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. 1981 May;314:513–529. doi: 10.1113/jphysiol.1981.sp013722

Monoamine release from cat spinal cord by somatic stimuli: an intrinsic modulatory system.

G M Tyce, T L Yaksh
PMCID: PMC1249448  PMID: 7310700

Abstract

1. Superfusates taken from spinal cords of cats anaesthetized with chloralose and urethane were assayed for endogenous serotonin and noradrenaline by high-pressure liquid chromatography with electrochemical detection. 2. Stimulating the dorsolateral funiculus, caudal to a spinal transection, enhanced in a frequency-dependent manner the levels of monoamines in the spinal superfusate. 3. Tyramine added to the superfusate enhanced the release of noradrenaline and serotonin. 4. In cats with intact neuraxes, stimulation of the sciatic nerve at high, but not low intensities produced a 2- to 3-fold increase in the levels of monoamines in the spinal superfusate. This evoked monoamine efflux was attenuated by cold block of the cervical spinal cord. 5. Stimulation of the infraorbital branch of the trigeminal nerve evoked the release of noradrenaline and serotonin from the lumbar cord in animals with intact neuraxes. Cold block of the cervical cord blocked trigeminal-evoked release of lumbar serotonin and noradrenaline. 6. That the monoamine efflux was not due to elevations in blood pressure was indicated by the failure of vasoxyl, an alpha-agonist producing hypertension, to evoke any changes in spinal monoamine levels. 7. The monoamine release was not dependent upon either an opiate-sensitive link or upon the activation of the sympathetic ganglia, because systemic administration of naloxone (an opiate antagonist) and chlorisondamine (a ganglionic blocking agent) failed to antagonize the evoked release of amines. 8. These results suggest the existence of a spinopetal monoamine system which is activated by peripheral stimuli. The modulatory influence associated with increasing monoamine tone in the spinal cord clearly indicated that somatic stimuli may activate a descending monoamine pathway which serves to modulate the magnitude of the ascending sensory message.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson E. G. Bulbospinal serotonin-containing neurons and motor control. Fed Proc. 1972 Jan-Feb;31(1):107–112. [PubMed] [Google Scholar]
  2. Basbaum A. I., Clanton C. H., Fields H. L. Three bulbospinal pathways from the rostral medulla of the cat: an autoradiographic study of pain modulating systems. J Comp Neurol. 1978 Mar 15;178(2):209–224. doi: 10.1002/cne.901780203. [DOI] [PubMed] [Google Scholar]
  3. Basbaum A. I., Fields H. L. The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J Comp Neurol. 1979 Oct 1;187(3):513–531. doi: 10.1002/cne.901870304. [DOI] [PubMed] [Google Scholar]
  4. Behbehani M. M., Pomeroy S. L. Effect of morphine injectedin periadueductal gray on the activity of single units in nucleus raphe magnus of the rat. Brain Res. 1978 Jun 23;149(1):266–269. doi: 10.1016/0006-8993(78)90609-1. [DOI] [PubMed] [Google Scholar]
  5. Benjamin R. M. Single neurons in the rat medulla responsive to nociceptive stimulation. Brain Res. 1970 Dec 18;24(3):525–529. doi: 10.1016/0006-8993(70)90191-5. [DOI] [PubMed] [Google Scholar]
  6. Cabot J. B., Wild J. M., Cohen D. H. Raphe inhibition of sympathetic preganglionic neurons. Science. 1979 Jan 12;203(4376):184–186. doi: 10.1126/science.758687. [DOI] [PubMed] [Google Scholar]
  7. Coote J. H., Sato A. Supraspinal regulation of spinal reflex discharge into cardiac sympathetic nerves. Brain Res. 1978 Mar 10;142(3):425–437. doi: 10.1016/0006-8993(78)90906-x. [DOI] [PubMed] [Google Scholar]
  8. Crowley W. R., Rodriguez-Sierra J. F., Komisaruk B. R. Analgesia induced by vaginal stimulation in rats is apparently independent of a morphine-sensitive process. Psychopharmacology (Berl) 1977 Nov 15;54(3):223–225. doi: 10.1007/BF00426567. [DOI] [PubMed] [Google Scholar]
  9. Duggan A. W. Pharmacology of mammalian central inhibition. Int Rev Physiol. 1978;17:119–148. [PubMed] [Google Scholar]
  10. FISCHER J. E., MUSACCHIO J., KOPIN I. J., AXELROD J. EFFECTS OF DENERVATION ON THE UPTAKE AND BETA-HYDROXYLATION OF TYRAMINE IN THE RAT SALIVARY GLAND. Life Sci. 1964 May;3:413–419. doi: 10.1016/0024-3205(64)90201-2. [DOI] [PubMed] [Google Scholar]
  11. Guilbaud G., Besson J. M., Oliveras J. L., Wyon-Maillard M. C. Modifications of the firing rate of bulbar reticular units (nucleus gigantocellularis) after intra-arterial injection of bradykinin into the limbs. Brain Res. 1973 Dec 7;63:131–140. doi: 10.1016/0006-8993(73)90082-6. [DOI] [PubMed] [Google Scholar]
  12. Hamilton B. L. Projections of the nuclei of the periaqueductal gray matter in the cat. J Comp Neurol. 1973 Nov 1;152(1):45–58. doi: 10.1002/cne.901520104. [DOI] [PubMed] [Google Scholar]
  13. Headley P. M., Duggan A. W., Griersmith B. T. Selective reduction by noradrenaline and 5-hydroxytryptamine of nociceptive responses of cat dorsal horn neurones. Brain Res. 1978 Apr 21;145(1):185–189. doi: 10.1016/0006-8993(78)90809-0. [DOI] [PubMed] [Google Scholar]
  14. Kerr F. W. The ventral spinothalamic tract and other ascending systems of the ventral funiculus of the spinal cord. J Comp Neurol. 1975 Feb 1;159(3):335–356. doi: 10.1002/cne.901590304. [DOI] [PubMed] [Google Scholar]
  15. Komisaruk B. R., Larsson K. Suppression of a spinal and a cranial nerve reflex by vaginal or rectal probing in rats. Brain Res. 1971 Dec 10;35(1):231–235. doi: 10.1016/0006-8993(71)90608-1. [DOI] [PubMed] [Google Scholar]
  16. Komisaruk B. R., Wallman J. Antinociceptive effects of vaginal stimulation in rats: neurophysiological and behavioral studies. Brain Res. 1977 Nov 25;137(1):85–107. doi: 10.1016/0006-8993(77)91014-9. [DOI] [PubMed] [Google Scholar]
  17. Kuraishi Y., Harada Y., Satoh M., Takagi H. Antagonism by phenoxybenzamine of the analgesic effect of morphine injected into the nucleus reticularis gigantocellularis of the rat. Neuropharmacology. 1979 Jan;18(1):107–110. doi: 10.1016/0028-3908(79)90016-9. [DOI] [PubMed] [Google Scholar]
  18. Kuraishi Y., Harada Y., Takagi H. Noradrenaline regulation of pain-transmission in the spinal cord mediated by alpha-adrenoceptors. Brain Res. 1979 Oct 5;174(2):333–336. doi: 10.1016/0006-8993(79)90857-6. [DOI] [PubMed] [Google Scholar]
  19. Le Bars D., Dickenson A. H., Besson J. M. Diffuse noxious inhibitory controls (DNIC). I. Effects on dorsal horn convergent neurones in the rat. Pain. 1979 Jun;6(3):283–304. doi: 10.1016/0304-3959(79)90049-6. [DOI] [PubMed] [Google Scholar]
  20. Le Bars D., Dickenson A. H., Besson J. M. Diffuse noxious inhibitory controls (DNIC). II. Lack of effect on non-convergent neurones, supraspinal involvement and theoretical implications. Pain. 1979 Jun;6(3):305–327. doi: 10.1016/0304-3959(79)90050-2. [DOI] [PubMed] [Google Scholar]
  21. LeBlanc H. J., Gatipon G. B. Medial bulboreticular response to peripherally applied noxious stimuli. Exp Neurol. 1974 Feb;42(2):264–273. doi: 10.1016/0014-4886(74)90024-7. [DOI] [PubMed] [Google Scholar]
  22. MEHLER W. R., FEFERMAN M. E., NAUTA W. J. Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain. 1960 Dec;83:718–750. doi: 10.1093/brain/83.4.718. [DOI] [PubMed] [Google Scholar]
  23. Matthaei H., Lentzen H., Philippu A. Competition of some biogenic amines for uptake into synaptic vesicles of the striatum. Naunyn Schmiedebergs Arch Pharmacol. 1976;293(1):89–96. doi: 10.1007/BF00498875. [DOI] [PubMed] [Google Scholar]
  24. Mayer D. J., Liebeskind J. C. Pain reduction by focal electrical stimulation of the brain: an anatomical and behavioral analysis. Brain Res. 1974 Mar 15;68(1):73–93. doi: 10.1016/0006-8993(74)90534-4. [DOI] [PubMed] [Google Scholar]
  25. McCreery D. B., Bloedel J. R. Effect of trigeminal stimulation on the excitability of cat spinothalamic neurons. Brain Res. 1976 Nov 19;117(1):136–140. doi: 10.1016/0006-8993(76)90563-1. [DOI] [PubMed] [Google Scholar]
  26. Melzack R., Wall P. D. Pain mechanisms: a new theory. Science. 1965 Nov 19;150(3699):971–979. doi: 10.1126/science.150.3699.971. [DOI] [PubMed] [Google Scholar]
  27. Mendell L. M. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol. 1966 Nov;16(3):316–332. doi: 10.1016/0014-4886(66)90068-9. [DOI] [PubMed] [Google Scholar]
  28. Oliveras J. L., Bourgoin S., Hery F., Besson J. M., Hamon M. The topographical distribution of serotoninergic terminals in the spinal cord of the cat: biochemical mapping by the combined use of microdissection and microassay procedures. Brain Res. 1977 Dec 23;138(3):393–406. doi: 10.1016/0006-8993(77)90680-1. [DOI] [PubMed] [Google Scholar]
  29. Pomeranz B., Chiu D. Naloxone blockade of acupuncture analgesia: endorphin implicated. Life Sci. 1976 Dec 1;19(11):1757–1762. doi: 10.1016/0024-3205(76)90084-9. [DOI] [PubMed] [Google Scholar]
  30. Reddy S. V., Maderdrut J. L., Yaksh T. L. Spinal cord pharmacology of adrenergic agonist-mediated antinociception. J Pharmacol Exp Ther. 1980 Jun;213(3):525–533. [PubMed] [Google Scholar]
  31. Reddy S. V., Yaksh T. L. Spinal noradrenergic terminal system mediates antinociception. Brain Res. 1980 May 12;189(2):391–401. doi: 10.1016/0006-8993(80)90099-2. [DOI] [PubMed] [Google Scholar]
  32. Rhodes D. L., Liebeskind J. C. Analgesia from rostral brain stem stimulation in the rat. Brain Res. 1978 Mar 31;143(3):521–532. doi: 10.1016/0006-8993(78)90362-1. [DOI] [PubMed] [Google Scholar]
  33. Sastry B. S., Sinclair J. G. Tonic inhibitory influence of a supraspinal monoaminergic system on presynaptic inhibition of an extensor monosynaptic reflex. Brain Res. 1977 Mar 18;124(1):109–120. doi: 10.1016/0006-8993(77)90867-8. [DOI] [PubMed] [Google Scholar]
  34. Sato A. Spinal and medullary reflex components of the somatosympathetic reflex discharges evoked by stimulation of the group IV somatic afferents. Brain Res. 1973 Mar 15;51:307–318. doi: 10.1016/0006-8993(73)90381-8. [DOI] [PubMed] [Google Scholar]
  35. Schroeder D. M., Jane J. A. Projection of dorsal column nuclei and spinal cord to brainstem and thalamus in the tree shrew, Tupaia glis. J Comp Neurol. 1971 Jul;142(3):309–350. doi: 10.1002/cne.901420305. [DOI] [PubMed] [Google Scholar]
  36. Sjölund B., Terenius L., Eriksson M. Increased cerebrospinal fluid levels of endorphins after electro-acupuncture. Acta Physiol Scand. 1977 Jul;100(3):382–384. doi: 10.1111/j.1748-1716.1977.tb05964.x. [DOI] [PubMed] [Google Scholar]
  37. Smits J. F., van Essen H., Struyker-Boudier A. J. Serotonin-mediated cardiovascular responses to electrical stimulation of the raphe nuclei in the rat. Life Sci. 1978 Jul 10;23(2):173–178. doi: 10.1016/0024-3205(78)90267-9. [DOI] [PubMed] [Google Scholar]
  38. Trulson M. E., Jacobs B. L. Long-term amphetamine treatment decreases brain serotonin metabolism: implications for theories of schizophrenia. Science. 1979 Sep 21;205(4412):1295–1297. doi: 10.1126/science.572992. [DOI] [PubMed] [Google Scholar]
  39. Westman J., Bowsher D. Ultrastructural observations on the degeneration of spinal afferents to the nucleus medullae oblongatae centralis (pars caudalis) of the cat. Brain Res. 1971 Mar 5;26(2):395–398. [PubMed] [Google Scholar]
  40. Woolf C. J., Barrett G. D., Mitchell D., Myers R. A. Naloxone-reversible peripheral electroanalgesia in intact and spinal rats. Eur J Pharmacol. 1977 Oct 1;45(3):311–314. doi: 10.1016/0014-2999(77)90016-4. [DOI] [PubMed] [Google Scholar]
  41. Yaksh T. L. Direct evidence that spinal serotonin and noradrenaline terminals mediate the spinal antinociceptive effects of morphine in the periaqueductal gray. Brain Res. 1979 Jan 5;160(1):180–185. doi: 10.1016/0006-8993(79)90616-4. [DOI] [PubMed] [Google Scholar]
  42. Yaksh T. L., Rudy T. A. Narcotic analgestics: CNS sites and mechanisms of action as revealed by intracerebral injection techniques. Pain. 1978 Apr;4(4):299–359. doi: 10.1016/0304-3959(77)90145-2. [DOI] [PubMed] [Google Scholar]
  43. Yaksh T. L., Tyce G. M. Microinjection of morphine into the periaqueductal gray evokes the release of serotonin from spinal cord. Brain Res. 1979 Jul 27;171(1):176–181. doi: 10.1016/0006-8993(79)90747-9. [DOI] [PubMed] [Google Scholar]
  44. Yaksh T. L., Tyce G. M. Resting and K+-evoked release of serotonin and norephinephrine in vivo from the rat and cat spinal cord. Brain Res. 1980 Jun 16;192(1):133–146. doi: 10.1016/0006-8993(80)91014-8. [DOI] [PubMed] [Google Scholar]
  45. Yaksh T. L., Wilson P. R. Spinal serotonin terminal system mediates antinociception. J Pharmacol Exp Ther. 1979 Mar;208(3):446–453. [PubMed] [Google Scholar]

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