory effects of medial and lateral midbrain stimulation on spinal neuronal discharges to noxious skin heating in the cat. J. Neurophysiol. 43:332–342, 1980.PubMedGoogle Scholar
  11. Carstens, E., Bihl, H., Irvine, D. R. F., and Zimmermann, M. Descending inhibition from medial and lateral midbrain of spinal dorsal horn neuronal responses to noxious and non-noxious cutaneous stimuli in the cat. J. Neurophysiol. 45:1029–1042, 1981.PubMedGoogle Scholar
  12. Carstens, E., MacKinnon, J. D., and Guinan, M. J. Inhibition of spinal dorsal horn neuronal responses to noxious skin heating by medial preoptic and septal stimulation in the cat. J. Neurophysiol. 48:981–991, 1982.PubMedGoogle Scholar
  13. Carstens, E., Fraunhoffer, M., and Suberg, S. N. Inhibition of spinal dorsal horn neuronal responses to noxious skin heating by lateral hypothalamic stimulation in the cat. J. Neurophysiol. 50:192–204, 1983.PubMedGoogle Scholar
  14. Chung, J. M., Fang, Z. E., Cargill, C. L., and Willis, W. D. Prolonged, naloxone-reversible inhibition of the flexion reflex in the cat. Pain 15:35–53, 1983.CrossRefGoogle Scholar
  15. Clark, S. L., and Ryall, R. W. The antinociceptive action of etorphine in the dorsal horn is due to direct spinal action and not to activation of descending inhibition. Br. J. Pharmacol. 78:307–319, 1983.PubMedCrossRefGoogle Scholar
  16. Clark, S. L., Edeson, R. O., and Ryall, R. W. The relative significance of spinal and supraspinal actions in the antinociceptive effect of morphine in the dorsal horn: An evaluation of the microinjection technique. Br.J. Pharmacol. 79:807–818, 1983.PubMedCrossRefGoogle Scholar
  17. Coulter, J. D., Maunz, R. A., and Willis, W. D. Effect of stimulation of sensorimotor cortex on primate spinothalamic neurons. Brain Res. 65:351–356, 1974.PubMedCrossRefGoogle Scholar
  18. Dostrovsky, J. O. Brain stem influences on transmission of somatosensory information in the spinocervicothalamic pathway. Brain Res. 292:229–238, 1984.PubMedCrossRefGoogle Scholar
  19. Dostrovsky, J. O., Hu, J. W., Sessle, B. J., and Sumino, R. Stimulation sites in periaqueductal gray, nucleus raphe magnus and adjacent regions effective in suppressing oral-facial reflexes. Brain Res. 252:287–297, 1982.PubMedCrossRefGoogle Scholar
  20. Du, H.-J., Kitahata, L. M., Thalhammer, J. G., and Zimmermann, M. Inhibition of nociceptive neuronal responses in the cat’s spinal dorsal horn by electrical stimulation and morphine microinjection in nucleus raphe magnus. Pain 19:249–257, 1984.PubMedCrossRefGoogle Scholar
  21. Dubner, R., Ruda, M. A., Miletic., V., Hoffert, M. J., Bennett, G. J., Nishikawa, N., and Coffield, J. Neural circuitry mediating nociception in the medullary and spinal dorsal horns. Adv. Pain Res. Ther. 6:151–166, 1984.Google Scholar
  22. Duggan, A. W. Brain stem inhibition of the spinal transmission of nociceptive information—pharmacologic studies of tonic and stimulation-induced inhibition, in: Brain Stem Control of Spinal Mechanisms, (B. Sjolund and A. Bjorklund, eds.), Elsevier, Amsterdam, 1982, pp. 439–450.Google Scholar
  23. Fields, H. L., and Basbaum, A. I. Brain stem control of spinal pain-transmission neurons. Annu. Rev. Physiol. 40:217–248, 1978.PubMedCrossRefGoogle Scholar
  24. Fields, H. L., Basbaum, A. I., Clanton, C. H., and Anderson, S. D. Nucleus raphe magnus inhibition of spinal cord dorsal horn neurons. Brain Res. 126:441–453, 1977.PubMedCrossRefGoogle Scholar
  25. Fitzgerald, M., and Lynn, B. The sensitization of high threshold mechanoreceptors with mye-linated axons by repeated heating. J. Physiol. (Lond.) 365:549–563, 1977.Google Scholar
  26. Gebhart, G. F. Opioid and opioid peptide effects on brain stem neurons: Relevance to nociception and antinociceptive mechanisms. Pain 12:93–140, 1982.PubMedCrossRefGoogle Scholar
  27. Gebhart, G. F., Sandkühler, J., Thalhammer, J. G., and Zimmermann, M. Quantitative comparison of inhibition in spinal cord of nociceptive information by stimulation in periaqueductal gray or nucleus raphe magnus of the cat. J. Neurophysiol. 50:1433–1445, 1983a.PubMedGoogle Scholar
  28. Gebhart, G. F., Sandkühler, J., Thalhammer, J. G., and Zimmermann, M. Inhibition of spinal nociceptive information by Stimulation in midbrain of the cat is blocked by lidocaine microinjected in nucleus raphe magnus and medullary reticular formation. J. Neurophysiol. 50:1446–1459, 1983b.PubMedGoogle Scholar
  29. Gebhart, G., Sandkühler, J., Thalhammer, J. G., and Zimmermann, M. Inhibition in spinal cord of nociceptive information by electrical stimulation and morphine microinjection at identical sites in midbrain of the cat. J. Neurophysiol. 51:75–89, 1984.PubMedGoogle Scholar
  30. Gerhart, K. D., Wilcox, T. K., Chung, J. M., and Willis, W. D. Inhibition of nociceptive and nonnociceptive responses of primate spinothalamic cells by stimulation in the medial brain stem. J. Neurophysiol. 45:121–136, 1981.PubMedGoogle Scholar
  31. Gerhart, K. D., Yezierski, R. P., Fang, Z. R., and Willis, W. D. Inhibition of primate spinothalamic tract neurons by stimulation in ventral posterior lateral (VPLc) thalamic nucleus: Possible mechanisms. J. Neurophysiol. 49:406–423, 1983.PubMedGoogle Scholar
  32. Gerhart, K. D., Yezierski, R. P., Wilcox, T. K., and Willis, W. D. Inhibition of primate spinothalamic tract neurons by stimulation in periaqueductal gray or adjacent midbrain reticular formation. J. Neurophysiol. 51:450–466, 1984.PubMedGoogle Scholar
  33. Giesler, G. J., Jr., Gerhart, K. D., Yezierski, R. P., Wilcox, T. K., and Willis, W. D. Post-synaptic inhibition of primate spinothalamic neurons by stimulation in nucleus raphe magnus. Brain Res. 204:184–188, 1981.PubMedCrossRefGoogle Scholar
  34. Gray, B. G., and Dostrovsky, J. O. Descending inhibitory influences from periaqueductal gray, nucleus raphe magnus, and adjacent reticular formation. I. Effects on lumbar spinal cord nociceptive and nonnociceptive neurons. J. Neurophysiol. 49:932–947, 1983.PubMedGoogle Scholar
  35. Guilbaud, G., Oliveras, J. L., Giesler, G., Jr., and Besson, J. M. Effects induced by stimulation of the centralis inferior nucleus of the raphe on dorsal horn interneurons in cat’s spinal cord. Brain Res. 126:355–360, 1977.PubMedCrossRefGoogle Scholar
  36. Haber, L. H., Martin, F. R., Chung, J. M., and Willis, W. D. Inhibition and excitation of primate spinothalamic tract neurons by stimulation in region of nucleus reticularis gigan-ocellularis. J. Neurophysiol. 43:1578–1593, 1980.PubMedGoogle Scholar
  37. Handwerker, H. O., Iiggo, A., and Zimmermann, M. Segmental and supraspinal actions on dorsal horn neurons responding to noxious and non-noxious skin stimuli. Pain 1:147–165, 1975.PubMedCrossRefGoogle Scholar
  38. Hentall, I. D., and Fields, H. L. Segmental and descending influences on intraspinal thresholds of single C-fibers. J. Neurophysiol. 42:1527–1537, 1979.PubMedGoogle Scholar
  39. Homma, E., Collins, J. G., Kitahata, L. M., Matsumoto, M., and Kawahara, M. Suppression of noxiously evoked WDR dorsal horn neuronal activity by spinally administered morphine. Anesthesiology 58:232–236, 1983.PubMedCrossRefGoogle Scholar
  40. Hosobuchi, Y., Adams, J. E., and Linchintz, R. Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone. Science 197:183–186, 1977.PubMedCrossRefGoogle Scholar
  41. Kenshalo, D. R., Jr., Leonard, R. B., Chung, J. M., and Willis, W. D. Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. J. Neurophysiol. 42:1370–1389, 1979.PubMedGoogle Scholar
  42. Le Bars, D., Menetrev, D., and Besson, J. M. Effects of morphine upon the laminae V type cells activities in the dorsal horn on the decerebrate cat. Brain Res. 113:293–310, 1976.CrossRefGoogle Scholar
  43. Le Bars, D., Dickenson, A. H., and Besson, J. M. Microinjection of morphine within nucleus raphe magnus and dorsal horn neuron activities related to nociception in the rat. Brain Res. 189:467–481, 1980.PubMedCrossRefGoogle Scholar
  44. Liebeskind, J. C., Guilbaud, G., Besson, J. M., and Oliveras, J. L. Analgesia from electrical stimulation of the periaqueductal gray matter in the cat: Behavioral observations and inhibitory effects on spinal cord interneurons. Brain Res. 50:441–446, 1973.PubMedCrossRefGoogle Scholar
  45. MacIewicz, R., Sandrew, B. B., Phipps, B. S., Poletti, C. E., and Foote, W. E. Pontomedullary raphe neurons: Intracellular responses to central and peripheral electrical stimulation. Brain Res. 293:17–33, 1984.PubMedCrossRefGoogle Scholar
  46. Martin, R. F., Haber, L. H., and Willis, W. D. Primary afferent depolarization of identified cutaneous fibers following stimulation in medial brain stem. J. Neurophysiol. 42:779–790, 1979.PubMedGoogle Scholar
  47. Mayer, D. J. Endogenous analgesia systems: Neural and behavioral mechanisms. Adv. Pain Res. Ther. 1:385–410, 1979.Google Scholar
  48. Mayer, D. J., and Liebeskind, J. C. Pain reduction by focal electrical stimulation of the brain: An anatomical and behavioral analysis. Brain Res. 68:73–93, 1974.PubMedCrossRefGoogle Scholar
  49. Mayer, D. J., and Price, D. D. Central nervous system mechanisms of analgesia. Pain 2:379–404, 1976.PubMedCrossRefGoogle Scholar
  50. Menétrey, D., Giesler, G. J., and Besson, J. M. An analysis of response properties of spinal cord dorsal horn neurons to nonnoxious and noxious stimuli in the spinal rat. Exp. Brain Res. 27:15–33, 1977.PubMedCrossRefGoogle Scholar
  51. Morton, C. R., Duggan, A. W., and Zhaq, Z. Q. The effects of lesions of medullary midline and lateral reticular areas on inhibition in the dorsal horn produced by periaqueductal gray stimulation in the cat. Brain Res. 301:121–130, 1984.PubMedCrossRefGoogle Scholar
  52. Oliveras, J. L., Fardin, V. and Besson, J. M. Stimulation produced analgesia in animals: A review based on behavioral investigations, in: Current Topics in Pain Research and Therapy (T. Yokota and R. Dubner, eds.), Excerpta Medica, Amsterdam, 1983, pp. 95–105.Google Scholar
  53. Ossipov, M. H., and Gebhart, G. F. Light pentobarbital anesthesia diminishes the antinociceptive potency of morphine administered intracranially but not intrathecally in the rat. Eur. J. Pharmacol. 97:137–140, 1984.PubMedCrossRefGoogle Scholar
  54. Price, D. D., and Browe, A. C. Spinal cord coding of graded nonnoxious and noxious temperature increases. Exp. Neurol. 48:201–221, 1975.PubMedCrossRefGoogle Scholar
  55. Price, D. D., and Dubner, R. Neurons that subserve the sensory-discriminative aspects of pain. Pain 3:307–338, 1977.PubMedCrossRefGoogle Scholar
  56. Proudfit, H. K., and Anderson, E. G. New long latency bulbospinal evoked potential blocked by serotonin antagonists. Brain Res. 65:542–546, 1974.PubMedCrossRefGoogle Scholar
  57. Reynolds, D. V. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science 164:444–445, 1969.PubMedCrossRefGoogle Scholar
  58. Richardson, D. E., and Akil, H. Pain reduction by electrical brain stimulation in man: Part 1: Acute administration in periaqueductal and periventricular sites. J. Neurosurg. 47:178–183, 1977.PubMedCrossRefGoogle Scholar
  59. Rivot, J. P., Chaouch, A., and Besson, J. M. Nucleus raphe magnus modulation of response of rat dorsal horn neurons to unmyelinated fiber inputs: Partial involvement of serotonergic pathways. J. Neurophysiol. 44:1039–1057, 1980.PubMedGoogle Scholar
  60. Sandkühler, J., and Gebhart, G. F. Characterization of inhibition of a spinal nociceptive reflex by stimulation medially and laterally in the midbrain and medulla in the pentobarbital-anesthetized rat. Brain Res. 305:67–76, 1984a.PubMedCrossRefGoogle Scholar
  61. Sandkühler, J., and Gebhart, G. F. Relative contributions of the nucleus raphe magnus and adjacent medullary reticular formation to the inhibition by stimulation in the periaqueductal gray of a spinal nociceptive reflex in the pentobarbital-anesthetized rat. Brain Res. 305:77–87, 1984b.PubMedCrossRefGoogle Scholar
  62. Schouenborg, J., and Sjolund, B. G. Activity evoked by A-and C-afferent fibers in rat dorsal horn neurons and its relation to a flexion reflex. J. Neurophysiol. 50:1108–1121, 1983.PubMedGoogle Scholar
  63. Soper, W. Y. Effects of analgesic midbrain stimulation on reflex withdrawal and thermal escape in the rat. J. Comp. Physiol. Psychol. 90:91–101, 1976.PubMedCrossRefGoogle Scholar
  64. Soper, W. Y., and Melzack, R. Stimulation-produced analgesia: Evidence for somatotopic organization in the midbrain. Brain Res. 251:301–311, 1982.PubMedCrossRefGoogle Scholar
  65. Willis, W. D. Control of nociceptive transmission in the spinal cord. Progress in Sensory Physiology 3. Springer-Verlag, Heidelberg, 1982, 159 pp.Google Scholar
  66. Willis, W. D. The raphe-spinal system, in: Brain Stem Control of Spinal Cord Function (C. D. Barnes, ed.), Academic Press, Orlando, 1984, pp. 141–214.Google Scholar
  67. Willis, W. D., Haber, L. D., and Martin, R. F. Inhibition of spinothalamic tract cells and interneurons by brain stem stimulation in the monkey. J. Neurophysiol. 40:968–981, 1977.PubMedGoogle Scholar
  68. Yaksh, T. L. Spinal opiate analgesia: Characteristics and principles of action. Pain 11:293–346, 1981.PubMedCrossRefGoogle Scholar
  69. Yaksh, T. L., and Rudy, T. A. Narcotic analgetics: CNS sites and mechanisms of action as revealed by intracerebral injection techniques. Pain 4:299–359, 1978.PubMedCrossRefGoogle Scholar
  70. Yezierski, R. P., Gerhart, K. D., Schrock, B. J., and Willis, W. D. A further examination of effects of cortical stimulation on primate spinothalamic tract cells. J. Neurophysiol. 49:424–441, 1983.PubMedGoogle Scholar
  71. Zimmermann, M. Encoding in dorsal horn interneurons receiving noxious and nonnoxious afferents. J. Physiol. (Paris) 73:221–232, 1977.Google Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • G. F. Gebhart
    • 1
  1. 1.Department of Pharmacology, College of MedicineUniversity of IowaIowa CityUSA

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