Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro

Z. Z. Pan, John Williams, P. B. Osborne

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Abstract

Intracellular recordings were made from neurons of the nucleus raphe magnus (NRM) from rat (n = 128) and guinea-pig (n = 115). Two types of cells were found in each, primary (103 in rat, 27 in guinea-pig) and secondary cells (25 in rat, 88 in guinea-pig). Primary cells had input resistances of 186 ± 9 MΩ (n = 9) in rat and 255 ± 50 MΩ (n = 11) in guinea-pig. The action potential in each was about 1.5 ms in duration. Synaptic potentials were evoked by focal electrical stimulation and consisted of both γ-aminobutyric acid (GABA) and excitatory amino acid components. Morphine, [Met5]enkephalin (ME) and [D-Ala2, N-Me-Phe4, Gly5-ol]enkephalin (DAMGO) depressed the amplitude of the GABA-mediated synaptic potential by a maximum of 50-65% and had little effect on the excitatory amino acid-mediated synaptic potential. There was no effect of these opioids on the resting membrane potential or input resistance of primary cells in rat or guinea-pig. Secondary cells had short duration action potentials (<1 ms) and an input resistance of 354 ± 47 MΩ in rat (n = 6) and 290 ± 40 MΩ in guinea-pig (n = 15). The synaptic potential observed in the cells of this group was mediated by activation of only excitatory amino acid receptors. ME hyperpolarized and/or abolished the spontaneous firing in sixteen out of twenty-four neurons in the secondary group from rat and eighty out of eighty-four neurons from guinea-pig. ME induced an outward current at -60 mV that reversed polarity at potentials more negative than -92 ± 3 mV in rat (n = 6) and -98 ± 2 in guinea-pig (n = 18). The reversal potential of the opioid current was shifted to less mV negative potentials when the external potassium concentration was increased, as predicted by the Nernst equation. The morphology of the two types of cells were distinguishable in that primary cells were oval (29 x 18 μm in rat; 36 x 19 μm in guinea-pig) with two to four thick tapering dendrites that branched within 50 μm of the cell body. Secondary cells were generally round or oval (about 24 x 13 μm in rat; 27 x 17 μm in guinea-pig) with two to five thin non-tapering dendrites. The results suggest that opioids increase the activity of a population of Nrm neurons by presynaptic depression of GABA-mediated inhibitory input. This could be one of the mechanisms by which opioids modulate the descending inhibition from the Nrm in the endogenous pain-modulation system.

Original languageEnglish (US)
Pages (from-to)519-532
Number of pages14
JournalJournal of Physiology
Volume427
StatePublished - 1990

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Opioid Analgesics
Guinea Pigs
Neurons
Synaptic Potentials
Enkephalins
gamma-Aminobutyric Acid
Excitatory Amino Acids
Dendrites
Action Potentials
Nucleus Raphe Magnus
In Vitro Techniques
Aminobutyrates
Glutamate Receptors
Membrane Potentials
Morphine
Electric Stimulation
Potassium
Pain

ASJC Scopus subject areas

  • Physiology

Cite this

Opioid actions on single nucleus raphe magnus neurons from rat and guinea-pig in vitro. / Pan, Z. Z.; Williams, John; Osborne, P. B.

In: Journal of Physiology, Vol. 427, 1990, p. 519-532.

Research output: Contribution to journalArticle

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N2 - Intracellular recordings were made from neurons of the nucleus raphe magnus (NRM) from rat (n = 128) and guinea-pig (n = 115). Two types of cells were found in each, primary (103 in rat, 27 in guinea-pig) and secondary cells (25 in rat, 88 in guinea-pig). Primary cells had input resistances of 186 ± 9 MΩ (n = 9) in rat and 255 ± 50 MΩ (n = 11) in guinea-pig. The action potential in each was about 1.5 ms in duration. Synaptic potentials were evoked by focal electrical stimulation and consisted of both γ-aminobutyric acid (GABA) and excitatory amino acid components. Morphine, [Met5]enkephalin (ME) and [D-Ala2, N-Me-Phe4, Gly5-ol]enkephalin (DAMGO) depressed the amplitude of the GABA-mediated synaptic potential by a maximum of 50-65% and had little effect on the excitatory amino acid-mediated synaptic potential. There was no effect of these opioids on the resting membrane potential or input resistance of primary cells in rat or guinea-pig. Secondary cells had short duration action potentials (<1 ms) and an input resistance of 354 ± 47 MΩ in rat (n = 6) and 290 ± 40 MΩ in guinea-pig (n = 15). The synaptic potential observed in the cells of this group was mediated by activation of only excitatory amino acid receptors. ME hyperpolarized and/or abolished the spontaneous firing in sixteen out of twenty-four neurons in the secondary group from rat and eighty out of eighty-four neurons from guinea-pig. ME induced an outward current at -60 mV that reversed polarity at potentials more negative than -92 ± 3 mV in rat (n = 6) and -98 ± 2 in guinea-pig (n = 18). The reversal potential of the opioid current was shifted to less mV negative potentials when the external potassium concentration was increased, as predicted by the Nernst equation. The morphology of the two types of cells were distinguishable in that primary cells were oval (29 x 18 μm in rat; 36 x 19 μm in guinea-pig) with two to four thick tapering dendrites that branched within 50 μm of the cell body. Secondary cells were generally round or oval (about 24 x 13 μm in rat; 27 x 17 μm in guinea-pig) with two to five thin non-tapering dendrites. The results suggest that opioids increase the activity of a population of Nrm neurons by presynaptic depression of GABA-mediated inhibitory input. This could be one of the mechanisms by which opioids modulate the descending inhibition from the Nrm in the endogenous pain-modulation system.

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