Opioids suppress spontaneous and NMDA-induced inhibitory postsynaptic currents in the dorsal raphe nucleus of the rat in vitro

Brain Research

Volumn 755, Issue 2, 1997, Pages 229-245

  Jolas, Thierry ^a   Aghajanian, George K ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

aminobutyric acid (GABA); brain slice; dorsal raphe; interneuron; intracellular; opioid; periaqueductal gray; serotonergic

Indexed keywords

3,4 DICHLORO N METHYL N [2 (1 PYRROLIDINYL)CYCLOHEXYL]BENZENEACETAMIDE; 6 [2 (1H TETRAZOL 5 YL)ETHYL]DECAHYDRO 3 ISOQUINOLINECARBOXYLIC ACID; BICUCULLINE; DECAHYDRO 6 [2 (1H TETRAZOL 5 YL)ETHYL] 3 ISOQUINOLINECARBOXYLIC ACID; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLORNITHYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; METENKEPHALIN; N METHYL DEXTRO ASPARTIC ACID; OPIATE AGONIST; OPIATE ANTAGONIST; OPIATE PEPTIDE; PHENYLEPHRINE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; IONTOPHORESIS; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAPHE NUCLEUS; RAT; SEROTONINERGIC NERVE CELL;

ANIMALS; DRUG EVALUATION, PRECLINICAL; ENKEPHALIN, METHIONINE; EVOKED POTENTIALS; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; IONTOPHORESIS; MALE; NARCOTICS; NEURONS; PATCH-CLAMP TECHNIQUES; RAPHE NUCLEI; RATS; RECEPTORS, N-METHYL-D-ASPARTATE; SEROTONIN;

EID: 0030898428     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)00103-0     Document Type: Article

References (72)

1. Aghajanian, G.K., Rosecrans, J.A. and Sheard, M.H., Serotonin: release in the forebrain by stimulation of midbrain raphé, Science, 156 (1967) 402-403.
2. Aghajanian, G.K. and Vandermaelen, C.P., Intracellular identification of central noradrenergic and serotonergic neurons by double labeling procedure, J. Neurosci., 2 (1982) 1786-1792.
3. Aghajanian, G.K., Wang, R.Y. and Baraban, J., Serotonergic and non-serotonergic neurons of the dorsal raphe: reciprocal changes in firing induced by peripheral nerve stimulation, Brain Res., 153 (1978) 169-175.
4. 1A receptors inhibits midbrain periaqueductal gray neurons of the rat, Brain Res., 612 (1993) 56-60.
5. Belin, M.F., Aguera, M., Tappaz, M., McRae-Degueurce, A., Bobillier, P. and Pujol, J.F., Gaba-accumulating neurons in the nucleus raphe dorsalis and periaqueductal gray in the rat: A biochemical and radioautographic study, Brain Res., 170 (1979) 279-297.
6. Bineau-Thurotte, M., Godefroy, F., Weil-Fugazza, J. and Besson, J.M., The effect of morphine on the potassium evoked release of tritiated 5-hydroxytryptamine from spinal cord slices in the rat, Brain Res., 291 (1984) 293-299.
7. Boadle-Biber, M.C., Johannessen, J.N., Narasimhachari, N. and Phan, T.-H., Activation of cortical tryptophan hydroxylase by acute morphine treatment: blockade by 6-hydroxydopamine, Eur. J. Pharmacol., 139 (1987) 193-204.
8. 2+ conductance, Synapse, 1 (1987) 582-588.
9. + channel, J. Biol. Chem., 269 (1993) 7839-7842.
10. Chieng, B. and Christie, M.J., Hyperpolarization by opioids acting on μ-receptors of a sub-population of rat periaqueductal gray neurones in vitro, Br. J. Pharmacol., 113 (1994) 121-128.
11. Chieng, B. and Christie, M.J., Inhibition by opioids acting on μ-receptors of GABAergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro, Br. J. Pharmacol., 113 (1994) 303-309.
12. Dafny, N., Reyes-Vasquez, C. and Qiao, J.T., Modification of Nociceptively identified neurons in thalamic parafascicularis by chemical stimulation of dorsal raphe with glutamate, morphine, serotonin and focal dorsal raphe electrical stimulation, Brain Res. Bull., 24 (1989) 717-723.
13. Dascal, N., Lim, N.F., Schreibmayer, W., Wang, W., Davidson, N. and Lester, H.A., Expression of an atrial G-protein-activated potassium channel in Xenopus oocytes, Proc. Natl. Acad. Sci. USA, 90 (1993) 6596-6600.
14. + channel: expression cloning and molecular properties, Proc. Natl. Acad. Sci. USA, 90 (1993) 10235-10239.
15. DePaoli, A.M., Bell, G.I. and Stoffel, M., G protein-activated inwardly rectifying potassium channel (GIRK1/KGA) mRNA in adult rat heart and brain by in situ hybridization histochemistry, Mol. Cell. Neurosci., 5 (1994) 515-522.
16. Duggan, A.W. and North, R.A., Electrophysiology of opioids, Pharmacol. Rev., 35 (1983) 219-281.
17. Gallager, D.W. and Aghajanian, G.K., Effect of antipsychotic drugs on the firing of dorsal raphe cells. II. Reversal by picrotoxin, Brain Res., 39 (1976) 357-364.
18. Goodman, L.A., Kolmogorov-Smirnov tests for psychological research, Psychol. Bull., 51 (1954) 160-168.
19. 3 receptors in drug dependence, Drug Alcohol Depend., 38 (1995) 155-171.
20. Gysling, K. and Wang, R., Morphine-induced activation of A10 dopamine neurons in the rat, Brain Res., 211 (1983) 119-127.
21. Haigler, H.J., Morphine: Effects on serotonergic neurons and neurons in areas with a serotonergic input, Eur. J. Pharmacol., 51 (1978) 361-376.
22. Harandi, M., Aguera, M., Gamrani, H., Didier, M., Maitre, M., Calas, A. and Belin, M., γ-Aminobutiric acid and 5-hydroxytryptamine interrelationships in the rat nucleus raphe dorsalis: combination of radioautographic and immunocytochemical techniques at light and electron microscopy levels, Neuroscience, 21 (1987) 237-251.
23. Isaacson, J.S. and Walmsley, B., Receptors underlying excitatory synaptic transmission in slices of the rat anteroventral cochlear nucleus, J. Neurophysiol., 73 (1995) 964-973.
24. Johnson, S.W. and North, R.A., Opioids excite dopamine neurons by hyperpolarization of local interneurons, J. Neurosci., 12 (1992) 483-488.
25. Jolas, T. and Aghajanian, G.K., Neurotensin excitation of serotonergic neurons in the dorsal raphe nucleus of the rat in vitro, Eur. J. Neurosci., 8 (1996) 153-161.
26. 3H]aspartate tracing, Brain Res., 360 (1985) 285-297.
27. Kawaguchi, Y., Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex, J. Neurophysiol., 69 (1993) 416-431.
28. Kawaguchi, Y., Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex, J. Neurosci., 15 (1995) 2638-2655.
29. Klitenick, M.A., DeWitte, P. and Kalivas, P.W., Regulation of somatodendritic dopamine release in the ventral tegmental area by opioids and GABA: an in vivo microdialysis study, J. Neurosci., 12 (1992) 2623-2632.
30. Kovoor, A., Henry, D.J. and Chavkin, C., Agonist-induced desensitization of the mu opioid receptor-coupled potassium channel (GIRK1), J. Biol. Chem., 270 (1995) 589-595.
31. Kubo, Y., Reuveny, E., Slesinger, P.A., Jan, Y.N. and Jan, L.Y., Primary structure and functional expression of a rat G-protein-coupled muscarinic potassium channel, Nature, 364 (1993) 802-806.
32. Lacey, M.G., Mercuri, N.B. and North, R.A., Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids, J. Neurosci., 9 (1989) 1233-1241.
33. Levine, E.S. and Jacobs, B.L., Neurochemical afferents controlling the activity of serotonergic neurons in the dorsal raphe nucleus: microiontophoretic studies in the awake cat, J. Neurosci., 12 (1992) 4037-4044.
34. Madison, D.V. and Nicoll, R.A., Enkephalin hyperpolarizes interneurones in the rat hippocampus, J. Physiol., 398 (1988) 123-130.
35. Mansour, A., Fox, C.A., Akil, H. and Watson, S.J., Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications, Trends Neurosci., 18 (1995) 22-29.
36. Messing, R.B., Flinchbaugh, C. and Waymire, J.C., Tryptophan and 5-hydroxyindoles in different CNS regions following acute morphine, Eur. J. Pharmacol., 48 (1978) 137-140.
37. 3H]serotonin from spinal cord synaptosomes, Neuropharmacology, 25 (1986) 261-265.
38. Nanopoulos, D., Belin, M.F., Maitre, M., Vincendon, G. and Pujol, J.F., Immunocytochemical evidence for the existence of GABAergic neurons in nucleus raphe dorsalis. Possible existence of neurons containing serotonin and GABA, Brain Res., 232 (1982) 375-389.
39. Nicoll, R.A., Alger, B.E. and Jahr, C.E., Enkephalin blocks inhibitory pathways in the vertebrate CNS, Nature, 287 (1980) 22-25.
40. Osmanovic, S.S. and Shefner, S.A., Anomalous rectification in rat locus coeruleus neurons, Brain Res., 417 (1987) 161-166.
41. Pan, Z.Z., Wessendorf, M.W. and Williams, J.T., Modulation by serotonin of the neurons in rat nucleus raphe magnus in vitro, Neuroscience, 54 (1993) 421-429.
42. Pan, Z.Z. and Williams, J.T., GABA- and glutamate-mediated synaptic potentials in rat dorsal raphe neurons in vitro, J. Neurophysiol., 61 (1989) 719-726.
43. Pan, Z.Z., Williams, J.T. and Osborne, P.B., Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro, J. Physiol., 427 (1990) 519-532.
44. Park, M.R., Intracellular horseradish peroxidase labeling of rapidly firing dorsal raphe projection neurons, Brain Res., 402 (1987) 117-130.
45. Penington, N.J., Kelly, J.S. and Fox, A.P., Unitary properties of potassium channels activated by 5-HT in acutely isolated rat dorsal raphe neurones, J. Physiol., 469 (1993) 407-426.
46. 1A receptors on dorsal raphe neurones of the adult rat, J. Physiol., 469 (1993) 387-405.
47. Pinnock, R.D., Activation of κ-opioid receptors depresses electrically evoked excitatory postsynaptic potentials on 5-HT-sensitive neurones in the rat dorsal raphé nucleus in vitro, Brain Res., 583 (1992) 237-246.
48. Pinnock, R.D., A highly selective κ-opioid receptor agonist, CI-977, reduces excitatory synaptic potentials in the rat locus coeruleus in vitro, Neuroscience, 47 (1992) 87-94.
49. Rampon, C., Peyron, C., Gervasoni, D., Cespuglio, R., Fort, P. and Luppi, P.-H., Localization of the glycinergic neurons projecting to the rat locus coeruleus, dorsal raphe and trigeminal motor nuclei, Soc. Neurosci. Abstr., 22 (1996) 1838.
50. Rivot, J.P., Pointis, D. and Besson, J.M., In vivo electrochemical detection of 5-hydroxyindole within the trigeminal nucleus caudalis of freely moving rats: the effect of morphine, Brain Res., 463 (1988) 275-283.
51. Rompré, P.P. and Boye, S., Localization of reward-relevant neurons in the pontine tegmentum: a moveable electrode mapping study, Brain Res., 496 (1989) 295-302.
52. Rompré, P.P. and Wise, R.A., Opioid-neuroleptic interaction in brainstem self-stimulation, Brain Res., 477 (1989) 144-151.
53. Sharp, T., Bramwell, S.R., Clark, D. and Grahame-Smith, D.G., In vivo measurement of extracellular 5-hydroxytryptamine in hippocampus of anaesthetized rat using microdialysis: changes in relation to 5-hydroxytryptaminergic neuronal activity, J. Neurochem., 53 (1989) 234-240.
54. Siggins, G.R. and Zieglgänsberger, W., Morphine and opioid peptides reduce inhibitory synaptic potentials in hippocampal pyramidal cells in vitro without alteration of membrane potential, Proc. Natl. Acad. Sci. USA, 78 (1981) 5235-5239.
55. Smith, G.S.T., Savery, D., Marden, C., Lopez Costa, J.J., Averill, S., Priestley, J.V. and Rattray, M., Distribution of messenger RNAs encoding enkephalin, substance P, somatostatin, galanin, vasoactive intestinal polypeptide, neuropeptide Y, and calcitonin gene-related peptide in the midbrain periaqueductal grey in the rat, J. Comp. Neurol., 350 (1994) 23-40.
56. 1A autoreceptors on serotonergic neurons in the midbrain raphe nuclei, Eur. J. Neurosci., 2 (1990) 1144-1154.
57. Spampinato, U., Esposito, E., Romandini, S. and Samanin, R., Changes of serotonin and dopamine metabolism in various forebrain areas of rats injected with morphine either systemically or in the raphe nuclei dorsalis and medianus, Brain Res., 328 (1985) 89-95.
58. Tao, R. and Auerbach, S.B., Anesthetics block morphine-induced increases in serotonin release in rat CNS, Synapse, 18 (1994) 307-314.
59. Tao, R. and Auerbach, S.B., Increased extracellular serotonin in rat brain after systemic or intraraphe administration of morphine, J. Neurochem., 63 (1994) 517-524.
60. VanderMaelen, C.P. and Aghajanian, G.K., Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices, Brain Res., 289 (1983) 109-119.
61. Wang, Q.P., Guan, J.L. and Nakai, Y., Immunoelectron microscopy of enkephalinergic innervation of GABAergic neurons in the periaqueductal gray, Brain Res., 665 (1994) 39-46.
62. Wang, Q.P. and Nakai, Y., Enkephalinergic innervation of GABAergic neurons in the dorsal raphe nucleus of the rat, Brain Res. Bull., 32 (1993) 315-320.
63. Wang, Q.P. and Nakai, Y., The dorsal raphe: an important nucleus in pain modulation, Brain Res. Bull., 34 (1994) 575-585.
64. Wang, Q.P., Nakai, Y. and Shioda, S., Enkephalinergic synaptic axon terminals on serotonergic neurons in the dorsal raphe nucleus of the rat: an electron microscopic study by the double immunostaining method, Neurosci. Lett., 124 (1991) 129-132.
65. Wang, Q.P., Ochiai, H. and Nakai, Y., GABAergic innervation of serotonergic neurons in the dorsal raphe nucleus of the rat studied by electron microscopy double immunostaining, Brain Res. Bull., 29 (1992) 943-948.
66. Weil-Fugazza, J., Godefroy, F. and Besson, J.M., Changes in brain and spinal tryptophan and 5-hydroxyindoleacetic acid levels following acute morphine administration in normal and arthritic rats, Brain Res., 175 (1979) 291-301.
67. Williams, F.G. and Beitz, A.J., Ultrastructural morphometric analysis of enkephalin-immunoreactive terminals in the ventrocaudal periaqueductal gray: analysis of their relationship to periaqueductal gray-raphe magnus projection neurons, Neuroscience, 38 (1990) 381-394.
68. Williams, J.T., Colmers, W.F. and Pan, Z.Z., Voltage- and ligand- activated inwardly rectifying currents in dorsal raphe neurons in vitro, J. Neurosci., 8 (1988) 3499-3506.
69. Williams, J.T., Egan, T.M. and North, R.A., Enkephalin opens potassium channels on mammalian central neurones, Nature, 299 (1982) 74-77.
70. Williams, J.T., North, R.A. and Tokimasa, T., Inward rectification of resting and opiate-activated potassium currents in rat locus coeruleus neurons, J. Neurosci., 8 (1988) 4299-4306.
71. Yaksh, T.L. and Tyce, G.M., Microinjection of morphine into the periaqueductal gray evokes the release of serotonin from spinal cord, Brain Res., 171 (1979) 176-181.
72. Zieglgänsberger, W., French, E.D., Siggins, G.R. and Bloom, F.E., Opioid peptides may excite hippocampal neurons by inhibiting adjacent interneurons, Science, 205 (1979) 415-417.