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. 1994 Sep;113(1):303–309. doi: 10.1111/j.1476-5381.1994.tb16209.x

Inhibition by opioids acting on mu-receptors of GABAergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro.

B Chieng 1, M J Christie 1
PMCID: PMC1510063  PMID: 7812626

Abstract

1. Membrane properties of rat periaqueductal gray neurones were investigated by use of intracellular recordings from single neurones in brain slices. Morphological properties and anatomical location of each impaled neurone were characterized by intracellular staining with biocytin. The present paper considers the properties of electrically-evoked and spontaneous postsynaptic potentials impinging on periaqueductal gray neurones, and the actions of opioids on postsynaptic potentials in neurones which were not directly hyperpolarized by opioids. The preceding paper considers neurones which were hyperpolarized by opioids. 2. Electrical stimulation in the vicinity of impaled neurones evoked postsynaptic potentials having fast (duration at half-maximal amplitude 37 +/- 2 ms, n = 65) and in some cases slow (duration at half-maximal amplitude 817 +/- 187 ms, n = 3) components. Amplitudes of evoked potentials were dependent on stimulus voltage, membrane potential, and were abolished during superfusion with solutions containing tetrodoxotoxin (100 nM to 1 microM, n = 5) or Co2+ (4 mM, n = 2). 3. Fast postsynaptic potentials were mediated predominantly by activation of glutamate and GABAA receptors. The GABAA-receptor antagonist, bicucuilline (30 microM), inhibited postsynaptic potentials by 44 +/- 8% (n = 14). The non-NMDA-receptor antagonist, 6-cyano-7-nitroquinoxaline-2,3-dione (10 microM), inhibited postsynaptic potentials by 48 +/- 6% (n = 16). Combined superfusion of bicuculline (30 microM) and 6-cyano-7-nitroquinoxaline-2,3-dione (10 microM) inhibited postsynaptic potentials by 93 +/- 1% (n = 8). Additional superfusion of the NMDA-receptor antagonist, (+/-)-2-amino-5- phosphonovaleric acid (50 microM) inhibited synaptic potentials by 94 +/- 1% (n = 3).(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. Basbaum A. I., Fields H. L. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci. 1984;7:309–338. doi: 10.1146/annurev.ne.07.030184.001521. [DOI] [PubMed] [Google Scholar]
  2. Beart P. M., Summers R. J., Stephenson J. A., Cook C. J., Christie M. J. Excitatory amino acid projections to the periaqueductal gray in the rat: a retrograde transport study utilizing D[3H]aspartate and [3H]GABA. Neuroscience. 1990;34(1):163–176. doi: 10.1016/0306-4522(90)90310-z. [DOI] [PubMed] [Google Scholar]
  3. Behbehani M. M., Jiang M., Chandler S. D. The effect of [Met]enkephalin on the periaqueductal gray neurons of the rat: an in vitro study. Neuroscience. 1990;38(2):373–380. doi: 10.1016/0306-4522(90)90035-3. [DOI] [PubMed] [Google Scholar]
  4. Behbehani M. M., Liu H., Jiang M., Pun R. Y., Shipley M. T. Activation of serotonin1A receptors inhibits midbrain periaqueductal gray neurons of the rat. Brain Res. 1993 May 28;612(1-2):56–60. doi: 10.1016/0006-8993(93)91643-7. [DOI] [PubMed] [Google Scholar]
  5. Chieng B., Christie M. J. Hyperpolarization by opioids acting on mu-receptors of a sub-population of rat periaqueductal gray neurones in vitro. Br J Pharmacol. 1994 Sep;113(1):121–128. doi: 10.1111/j.1476-5381.1994.tb16183.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clements J. R., Beitz A. J., Fletcher T. F., Mullett M. A. Immunocytochemical localization of serotonin in the rat periaqueductal gray: a quantitative light and electron microscopic study. J Comp Neurol. 1985 Jun 1;236(1):60–70. doi: 10.1002/cne.902360106. [DOI] [PubMed] [Google Scholar]
  7. Egan T. M., Henderson G., North R. A., Williams J. T. Noradrenaline-mediated synaptic inhibition in rat locus coeruleus neurones. J Physiol. 1983 Dec;345:477–488. doi: 10.1113/jphysiol.1983.sp014990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Fields H. L., Heinricher M. M., Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci. 1991;14:219–245. doi: 10.1146/annurev.ne.14.030191.001251. [DOI] [PubMed] [Google Scholar]
  9. Herbert H., Saper C. B. Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J Comp Neurol. 1992 Jan 1;315(1):34–52. doi: 10.1002/cne.903150104. [DOI] [PubMed] [Google Scholar]
  10. Johnson S. W., North R. A. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci. 1992 Feb;12(2):483–488. doi: 10.1523/JNEUROSCI.12-02-00483.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lacey M. G., Mercuri N. B., 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. 1989 Apr;9(4):1233–1241. doi: 10.1523/JNEUROSCI.09-04-01233.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Madison D. V., Nicoll R. A. Enkephalin hyperpolarizes interneurones in the rat hippocampus. J Physiol. 1988 Apr;398:123–130. doi: 10.1113/jphysiol.1988.sp017033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McFadzean I., Lacey M. G., Hill R. G., Henderson G. Kappa opioid receptor activation depresses excitatory synaptic input to rat locus coeruleus neurons in vitro. Neuroscience. 1987 Jan;20(1):231–239. doi: 10.1016/0306-4522(87)90015-7. [DOI] [PubMed] [Google Scholar]
  14. Pan Z. Z., Colmers W. F., Williams J. T. 5-HT-mediated synaptic potentials in the dorsal raphe nucleus: interactions with excitatory amino acid and GABA neurotransmission. J Neurophysiol. 1989 Aug;62(2):481–486. doi: 10.1152/jn.1989.62.2.481. [DOI] [PubMed] [Google Scholar]
  15. Pan Z. Z., Williams J. T., Osborne P. B. Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. J Physiol. 1990 Aug;427:519–532. doi: 10.1113/jphysiol.1990.sp018185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Reichling D. B., Basbaum A. I. Contribution of brainstem GABAergic circuitry to descending antinociceptive controls: I. GABA-immunoreactive projection neurons in the periaqueductal gray and nucleus raphe magnus. J Comp Neurol. 1990 Dec 8;302(2):370–377. doi: 10.1002/cne.903020213. [DOI] [PubMed] [Google Scholar]
  17. Reichling D. B., Basbaum A. I. Contribution of brainstem GABAergic circuitry to descending antinociceptive controls: II. Electron microscopic immunocytochemical evidence of GABAergic control over the projection from the periaqueductal gray to the nucleus raphe magnus in the rat. J Comp Neurol. 1990 Dec 8;302(2):378–393. doi: 10.1002/cne.903020214. [DOI] [PubMed] [Google Scholar]
  18. Yaksh T. L., Al-Rodhan N. R., Jensen T. S. Sites of action of opiates in production of analgesia. Prog Brain Res. 1988;77:371–394. doi: 10.1016/s0079-6123(08)62803-4. [DOI] [PubMed] [Google Scholar]

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