Serotonin potentiates the response of neurons of the superficial laminae of the rat spinal dorsal horn to γ-aminobutyric acid

Brain Research Bulletin

Volumn 52, Issue 6, 2000, Pages 559-565

  Li, Hui ^a   Lang, Bing ^a   Kang, Jie Fang ^a   Li, Yun Qing ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

5 HT; Antinociception; GABA; Protein kinase C; Rat; Superficial dorsal horn

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ALPHA METHYLSEROTONIN; CHELERYTHRINE; KETANSERIN; NYSTATIN; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; SEROTONIN; SEROTONIN 2 AGONIST; SEROTONIN 2 ANTAGONIST; SEROTONIN 2 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CHLORIDE CURRENT; CONTROLLED STUDY; ENZYME INHIBITION; NERVE CELL INHIBITION; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; RECEPTOR AFFINITY; RECEPTOR BINDING; SEROTONINERGIC TRANSMISSION; SIGNAL TRANSDUCTION; SLOW INWARD CURRENT; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL;

ANIMALS; CELLS, CULTURED; DRUG INTERACTIONS; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; POSTERIOR HORN CELLS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, SEROTONIN; SEROTONIN; SIGNAL TRANSDUCTION;

EID: 0033847608     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0361-9230(00)00297-5     Document Type: Article

References (47)

1. Antal, M.; Petko, M.; Polgar, E.; Heizmann, C.; Stormmathisen, W. J. Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibers descending from the rostral ventromedial medulla. Neuroscience 73:509-518; 1996.
2. Barber, R. P.; Vaughn, J. E.; Saito, K.; Mclaughlin, B. J.; Roberts, E. GABAergic terminals are presynaptic to primary afferent terminals in the substantia gelatinosa of the rat spinal cord. Brain Res. 141:135-155; 1978.
3. Basbaum, A. I.; Ralston, D. D.; Ralston, H. J. III. Bulbospinal projec-lions in the primates: A light and electromicroscopic study of a pain modulation system. J. Comp. Neurol. 250:311-323; 1986.
4. A receptor subtypes in the spinal cord: An immunohistochemial study. J. Neurosci. 16:283-297; 1996.
5. Carlton, S. M.; Westlund, K. N.; Zhang, D.; Willis, W. D. GABAimmunoreactive terminals synapse on primate spinothalamic tract cells. J. Comp. Neurol. 322:528-537; 1992.
6. Cervero, F.; Bennett, G. J.; Headley, P. M. Processing of sensory information in the superficial dorsal horn of the spinal cord. New York: Plenum; 1995.
7. 2+ block of NMDA-receptor channels as a mechanism of modulation. Nature 356:521-523; 1992.
8. 2 receptors in spinal cord in control of nociceptive responsiveness. Neuropharmacology 30:727-731; 1991.
9. Fields, H. L.; Basbaum, A. I. Central nervous system mechanisms of pain modulation. In: Wall, P. D.; Melzack, R., eds. Textbook of pain, 3rd ed. New York: Churchill Livingstone; 1994:243-257.
10. Grudt, T. J.; Williams, J. T.; Travagli, R. A. Inhibition by 5-hydroxytryptamine and noradrenaline in substantia gelatinosa of guinea-pig spinal trigeminal nucleus. J. Physiol. 485:113-120; 1995.
11. Hentall, Y. D.; Fields, H. L. Actions of opiates, substance P and serotonin on the excitability of primary afferent terminals and observations on interneuronal activity in the neonatal rat's dorsal horn in vitro. Neuroscience 9:521-528; 1983.
12. Hiura, A.; Ishizuka, H.; Villalobos, E. L. GABAergic neurons in the mouse superficial dorsal horn with special emphasis on their relation to primary afferent central terminals. Arch. Histol. Cytol. 54:195-206; 1991.
13. Jones, S. L.; Light, A. R. Termination patterns of serotoninergic medullary raphe-spinal fibres in the rat lumbar spinal cord: An anterograde immunohistochemical study. J. Comp. Neurol. 297:267-282; 1990.
14. Kang, J.-F.; Pang, Z.-P.; Li, Y.-Q. Enhancement of glycine-activated whole-cell currents by serotonin in the superficial laminae neurons of the rat spinal dorsal horn. Chin. J. Neuroanat. 14:333-339; 1998.
15. Knapp, A. A.; Dowling, J. E. Dopamine enhances excitatory amino acid-gated conductances in cultured retinal horizontal cells. Nature 325:437-439; 1987.
16. Kwiat, G. C.; Basbaum, A. I. The origin of brainstem noradrenergic and serotoninergic projections to the spinal cord dorsal horn in the rat. Somatosens. Mot. Res. 9:157-173; 1992.
17. Levy, R. A. The role of GABA in primary afferent depolarization. Prog. Neurobiol. 9:211-267; 1977.
18. Li, J.-L.; Kaneko, T.; Nomura, S.; Li, Y.-Q.; Mizuno, N. Association of serotonin-like immunoreactive axons with nociceptive projection neurons in the caudal spinal trigeminal nucleus of the rat. J. Comp. Neurol. 384:127-141; 1997.
19. 2 receptor and GABA or glycine co-existant neurons in the superficial laminae of the medullary dorsal horn in the rat. Chin. J. Neuroanat. In press.
20. Light, A. R.; Kavookjian, A. M. The ultrastructure and synaptic connections of the spinal terminations from single, physiologically characterized axons descending in the dorsolateral funiculus from the midline, pontomedullary region. J. Comp. Neurol. 234:549-560; 1985.
21. A antagonists reduce the inhibition of primate spinothalamic tract neurons produced by stimulation of periaqueductal gray. Brain Res. 654:286-302; 1994.
22. Mao, J.; Price, D. D.; Mayer, D. J.; Hayes, R. L. Pain-related increases in spinal cord membrane-bound protein kinase C following peripheral nerve injury. Brain Res. 588:144-149; 1992.
23. Millhorn, D. E.; Hokfelt, T.; Seroogy, K.; Oertel, W.; Verhofstad, A. A. J.; Wu, J.-Y. Immunohistochemical evidence for colocalization of γ-aminobutyric acid and serotonin in neurons of the ventral medulla oblongata projecting to the spinal cord. Brain Res. 410:179-185; 1987.
24. Mitchell, K.; Spike, R. C.; Todd, A. J. An immunocytochemical study of glycine receptor and GABA in laminae I-III of rat spinal dorsal horn. J. Neurosci. 13:2371-2381; 1993.
25. A receptors by cAMP-dependent protein phospharylation. Science 257:661-665; 1992.
26. Murase, K.; Randic, M.; Shirasaki, T.; Nakagawa, T.; Akaike, N. Serotonin suppresses N-methyl-D-aspartate responses in acutely isolated spinal dorsal horn neurons of the rat. Brain Res. 525:84-91; 1990.
27. Nagashima, T.; Tanabe, H.; Fujioka, Y. Immunohistochemical localization of protein kinase C isozymes in human cerebellum, hippocampus and spinal cord. Acta. Histochem. Cytochem. 24:441-446; 1991.
28. Palecek, J.; Paleckova, V.; Willis, W. D. The effect of phorbol esters on spinal cord amino acid concentrations and responsiveness of rats to mechanical and thermal stimuli. Pain 80:597-605; 1999.
29. Peng, Y.-B.; Lin, Q.; Willis, W. D. Involvement of protein kinase C in responses of rat dorsal horn neurons to mechanical stimuli and periaqueductal gray descending inhibition. Exp. Brain Res. 114:561-570; 1997.
30. Potrebic, S. B.; Fields, H. L.; Mason, P. Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla. J. Neurosci. 14:1655-1665; 1994.
31. Ren, J.; Ye, J.-H.; McArdle, J. J. cAMP-dependent protein kinase modulation of glycine-activated chloride current in neurons freshly isolated from rat ventral tegmental area. Brain Res. 811:71-78; 1998.
32. Richard, E. C.; Susan, M. C. Receptor localization in the mammalian dorsal horn and primary afferent neurons. Brain Res. Rev. 24:28-66; 1997.
33. Roberts, E. Disinhibition as an organizing principle in the neurons system - The role of the GABA system. Application to neurologic and psychiatric disorders. In: Roberts, E.; Chase, T. N.; Tower, D. B., eds. GABA in nervous system function. New York: Raven Press; 1976: 515-539.
34. Roberts, E. GABA neurons in the mammalian central nervous system: Model for a minimal basic unit. Neurosci. Lett. 47:195-200; 1984.
35. Saito, N.; Kikkawa, U.; Nishizuka, Y.; Tanaka, Ch. Distribution of protein kinase C-like immunoreactive neurons in rat brain. J. Neurosci. 8:369-382; 1988.
36. Sorkin, L. S.; Mcadoo, D. J.; Willis, W. D. Raphe magnus stimulationinduced antinociception in the cat is associated with release of amino acids as well as serotonin in the lumbar dorsal horn. Brain Res. 618:95-108; 1993.
37. Todd, A. J.; Watt, C.; Spike, R. C.; Sieghart, W. Colocalization of GABA, glycine and their receptors at synapses in the rat spinal cord. J. Neurosci. 16:974-982; 1996.
38. Willcockson, W. S.; Chung, J. M.; Hori, Y. Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J. Neurosci. 4:732-740; 1984.
39. Willis, W. D.; Coggeshall, D. Sensory mechanisms of the spinal cord, 2nd ed. New York: Plenum Press; 1991.
40. Willis, W. D. Jr.; Coggeshall, R. E. Functional organization of dorsal horn interneurons. In: Willis, W. D. Jr.; Coggeshall, R. E., eds. Sensory mechanisms of the spinal cord. New York: Plenum Press; 1992:153-215.
41. Worley, P. F.; Baraban, J. M.; Snyder, S. H. Heterogeneous localization of protein kinase C in rat brain: Autoradiographic analysis of phorbol ester receptor binding. J. Neurosci. 6:199-207; 1986.
42. - channel currents in rat sacral dorsal commissural neurons is mediated by protein kinases. Prog. Physiol. Sci. 28:233-236; 1997.
43. Xu, T.-L.; Nabekura, J.; Akaike, N. Protein kinase C-mediated enhancement of glycine response in rat sacral dorsal commissural neurons by serotonin. J. Physiol. 496:491-501; 1996.
44. A response in the sacral dorsal commissural neurons. Br. J. Pharmacol. 124:779-787; 1998.
45. Yang, S.-W.; Zhang, Z.-H.; Wang, R.; Xie, Y.-F.; Qiao, J.-T.; Dafny, N. Norepinephrine and serotonin-induced antinociception are blocked by naloxon with different dosages. Brain Res. Bull. 35:113-117; 1994.
46. Yashpal, K.; Pitcher, G. M.; Parent, A.; Quirion, R.; Coderre, T. J. Noxious thermal and chemical stimulation induce increases in 3Hphorbol 12,13-dibutyrate binding in spinal cord dorsal horn as well as persistent pain and hyperalgesia, which is reduced by inhibition of protein kinase C. J. Neurosci. 15:3263-3272; 1995.
47. Yoshimura, M.; Nishi, S. Primary afferent-evoked glycine- and GABA-mediated IPSPs in substantia gelatinosa neurons in the rat spinal cord in vitro. J. Physiol. 482:29-38; 1995.