Abstract
We used intracellular recording in the hippocampal slice in vitro to characterize further the mechanisms behind the unusual excitatory action of opiates and opioid peptides on hippocampal pyramidal cells in vivo. No significant effect on resting membrane potential, input resistance, or action potential size in cortical area 1 (CA1) pyramidal cells was observed with morphine sulfate, beta-endorphin, [Met5]enkephalin, or [D-Ala2, D-Leu5]enkephalin at 1-50 microM. However, in all cells studied, these agents markedly reduced the size of inhibitory postsynaptic potentials generated by stimulation of the stratum radiatum or alveus. Excitatory postsynaptic potentials were also diminished in many of these cells. The effects of the opioids were antagonized by naloxone. These results are consistent with excitation of pyramidal neurons by a disinhibitory mechanism.
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Selected References
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- ANDERSEN P., ECCLES J. C., LOYNING Y. PATHWAY OF POSTSYNAPTIC INHIBITION IN THE HIPPOCAMPUS. J Neurophysiol. 1964 Jul;27:608–619. doi: 10.1152/jn.1964.27.4.608. [DOI] [PubMed] [Google Scholar]
- Alger B. E., Nicoll R. A. GABA-mediated biphasic inhibitory responses in hippocampus. Nature. 1979 Sep 27;281(5729):315–317. doi: 10.1038/281315a0. [DOI] [PubMed] [Google Scholar]
- Barker J. L., Neale J. H., Smith T. G., Jr, Macdonald R. L. Opiate peptide modulation of amino acid responses suggests novel form of neuronal communication. Science. 1978 Mar 31;199(4336):1451–1453. doi: 10.1126/science.204016. [DOI] [PubMed] [Google Scholar]
- Bloom F., Bayon A., Battenberg E., French E., Koda L., Koob G., Le Moal M., Rossier J., Shoemaker W. Endorphins: developmental, cellular, and behavioral aspects. Adv Biochem Psychopharmacol. 1980;22:619–632. [PubMed] [Google Scholar]
- Bornstein J. C., Fields H. L. Morphine presynaptically inhibits a ganglionic cholinergic synapse. Neurosci Lett. 1979 Nov;15(1):77–82. doi: 10.1016/0304-3940(79)91532-5. [DOI] [PubMed] [Google Scholar]
- Corrigall W. A., Linseman M. A. A specific effect of morphine on evoked activity in the rat hippocampal slice. Brain Res. 1980 Jun 16;192(1):227–238. doi: 10.1016/0006-8993(80)91022-7. [DOI] [PubMed] [Google Scholar]
- Deadwyler S. A., Robinson J. H. Effects of morphine on hippocampal cells recorded in vitro. Brain Res Bull. 1979 Sep-Oct;4(5):609–613. doi: 10.1016/0361-9230(79)90101-1. [DOI] [PubMed] [Google Scholar]
- Dunwiddie T., Mueller A., Palmer M., Stewart J., Hoffer B. Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus. I. Effects on pyramidal cell activity. Brain Res. 1980 Feb 24;184(2):311–330. doi: 10.1016/0006-8993(80)90801-x. [DOI] [PubMed] [Google Scholar]
- French E. D., Siggins G. R. An iontophoretic survey of opioid peptide actions in the rat limbic system: in search of opiate epileptogenic mechanisms. Regul Pept. 1980 Oct;1(2):127–146. doi: 10.1016/0167-0115(80)90016-6. [DOI] [PubMed] [Google Scholar]
- Frenk H., Urca G., Liebeskind J. C. Epileptic properties of leucine- and methionine-enkephalin: comparison with morphine and reversibility by naloxone. Brain Res. 1978 May 26;147(2):327–337. doi: 10.1016/0006-8993(78)90843-0. [DOI] [PubMed] [Google Scholar]
- Gähwiler B. H. Excitatory action of opioid peptides and opiates on cultured hippocampal pyramidal cells. Brain Res. 1980 Jul 21;194(1):193–203. doi: 10.1016/0006-8993(80)91328-1. [DOI] [PubMed] [Google Scholar]
- Haas H. L., Ryall R. W. Is excitation by enkephalins of hippocampal neurones in the rat due to presynaptic facilitation or to disinhibition? J Physiol. 1980 Nov;308:315–330. doi: 10.1113/jphysiol.1980.sp013473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henriksen S. J., Bloom F. E., McCoy F., Ling N., Guillemin R. beta-Endorphin induces nonconvulsive limbic seizures. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5221–5225. doi: 10.1073/pnas.75.10.5221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jessell T. M., Iversen L. L. Opiate analgesics inhibit substance P release from rat trigeminal nucleus. Nature. 1977 Aug 11;268(5620):549–551. doi: 10.1038/268549a0. [DOI] [PubMed] [Google Scholar]
- Konishi S., Tsunoo A., Otsuka M. Enkephalins presynaptically inhibit cholinergic transmission in sympathetic ganglia. Nature. 1979 Nov 29;282(5738):515–516. doi: 10.1038/282515a0. [DOI] [PubMed] [Google Scholar]
- Lee H. K., Dunwiddie T., Hoffer B. Electrophysiological interactions of enkephalins with neuronal circuitry in the rat hippocampus. II. Effects on interneuron excitability. Brain Res. 1980 Feb 24;184(2):331–342. doi: 10.1016/0006-8993(80)90802-1. [DOI] [PubMed] [Google Scholar]
- Mudge A. W., Leeman S. E., Fischbach G. D. Enkephalin inhibits release of substance P from sensory neurons in culture and decreases action potential duration. Proc Natl Acad Sci U S A. 1979 Jan;76(1):526–530. doi: 10.1073/pnas.76.1.526. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nicoll R. A., Alger B. E., Jahr C. E. Enkephalin blocks inhibitory pathways in the vertebrate CNS. Nature. 1980 Sep 4;287(5777):22–25. doi: 10.1038/287022a0. [DOI] [PubMed] [Google Scholar]
- Nicoll R. A., Siggins G. R., Ling N., Bloom F. E., Guillemin R. Neuronal actions of endorphins and enkephalins among brain regions: a comparative microiontophoretic study. Proc Natl Acad Sci U S A. 1977 Jun;74(6):2584–2588. doi: 10.1073/pnas.74.6.2584. [DOI] [PMC free article] [PubMed] [Google Scholar]
- North R. A. Opiates, opioid peptides and single neurones. Life Sci. 1979 Apr 23;24(17):1527–1545. doi: 10.1016/0024-3205(79)90014-6. [DOI] [PubMed] [Google Scholar]
- Sar M., Stumpf W. E., Miller R. J., Chang K. J., Cuatrecasas P. Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol. 1978 Nov 1;182(1):17–37. doi: 10.1002/cne.901820103. [DOI] [PubMed] [Google Scholar]
- Schwartzkroin P. A. Further characteristics of hippocampal CA1 cells in vitro. Brain Res. 1977 Jun 3;128(1):53–68. doi: 10.1016/0006-8993(77)90235-9. [DOI] [PubMed] [Google Scholar]
- Schwartzkroin P. A., Prince D. A. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Res. 1978 May 19;147(1):117–130. doi: 10.1016/0006-8993(78)90776-x. [DOI] [PubMed] [Google Scholar]
- Skrede K. K., Westgaard R. H. The transverse hippocampal slice: a well-defined cortical structure maintained in vitro. Brain Res. 1971 Dec 24;35(2):589–593. doi: 10.1016/0006-8993(71)90508-7. [DOI] [PubMed] [Google Scholar]
- Taylor D., Hoffer B., Zieglgänsberger W., Siggins G., Ling N., Seiger A., Olson L. Opioid peptides excite pyramidal neurons and evoke epileptiform activity in hippocampal transplants in oculo. Brain Res. 1979 Oct 26;176(1):135–142. doi: 10.1016/0006-8993(79)90875-8. [DOI] [PubMed] [Google Scholar]
- Yamamoto C. Activation of hippocampal neurons by mossy fiber stimulation in thin brain sections in vitro. Exp Brain Res. 1972;14(4):423–435. doi: 10.1007/BF00235037. [DOI] [PubMed] [Google Scholar]
- Zieglgänsberger W., Bayerl H. The mechanism of inhibition of neuronal activity by opiates in the spinal cord of cat. Brain Res. 1976 Oct 8;115(1):111–128. doi: 10.1016/0006-8993(76)90826-x. [DOI] [PubMed] [Google Scholar]
- Zieglgänsberger W., French E. D., Siggins G. R., Bloom F. E. Opioid peptides may excite hippocampal pyramidal neurons by inhibiting adjacent inhibitory interneurons. Science. 1979 Jul 27;205(4404):415–417. doi: 10.1126/science.451610. [DOI] [PubMed] [Google Scholar]
- Zieglgänsberger W., Tulloch I. F. The effects of methionine- and leucine-enkephalin on spinal neurones of the cat. Brain Res. 1979 May 5;167(1):53–64. doi: 10.1016/0006-8993(79)90262-2. [DOI] [PubMed] [Google Scholar]