Volatile anesthetics depress glutamate transmission via presynaptic actions

Anesthesiology

Volumn 85, Issue 4, 1996, Pages 823-834

  MacIver, M Bruce ^b,c   Mikulec, Anthony A ^b   Amagasu, Shanti M ^a   Monroe, Frances A ^b  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Stanford Biological Sciences ^*  (United States)

Author keywords

Anesthetics, volatile: halothane; isoflurane; Brain: CA1 neuron; hippocampal slices; synapses; synaptic transmission; Measurements techniques, electrophysiologic recordings: EPSP facilitation; Neurotransmitters, glutamate: release; GABA

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; INHALATION ANESTHETIC AGENT;

4 AMINOBUTYRIC ACID UPTAKE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; EXCITATORY POSTSYNAPTIC POTENTIAL; NEUROTRANSMISSION; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; RECEPTOR BINDING; SYNAPTIC TRANSMISSION;

ANESTHETICS, INHALATION; ANIMALS; CALCIUM; DEPRESSION, CHEMICAL; ELECTROPHYSIOLOGY; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HALOTHANE; HIPPOCAMPUS; ION TRANSPORT; ISOFLURANE; MALE; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; TEMPERATURE;

EID: 0029859633     PISSN: 00033022     EISSN: None     Source Type: Journal    
DOI: 10.1097/00000542-199610000-00018     Document Type: Article

References (54)

1. A receptor/chloride channel complex in anesthesia. ANESTHESIOLOGY 1993; 78:757-76
2. A receptor channels. Annu Rev Neurosci 1994; 17:569-602
3. Kendig JJ, MacIver MB, Roth SH: Anesthetic actions in the hippocampal formation. Ann N Y Acad Sci 1991; 625:37-53
4. Perouansky M, Baranov D, Salman M, Yaari Y: Effects of halothane on glutamate receptor-mediated excitatory postsynaptic currents. ANESTHESIOLOGY 1995; 83:109-19
5. A-mediated neuronal inhibition. Ann N Y Acad Sci 1991; 625:91-6
6. A receptor Cl- current correlates with in vivo anesthetic potency. J Pharmacol Exp Ther 1994; 270:987-91
7. Quastel DMJ, Hackett JT, Okamoto K: Presynaptic action of central depressant drugs: Inhibition of depolarization-secretion coupling. Can J Physiol Pharmacol 1972; 50:279-87
8. Weakly JN: Effect of barbiturates on 'quantal' synaptic transmission in spinal motoneurones. J Physiol 1969; 204:63-77
9. Collins GGS: Release of endogenous amino acid neurotransmitter candidates from rat olfactory cortex: Possible regulatory mechanisms and the effects of pentobarbitone. Brain Res 1980; 190:517-25
10. Bianchi M, Battistin T, Galzigna L: 2,6-diisopropylphenol, a general anesthetic, inhibits glutamate action on rat synaptosomes. Neurochem Res 1991; 16:443-6
11. Potashner SJ, Lake N, Langlois EA, Ploffe L, Lecavalier D: Pentobarbital: Differential effects on amino acid transmitter release, Molecular Mechanisms of Anesthesia (Progress in Anesthesiology). Edited by Fink BR. New York, Raven, 1980, pp 469-82
12. Kendall TJ, Minchin MC: The effects of anaesthetics on the uptake and release of amino acid neurotransmitters in thalamic slices. Br J Pharmacol 1982; 75:219-27
13. Suria A, Rasheed F: Evidence for involvement of amino acid neurotransmitters in anesthesia and naloxone induced reversal of respiratory paralysis. Life Sci 1994; 54:2021-33
14. Dingledine R, Somjen G: Calcium dependence of synaptic transmission in the hippocampal slice. Brain Res 1981; 207:218-22
15. Leung LS, Fu XW: Factors affecting paired-pulse facilitation in hippocampal CA1 neurons in vitro. Brain Res 1994; 650:75-84
16. Lupica CR, Proctor WR, Dunwiddie TV: Presynaptic inhibition of excitatory synaptic transmission by adenosine in rat hippocampus: Analysis of unitary EPSP variance measured by whole-cell recording. J Neurosci 1992; 12:3753-64
17. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA. Modulation of synaptic transmission and long-term potentiation: Effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol 1993; 70:1451-9
18. Manabe T, Nicoll RA: Long-term potentiation: Evidence against an increase in transmitter release probability in the CA1 region of the hippocampus. Science 1994; 265:1888-92
19. Study RE: Isoflurane inhibits multiple voltage-gated calcium currents in hippocampal pyramidal neurons. ANESTHESIOLOGY 1994; 81:104-16
20. Jones M, Brooks P, Harrison N: Enhancement of gamma-aminobutyric acid-activated chloride currents in cultured rat hippocampal neurones by three volatile anaesthetics. J Physiol (Lond) 1992; 449:279-93
21. Leung L-WS: Differential effects of pentobarbital and ether on the synaptic transmission of the hippocampal CA 1 region in the rat. Electroenceph Clin Neurophysiol 1981; 51:291-305
22. Pearce RA, Stringer JL, Lothman EW: Effect of volatile anesthetics on synaptic transmission in the rat hippocampus. ANESTHESIOLOGY 1989; 71:591-8
23. Richards CD, White AE: The actions of volatile anaesthetics on synaptic transmission in the dentate gyms. J Physiol (Lond) 1975; 252:241-57
24. Langmoen IA, Larsen M, Berg-Johnsen J: Volatile anaesthetics: Cellular mechanisms of action. Eur J Anaesthesiol 1995; 12:51-8
25. Larsen M, Grondahl TO, Haugstad TS, Langmoen IA: The effect of the volatile anesthetic isoflurane on Ca(2+)-dependent glutamate release from rat cerebral cortex. Brain Res 1994; 663:335-7
26. Weight FF, Aguayo LG, White G, Lovinger DM, Peoples RW: GABA-and glutamate-gated ion channels as molecular sites of alcohol and anesthetic action. Adv Biochem Psychopharmacol 1992; 47:335 -47
27. Martin DC, Plagenhoef M, Abraham J, Dennison RL, Aronstam RS: Volatile anesthetics and glutamate activation of N-rnethyl-D-aspartate receptors. Biochem Pharmacol 1995; 49:809-17
28. Hirose T, Inoue M, Uchida M, Inagaki C: Enflurane-induced release of an excitatory amino acid, glutamate, from mouse brain synaptosomes. ANESTHESIOLOGY 1992; 77:109-13
29. Schlame M, Hemmings HC: Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by a presynaptic mechanism. ANESTHESIOLOGY 1995; 82:1406-16
30. MacIver MB, Roth SH: Inhalation anaesthetics exhibit pathway-specific and differential actions on hippocampal synaptic responses in vitro. Br J Anaesth 1988; 60:680-91
31. MacIver MB, Tauck DL, Kendig JJ: General anaesthetic modification of synaptic facilitation and long-term potentiation in hippocampus. Br J Anaesth 1989; 62:301-10
32. MacIver MB, Kendig JJ: Enflurane-induced burst discharge of hippocampal CA1 neurones is blocked by the NMDA receptor antagonist APV. Br J Anaesth 1989; 63:296-305
33. MacIver MB, Roth SH: Barbiturate effects on hippocampal excitatory synaptic responses are selective and pathway specific. Can J Physiol Pharmacol 1987; 65:385-94
34. MacIver MB, Roth SH: Enflurane-induced burst firing of hippocampal CA 1 neurones. In vitro studies using a brain slice preparation. Br J Anaesth 1987; 59:369-78
35. Doze VA, Cohen GA, Madison DV: Synaptic localization of adrenergic disinhibition in the rat hippocampus. Neuron 1991; 6:889-900
36. Mody I, Tanelian DL, MacIver MB: Halothane enhances tonic neuronal inhibition by elevating intracellular calcium. Brain Res 1991; 538:319-23
37. Cohen GA, Doze VA, Madison DV: Opioid inhibition of GABA release from presynaptic terminals of rat hippocampal interneurons. Neuron 1992; 9:325-35
38. Berg-Johnsen J, Langmoen IA: The effect of isoflurane on excitatory synaptic transmission in the rat hippocampus. Acta Anaesthesiol Scand 1992; 36:350-5
39. 2+ transients and glutamate release in isolated cerebral synaptosomes. ANESTHESIOLOGY 1995; 83:593-603
40. Schiff SJ, Somjen GG: The effects of temperature on synaptic transmission in hippocampal tissue slices. Brain Res 1985; 345:279-84
41. Shen KF, Schwartzkroin PA: Effects of temperature alterations on population and cellular activities in hippocampal slices from mature and immature rabbit. Brain Res 1988; 475:305-16
42. Moser EI, Andersen P: Conserved spatial learning in cooled rats in spite of slowing of dentate field potentials. J Neurosci 1994; 14:4458-66
43. Cain DP, Hargreaves EL, Boon F: Brain temperature- and behavior-related changes in the dentate gyrus field potential during sleep, cold water immersion, radiant heating, and urethane anesthesia. Brain Res 1994; 658:135-44
44. Behan-Martin MK, Jones GR, Bowler K, Cossins AR: A near perfect temperature adaptation of bilayer order in vertebrate brain membranes. Biochim Biophys Acta 1993; 1151:216-22
45. Hazel JR: Thermal adaptation in biological membranes: Is homeoviscous adaptation the explanation? Annu Rev Physiol 1995; 57:19-42
46. Krelstein MS, Thomas MP, Horowitz JM: Thermal effects on long-term potentiation in the hamster hippocampus. Brain Res 1990; 520:115-22
47. Mihalovic LT: Cortical and subcortical electrical activity in hibernation and hypothermia, Hibernation and Hypothermia, Perspectives and Challenges. Edited by South FE, Hannon JP, Willis JR, Pengelley ET, Alpert NR. Amsterdam, Elsevier, 1972, pp 487-534
48. Daniell LC: Effect of volatile general anesthetics and n-alcohols on glutamate-stimulated increases in calcium ion flux in hippocampal membrane vesicles. Pharmacology 1995; 50:154-61
49. Hestrin S, Sah P, Nicoll RA: Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices. Neuron 1990; 5:247-53
50. Mikulec AA, Amagasu SM, Monroe FA, MacIver MB: Three sites of action are necessary and sufficient for halothane-induced depression of hippocampal CA1 neurons (abstract). ANESTHESIOLOGY 1995; 83:A1266
51. Benno R, Xiao Y-H, Duch DS: Central nervous system sodium channels are significantly suppressed at clinical concentrations of volatile anesthetics. ANESTHESIOLOGY 1996; 84:1123-33
52. Scheller RH: Membrane trafficking in the presynaptic nerve terminal. Neuron 1995; 893-97
53. O'Connor VM, Shamotienko O, Grishin E, Betz H: On the structure of the 'synaptosecretosome'. Evidence for a neurexin/synaptotagmin/symaxin/Ca2+ channel complex. FEBS Lett 1993; 326:255-60
54. Sheng ZH, Rettig J, Takahashi M, Catterall WA: Identification of a syntaxin-binding site on N-type calcium channels. Neuron 1994; 13:1303-13