Somatosensory Input to the Periaqueductal Gray: A Spinal Relay to a Descending Control Center

  • Robert P. Yezierski
Part of the NATO ASI Series book series (NSSA, volume 213)


The spinomesencephalic tract (SMT) with its varied origins (Mantyh, 1982; Menétrey et al., 1982; Swett et al., 1985; Wiberg and Blomqvist, 1984; Wiberg et al., 1987; Yezierski and Mendez, 1991; Zhang et al., 1990), spinal trajectories (Hylden et al., 1986b; Kerr, 1975; McMahon and Wall, 1985; Yezierski and Schwartz, 1986; Zemlan et al., 1978), and sites of termination (Anderson and Berry, 1959; McMahon and Wall 1985; Mehler, 1969; Morin, 1953; Björkeland and Boivie, 1984; Blomqvist and Craig, this volume; Yezierski, 1988) is often described as having a role in nociception (Bowsher, 1976; Mehler, 1969; Willis, 1985; Willis and Coggeshall, 1978; Yezierski, 1988). Consistent with this hypothesis are the responses of SMT cells to noxious mechanical and thermal stimuli (Hylden et al., 1986a; 1989; Menétrey et al., 1980; Yezierski and Schwartz, 1986; Yezierski et al., 1985). Furthermore, recent studies have shown SMT cells in the upper cervical and lumbosacral spinal cord respond to inputs from cutaneous and /or deep structures, including joints, muscles, and viscera (Yezierski and Broton, 1991; Yezierski and Schwartz, 1986; Yezierski et al., 1987; Yezierski, 1990). These observations as well as the varied functions associated with SMT projection targets supports a role of the SMT in sensory, motor and visceral functions.


Inferior Colliculus Wide Dynamic Range Stimulation Site Excitatory Response Somatosensory Input 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abols, I.A. and Basbaum, A.I., Afferent connections of the rostral medulla of the cat: a neural substrate for midbrain-medullary interactions in the modulation of pain, J. Comp. Neurol., 201 (1981) 285–297.CrossRefPubMedGoogle Scholar
  2. Andersen, E., Periaqueductal gray and cerebral cortex modulate responses of medial thalamic neurons to noxious stimulation, Brain Res., 375 (1986) 30–36.CrossRefPubMedGoogle Scholar
  3. Anderson, F.D. and Berry, C.M., Degeneration studies of long ascending fiber systems in the cat brain stem, J. Comp. Neurol., 111 (1959) 195–229.CrossRefPubMedGoogle Scholar
  4. Bandler, R., Carrive, P., Zhang, S.P., Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: viscerotopic, somatotopic and functional organization, Prog. Brain Res., 87 (1991) 269–305.CrossRefPubMedGoogle Scholar
  5. Barbaresi, P., Conti, F. and Manzoni, T., Periaqueductal gray projection to the ventrobasal complex in the cat: an HRP study, Neurosci. Lett., 30 (1982) 205–209.CrossRefPubMedGoogle Scholar
  6. Barone, F.C., Wagner, M.J. and Tsai, W.H., Effects of periaqueductal gray stimulation on diencephalic neural activity, Brain Res. Bull., 7 (1981) 195–207.CrossRefPubMedGoogle Scholar
  7. Berman, A.L., The Brain Stem of the Cat, a Stereotaxic Atlas with Stereotaxic Coordinates, Univ. of Wisconsin Press, Madison, 1968.Google Scholar
  8. Björkeland, M. and Boivie, J., The termination of spinomesencephalic fibers in the cat, an experimental anatomical study, Anat. Embryol. (Berl.), 170 (1984) 265–277.CrossRefGoogle Scholar
  9. Bowsher, D., Termination of the central pain pathway in man: the conscious appreciation of pain., Brain, 80 (1957) 606–622.CrossRefPubMedGoogle Scholar
  10. Bowsher, D., Role of the reticular formation in responses to noxious stimulation, Pain, 2 (1976) 361–378.CrossRefPubMedGoogle Scholar
  11. Chung, J.M., Kevetter, G.A., Yezierski, R.P., Haber, L.H., Martin, R.F. and Willis W.D., Midbrain nuclei projecting to the medial medulla oblongata in the monkey, J. Comp. Neurol., 214 (1983) 93–102.CrossRefPubMedGoogle Scholar
  12. Duggan, A.W. and Griersmith, B.T., Inhibition of the spinal transmission of nociceptive information by supraspinal stimulation in the cat, Pain, 6 (1979) 149–161.CrossRefPubMedGoogle Scholar
  13. Emmers, R., Dual alterations of thalamic nociceptive activity by stimulation of the periaqueductal gray matter, Exp. Neurol., 65 (1979) 186–201.CrossRefPubMedGoogle Scholar
  14. Gallager, D.W. and Pert, A., Afferents to brain stem nuclei in the rat as demonstrated by microiontophoretically applied horseradish peroxidase, Brain Res., 144 (1978) 257–275.CrossRefPubMedGoogle Scholar
  15. Gebhart, G.F., Modulatory effects of descending systems on spinal dorsal horn neurons, In: Spinal Afferent Processing, Yaksh T. (Ed.), Plenum, New York, 1986, pp. 391–416.Google Scholar
  16. 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 (1984) 450–466.PubMedGoogle Scholar
  17. 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 (1983) 932–947.PubMedGoogle Scholar
  18. Hamilton, B.L., Projections of the nuclei of the periaqueductal gray matter in the cat., J. Comp. Neurol., 152 (1974) 45–58.CrossRefGoogle Scholar
  19. Hammond, D.L., Control systems for nociceptive afferent processing: The descending inhibitory pathways, In: Spinal Afferent Processing, Yaksh T. (Ed.), Plenum, New York, 1986, pp. 363–390.Google Scholar
  20. Handwerker, H.O., Reeh, P.W. and Steen, K.H. Effects of 5HT on nociceptors, In: Serotonin and Pain, Besson J.-M. (Ed.), Elsevier, Amsterdam, 1990, pp. 1–15.Google Scholar
  21. Hardy, J.D., Wolff, H.G, and Goodell, H., Pain Sensations and Reactions, Williams and Wilkins, Baltimore, 1952.Google Scholar
  22. Hylden, J., Hayashi, H. and Bennett, G., Physiology and morphology of the lamina I spinomesencephalic projection, J. Comp. Neurol., 247 (1986a) 505–515.CrossRefPubMedGoogle Scholar
  23. Hylden, J., Hayashi, H. and Bennett, G., Lamina I spinomesencephalic neurons in the cat ascend via the dorsolateral funiculi, Somatosen. Res., 4 (1986b) 31–41.CrossRefGoogle Scholar
  24. Hylden, J.L.K., Nahin, R.L., Anton, F. and Dubner, R., Characterization of lamina I projection neurons: physiology and anatomy, In: Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord, Cervero F., Bennett G.J., Headley P.M. (Eds.), Plenum, New York, 1989, pp. 113–128.CrossRefGoogle Scholar
  25. Kayser, V., Benoist, J.-M. and Guilbaud, G., Low doses of morphine microinjected in the ventral periaqueductal gray matter of the rat depresses responses of nociceptive ventrobasal thalamic neurons, Neurosci. Lett., 37 (1983) 193–198.Google Scholar
  26. Kerr, F., The ventral spinothalamic tract and other ascending systems of the ventral funiculus of the spinal cord, J. Comp. Neurol., 159 (1975) 335–356.CrossRefPubMedGoogle Scholar
  27. Kniffki, K.-D., Mense, S. and Schmidt, R.F., Response of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation, Exp. Brain Res., 31 (1978) 511–522.CrossRefPubMedGoogle Scholar
  28. Lewis, V.A. and Gebhart, G.F., Evaluation of the periaqueductal central gray (PAG) as a morphine-specific locus of action and examination of morphine-induced and stimulation-produced analgesia as a coincident periaqueductal gray loci, Brain Res., 124 (1977) 283–303.CrossRefPubMedGoogle Scholar
  29. Liebeskind, J.C., Guilbaud, G., Besson, J.M. and Olivéras, 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 (1973) 441–446.CrossRefPubMedGoogle Scholar
  30. Magoun, H.W., Atlas, D., Ingersoll, E.H. and Ranson, S.W., Associated facial, vocal, and respiratory components of emotional expression. An experimental study, J. Neurol. Psychopath., 17 (1936) 241–255.CrossRefGoogle Scholar
  31. Mantyh, P.W., The ascending input to the midbrain periaqueductal gray of the primate, J. Comp. Neurol., 211 (1982) 50–64.CrossRefPubMedGoogle Scholar
  32. Mantyh, P.W., Connections of midbrain periaqueductal gray in the monkey. I. Ascending efferent projections, J. Neurophysiol., 49 (1983) 567–581.PubMedGoogle Scholar
  33. McMahon, S.B. and Wall, P.D., Electrophysiological mapping of brainstem projections of spinal cord lamina I cells in the rat, Brain Res., 333 (1985) 19–26.CrossRefPubMedGoogle Scholar
  34. McMahon, S.B and Wall, P.D., The significance of plastic changes in lamina I systems, In: Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord, Cervero F., Bennett G.J., Headley P.M. (Eds.) Plenum, New York, 1989, pp. 249–271.CrossRefGoogle Scholar
  35. Mehler, W.R., Some neurological species differences-a posteriori, Ann. NY Acad. Sci., 167 (1969) 424–468.CrossRefGoogle Scholar
  36. Meiler, S.T., Lewis, S.J., Ness, T.J., Brody, M.J. and Gebhart, G.F., Vagal afferent-mediated inhibition of a nociceptive reflex by intravenous serotonin in the rat. I. Characterization, Brain Res., 524 (1990a) 90–100.CrossRefGoogle Scholar
  37. Meiler, S.T., Lewis, S.J., Brody, M.J. and Gebhart, G.F., Is intravenous serotonin noxious?, Pain, 5 (1990b) S408.CrossRefGoogle Scholar
  38. Melzack, R. and Casey, K.L., Sensory, motivational and central control determinants of pain. A new conceptual model, In: The Skin Senses, Kenshalo D.R. (Ed.), Thomas, Springfield, 1968, pp. 423–443.Google Scholar
  39. Menétrey, D., Chaouch, A. and Besson, J.M., Location and properties of dorsal horn neurons at origin of spinoreticular tract in lumbar enlargement of the rat, J. Neurophysiol., 44 (1980) 862–877.PubMedGoogle Scholar
  40. Menétrey, D., Chaouch, A., Binder, D. and Besson, J.M., The origin of the spinomesencephalic tract in the rat: an anatomical study using the retrograde transport of horseradish peroxidase, J. Comp. Neurol., 206 (1982) 193–207.CrossRefPubMedGoogle Scholar
  41. Mense, S. and Schmidt, R.F., Activation of group IV afferent units from muscle by algesic agents, Brain Res., 72 (1974) 305–310.CrossRefPubMedGoogle Scholar
  42. Morin, F., Afferent projections to the midbrain tegmentum and their spinal course, Am. J. Physiol., 172 (1953) 483–496.PubMedGoogle Scholar
  43. Olivéras, J.-L., Besson, J.-M., Guilbaud, G. and Liebeskind, J.C., Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat, Exp. Brain Res., 20 (1974) 32–44.CrossRefPubMedGoogle Scholar
  44. Olivéras, J.-L., Guilbaud, G. and Besson, J.M., A map of serotoninergic structures involved in stimulation producing analgesia in unrestrained freely moving cats, Brain Res., 164 (1979) 317–322.CrossRefPubMedGoogle Scholar
  45. 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 phenobarbital anesthetized rat, Brain Res., 305 (1984) 77–87.CrossRefPubMedGoogle Scholar
  46. Skultety, F., Relation of periaqueductal gray matter to stomach and bladder motility, Neurology, 9 (1959) 190–197.CrossRefPubMedGoogle Scholar
  47. Spiegel, E.A, Kletzkin, M. and Szekely, E.G., Pain reactions upon stimulation of the tectum mesencephali, J. Neuropathol. Exp. Neurol., 13 (1954) 212–220.CrossRefPubMedGoogle Scholar
  48. Spruijt, B.M., Cools, A.R. and Gispen, W.H., The periaqueductal gray: a prerequisite for ACTH-induced excessive grooming, Behav. Brain Res., 20 (1986) 19–25.CrossRefPubMedGoogle Scholar
  49. Swett, J.E., McMahon, S.B. and Wall, P.D., Long ascending projections to the midbrain from cells of lamina I and nucleus of the dorsolateral funiculus of the rat spinal cord, J. Comp. Neurol., 238 (1985) 401–416.CrossRefPubMedGoogle Scholar
  50. Wiberg, M. and Blomqvist, A., The spinomesencephalic tract in the cat: its cells of origin and termination pattern as demonstrated by the intraxonal transport method, Brain Res., 291 (1984) 1–18.CrossRefPubMedGoogle Scholar
  51. Wiberg, M., Westman, J. and Blomqvist, A., Somatosensory projections to the mesencephalon: an anatomical study in the monkey, J. Comp. Neurol., 264 (1987) 92–117.CrossRefPubMedGoogle Scholar
  52. Willis, W.D., The pain system, In: Pain and Headache, Vol. 8, Karger, New York, 1985.Google Scholar
  53. Willis, W.D., Anatomy and physiology of descending control of nociceptive responses of dorsal horn neurons: comprehensive review, Prog. Brain Res., 77 (1988) 1–29.CrossRefPubMedGoogle Scholar
  54. Willis, W.D., Projections of the superficial dorsal horn to the midbrain and thalamus, In: Processing of Sensory Information in the Superficial Dorsal Horn of the Spinal Cord, Cervero F., Bennett G.J., Headley P.M. (Eds.), Plenum, New York, 1989, pp. 217–237.CrossRefGoogle Scholar
  55. Willis, W.D. and Coggeshall, R.E., Sensory mechanisms of the spinal cord, Plenum, New York, 1978.Google Scholar
  56. Yaksh, T.L., Yeung, J.C. and Rudy, T.A., Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observations of differential effects within the periaqueductal gray, Brain Res., 114 (1976) 83–104.CrossRefPubMedGoogle Scholar
  57. Yezierski, R.P., The spinomesencephalic tract: projections from the lumbosacral spinal cord of the rat, cat and monkey, J. Comp. Neurol., 267 (1988) 131–146.CrossRefPubMedGoogle Scholar
  58. Yezierski, R.P., The effects of midbrain and medullary stimulation on spinomesencephalic tract cells in the cat, J. Neurophysiol., 63 (1990) 240–255.PubMedGoogle Scholar
  59. Yezierski, R.P. and Broton, J.G., Functional properties of spinomesencephalic tract (SMT) cells in the upper cervical spinal cord of the cat, Pain, 45 (1991) 187–196.CrossRefPubMedGoogle Scholar
  60. Yezierski, R.P., Hirata, H. and Olson, N.A., Responses of spinomesencephalic tract (SMT) cells to thermal stimuli, Soc. Neurosci. Abstr., 11 (1985) 172.Google Scholar
  61. Yezierski, R.P. and Schwartz, R.H., Response and receptive field properties of spinomesencephalic tract cells in the cat, J. Neurophysiol., 55 (1986) 76–96.PubMedGoogle Scholar
  62. Yezierski, R.P., Sorkin, L.S. and Willis, W.D., Response properties of spinal neurons projecting to midbrain or midbrain and thalamus in the monkey, Brain Res., 437 (1987) 165–170.CrossRefPubMedGoogle Scholar
  63. Yezierski, R.P. and Mendez C.M., Spinal distribution and collateral projections of rat spinomesencephalic tract cells, Neurosci., 1991, in press.Google Scholar
  64. Zamir, N. and Maixner, W., The relationship between cardiovascular and pain regulatory systems, Annals NY Acad. Sci., 467 (1986) 371–384.CrossRefGoogle Scholar
  65. Zemlan, F.P., Leonard, C.M., Kow, L. and Pfaff, D.W., Ascending tracts of the lateral columns of the rat spinal cord: a study using the silver impregnation and horseradish peroxidase techniques, Exp. Neurol., 62 (1978) 298–334.CrossRefPubMedGoogle Scholar
  66. Zhang, D., Carlton, S.M., Sorkin, L.S. and Willis, W.D., Collaterals of primate spinothalamic tract neurons to the periaqueductal gray, J. Comp. Neurol., 296 (1990) 277–290.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Robert P. Yezierski
    • 1
  1. 1.Department of Neurological SurgeryUniversity of Miami, School of MedicineMiamiUSA

Personalised recommendations