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. 1995 Jun 15;485(Pt 3):787–796. doi: 10.1113/jphysiol.1995.sp020769

Tachykininergic slow depolarization of motoneurones evoked by descending fibres in the neonatal rat spinal cord.

T Kurihara 1, K Yoshioka 1, M Otsuka 1
PMCID: PMC1158044  PMID: 7562617

Abstract

1. In the isolated spinal cord of the neonatal rat, repetitive electrical stimulation of the upper cervical region elicited a prolonged depolarization of lumbar motoneurones (L3-5) lasting 1-2 min, which was recorded extracellularly from ventral roots, or intracellularly. 2. This depolarizing response was markedly depressed by the excitatory amino acid receptor antagonists D-(-)-2-amino-5-phosphonovaleric acid (D-APV, 30 microM) and 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM). The remaining response was further depressed by a 5-hydroxytryptamine (5-HT) receptor antagonist, ketanserin (3 microM). 3. In the presence of these antagonists, a small part of the depolarizing response of slow time course remained, and this response was partially blocked by the tachykinin NK1 receptor antagonists GR71251 (0.3-5 microM) and RP67580 (0.3-1 microM). In contrast, RP68651 (0.3-1 microM), the inactive enantiomer of RP67580, had no effect on the depolarizing response. 4. The slow depolarizing response in the presence of D-APV, CNQX and ketanserin was markedly potentiated by a peptidase inhibitor, thiorphan (1 microM). 5. This descending fibre-evoked slow depolarization became smaller after prolonged treatment (5-7 h) with 5,7-dihydroxytryptamine (10 microM), a neurotoxin for 5-HT neurones. Under such conditions, the effects of thiorphan and GR71251 on the slow depolarization were virtually absent. 6. Under the action of D-APV, CNQX and ketanserin, applications of tachykinins, substance P and neurokinin A produced depolarizing responses of lumbar motoneurones, and the responses were depressed by GR71251 and potentiated by thiorphan. 7. These results suggest that tachykinins contained in serotonergic fibres serve as neurotransmitters mediating the descending fibre-evoked slow excitatory postsynaptic potentials in motoneurones.

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Selected References

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  1. Akagi H., Konishi S., Otsuka M., Yanagisawa M. The role of substance P as a neurotransmitter in the reflexes of slow time courses in the neonatal rat spinal cord. Br J Pharmacol. 1985 Mar;84(3):663–673. doi: 10.1111/j.1476-5381.1985.tb16148.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baumgarten H. G., Klemm H. P., Lachenmayer L., Björklund A., Lovenberg W., Schlossberger H. G. Mode and mechanism of action of neurotoxic indoleamines: a review and a progress report. Ann N Y Acad Sci. 1978 Jun 12;305:3–24. doi: 10.1111/j.1749-6632.1978.tb31507.x. [DOI] [PubMed] [Google Scholar]
  3. Buijs R. M. Intra- and extrahypothalamic vasopressin and oxytocin pathways in the rat. Pathways to the limbic system, medulla oblongata and spinal cord. Cell Tissue Res. 1978 Sep 26;192(3):423–435. doi: 10.1007/BF00212323. [DOI] [PubMed] [Google Scholar]
  4. Chan-Palay V., Jonsson G., Palay S. L. Serotonin and substance P coexist i, neurons of the rat's central nervous system. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1582–1586. doi: 10.1073/pnas.75.3.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. De Koninck Y., Henry J. L. Substance P-mediated slow excitatory postsynaptic potential elicited in dorsal horn neurons in vivo by noxious stimulation. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11344–11348. doi: 10.1073/pnas.88.24.11344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Elliott P., Wallis D. I. Glutamatergic and non-glutamatergic responses evoked in neonatal rat lumbar motoneurons on stimulation of the lateroventral spinal cord surface. Neuroscience. 1993 Sep;56(1):189–197. doi: 10.1016/0306-4522(93)90573-x. [DOI] [PubMed] [Google Scholar]
  7. Franck J., Brodin E., Fried K., Rosén A., Yamamoto Y., Fried G. The effect of selective serotonergic neurotoxin treatment on tachykinin levels in the rat ventral spinal cord. Neuroscience. 1991;45(2):339–345. doi: 10.1016/0306-4522(91)90231-c. [DOI] [PubMed] [Google Scholar]
  8. Garret C., Carruette A., Fardin V., Moussaoui S., Peyronel J. F., Blanchard J. C., Laduron P. M. Pharmacological properties of a potent and selective nonpeptide substance P antagonist. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10208–10212. doi: 10.1073/pnas.88.22.10208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Guo J. Z., Yoshioka K., Yanagisawa M., Hosoki R., Hagan R. M., Otsuka M. Depression of primary afferent-evoked responses by GR71251 in the isolated spinal cord of the neonatal rat. Br J Pharmacol. 1993 Nov;110(3):1142–1148. doi: 10.1111/j.1476-5381.1993.tb13933.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Holstege J. C., Kuypers H. G. Brainstem projections to spinal motoneurons: an update. Neuroscience. 1987 Dec;23(3):809–821. doi: 10.1016/0306-4522(87)90160-6. [DOI] [PubMed] [Google Scholar]
  11. Hosoki R., Yanagisawa M., Guo J. Z., Yoshioka K., Maehara T., Otsuka M. Effects of RP 67580, a tachykinin NK1 receptor antagonist, on a primary afferent-evoked response of ventral roots in the neonatal rat spinal cord. Br J Pharmacol. 1994 Dec;113(4):1141–1146. doi: 10.1111/j.1476-5381.1994.tb17116.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hökfelt T., Ljungdahl A., Steinbusch H., Verhofstad A., Nilsson G., Brodin E., Pernow B., Goldstein M. Immunohistochemical evidence of substance P-like immunoreactivity in some 5-hydroxytryptamine-containing neurons in the rat central nervous system. Neuroscience. 1978;3(6):517–538. doi: 10.1016/0306-4522(78)90017-9. [DOI] [PubMed] [Google Scholar]
  13. Jacobs B. L., Azmitia E. C. Structure and function of the brain serotonin system. Physiol Rev. 1992 Jan;72(1):165–229. doi: 10.1152/physrev.1992.72.1.165. [DOI] [PubMed] [Google Scholar]
  14. Jessell T., Tsunoo A., Kanazawa I., Otsuka M. Substance P: depletion in the dorsal horn of rat spinal cord after section of the peripheral processes of primary sensory neurons. Brain Res. 1979 May 25;168(2):247–259. doi: 10.1016/0006-8993(79)90167-7. [DOI] [PubMed] [Google Scholar]
  15. Johansson O., Hökfelt T., Pernow B., Jeffcoate S. L., White N., Steinbusch H. W., Verhofstad A. A., Emson P. C., Spindel E. Immunohistochemical support for three putative transmitters in one neuron: coexistence of 5-hydroxytryptamine, substance P- and thyrotropin releasing hormone-like immunoreactivity in medullary neurons projecting to the spinal cord. Neuroscience. 1981;6(10):1857–1881. doi: 10.1016/0306-4522(81)90028-2. [DOI] [PubMed] [Google Scholar]
  16. Johnson S. M., Katayama Y., Morita K., North R. A. Mediators of slow synaptic potentials in the myenteric plexus of the guinea-pig ileum. J Physiol. 1981 Nov;320:175–186. doi: 10.1113/jphysiol.1981.sp013942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kanazawa I., Sutoo D., Oshima I., Saito S. Effect of transection on choline acetyltransferase, thyrotropin releasing hormone and substance P in the cat cervical cord. Neurosci Lett. 1979 Aug;13(3):325–330. doi: 10.1016/0304-3940(79)91514-3. [DOI] [PubMed] [Google Scholar]
  18. Millhorn D. E., Hökfelt T., Verhofstad A. A., Terenius L. Individual cells in the raphe nuclei of the medulla oblongata in rat that contain immunoreactivities for both serotonin and enkephalin project to the spinal cord. Exp Brain Res. 1989;75(3):536–542. doi: 10.1007/BF00249904. [DOI] [PubMed] [Google Scholar]
  19. Nussbaumer J. C., Yanagisawa M., Otsuka M. Pharmacological properties of a C-fibre response evoked by saphenous nerve stimulation in an isolated spinal cord-nerve preparation of the newborn rat. Br J Pharmacol. 1989 Oct;98(2):373–382. doi: 10.1111/j.1476-5381.1989.tb12607.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Otsuka M., Yoshioka K. Neurotransmitter functions of mammalian tachykinins. Physiol Rev. 1993 Apr;73(2):229–308. doi: 10.1152/physrev.1993.73.2.229. [DOI] [PubMed] [Google Scholar]
  21. Pelletier G., Steinbusch H. W., Verhofstad A. A. Immunoreactive substance P and serotonin present in the same dense-core vesicles. Nature. 1981 Sep 3;293(5827):71–72. doi: 10.1038/293071a0. [DOI] [PubMed] [Google Scholar]
  22. Randić M., Ryu P. D., Urban L. Effects of polyclonal and monoclonal antibodies to substance P on slow excitatory transmission in rat spinal dorsal horn. Brain Res. 1986 Sep 24;383(1-2):15–27. doi: 10.1016/0006-8993(86)90003-x. [DOI] [PubMed] [Google Scholar]
  23. Roques B. P., Fournié-Zaluski M. C., Soroca E., Lecomte J. M., Malfroy B., Llorens C., Schwartz J. C. The enkephalinase inhibitor thiorphan shows antinociceptive activity in mice. Nature. 1980 Nov 20;288(5788):286–288. doi: 10.1038/288286a0. [DOI] [PubMed] [Google Scholar]
  24. Suzue T., Yanaihara N., Otsuka M. Actions of vasopressin, gastrin releasing peptide and other peptides on neurons on newborn rat spinal cord in vitro. Neurosci Lett. 1981 Oct 23;26(2):137–142. doi: 10.1016/0304-3940(81)90339-6. [DOI] [PubMed] [Google Scholar]
  25. Suzuki H., Yoshioka K., Yanagisawa M., Urayama O., Kurihara T., Hosoki R., Saito K., Otsuka M. Involvement of enzymatic degradation in the inactivation of tachykinin neurotransmitters in neonatal rat spinal cord. Br J Pharmacol. 1994 Sep;113(1):310–316. doi: 10.1111/j.1476-5381.1994.tb16210.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Takahashi T. Thyrotropin-releasing hormone mimics descending slow synaptic potentials in rat spinal motoneurons. Proc R Soc Lond B Biol Sci. 1985 Sep 23;225(1240):391–398. doi: 10.1098/rspb.1985.0068. [DOI] [PubMed] [Google Scholar]
  27. Tsunoo A., Konishi S., Otsuka M. Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience. 1982;7(9):2025–2037. doi: 10.1016/0306-4522(82)90117-8. [DOI] [PubMed] [Google Scholar]
  28. Ulfhake B., Arvidsson U., Cullheim S., Hökfelt T., Brodin E., Verhofstad A., Visser T. An ultrastructural study of 5-hydroxytryptamine-, thyrotropin-releasing hormone- and substance P-immunoreactive axonal boutons in the motor nucleus of spinal cord segments L7-S1 in the adult cat. Neuroscience. 1987 Dec;23(3):917–929. doi: 10.1016/0306-4522(87)90168-0. [DOI] [PubMed] [Google Scholar]
  29. Urbán L., Randić M. Slow excitatory transmission in rat dorsal horn: possible mediation by peptides. Brain Res. 1984 Jan 9;290(2):336–341. doi: 10.1016/0006-8993(84)90952-1. [DOI] [PubMed] [Google Scholar]
  30. Vacca L. L., Hobbs J., Abrahams S., Naftchi E. Ultrastructural localization of substance P immunoreactivity in the ventral horn of the rat spinal cord. Histochemistry. 1982;76(1):33–49. doi: 10.1007/BF00493283. [DOI] [PubMed] [Google Scholar]
  31. Wallis D. I., Wu J. The pharmacology of descending responses evoked by thoracic stimulation in the neonatal rat spinal cord in vitro. Naunyn Schmiedebergs Arch Pharmacol. 1993 Jun;347(6):643–651. doi: 10.1007/BF00166948. [DOI] [PubMed] [Google Scholar]
  32. Ward P., Ewan G. B., Jordan C. C., Ireland S. J., Hagan R. M., Brown J. R. Potent and highly selective neurokinin antagonists. J Med Chem. 1990 Jul;33(7):1848–1851. doi: 10.1021/jm00169a003. [DOI] [PubMed] [Google Scholar]
  33. Yanagisawa M., Otsuka M. Pharmacological profile of a tachykinin antagonist, spantide, as examined on rat spinal motoneurones. Br J Pharmacol. 1990 Aug;100(4):711–716. doi: 10.1111/j.1476-5381.1990.tb14080.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yomono H. S., Suzuki H., Yoshioka K. Serotonergic fibers induce a long-lasting inhibition of monosynaptic reflex in the neonatal rat spinal cord. Neuroscience. 1992;47(3):521–531. doi: 10.1016/0306-4522(92)90162-u. [DOI] [PubMed] [Google Scholar]
  35. de Lanerolle N. C., LaMotte C. C. The morphological relationships between substance P immunoreactive processes and ventral horn neurons in the human and monkey spinal cord. J Comp Neurol. 1982 Jun 1;207(4):305–313. doi: 10.1002/cne.902070402. [DOI] [PubMed] [Google Scholar]

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