Anesthetic agent-specific effects on synaptic inhibition

Anesthesia and Analgesia

Volumn 119, Issue 3, 2014, Pages 558-569

  MacIver, M Bruce ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; ANESTHETIC AGENT; GLUTAMIC ACID; HALOTHANE; ISOFLURANE; PENTOBARBITAL; PROPOFOL; THIOPENTAL;

ANESTHESIA MECHANISM; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; DRUG RECEPTOR BINDING; DRUG SELECTIVITY; DRUG SENSITIVITY; FACILITATION; GABAERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; NERVE CELL INHIBITION; NERVE EXCITABILITY; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; RAT; SYNAPTIC INHIBITION;

ANESTHESIOLOGY; ANESTHETICS; ANIMALS; BARBITURATES; BICUCULLINE; CA1 REGION, HIPPOCAMPAL; DATA INTERPRETATION, STATISTICAL; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; EVOKED POTENTIALS; GABA ANTAGONISTS; KINETICS; MALE; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PHARMACEUTICAL SOLUTIONS; PICROTOXIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPSES;

EID: 84906934533     PISSN: 00032999     EISSN: 15267598     Source Type: Journal    
DOI: 10.1213/ANE.0000000000000321     Document Type: Article

References (46)

1. Nicoll RA, Eccles JC, Oshima T, Rubia F. Prolongation of hippocampal inhibitory postsynaptic potentials by barbiturates. Nature 1975;258:625-7
2. Pearce RA, Stringer JL, Lothman EW. Effect of volatile anesthetics on synaptic transmission in the rat hippocampus. Anesthesiology 1989;71:591-8
3. Tanelian DL, Kosek P, Mody I, MacIver MB. The role of the GABAA receptor/chloride channel complex in anesthesia. Anesthesiology 1993;78:757-76
4. Trudell JR, Bertaccini E, Maciver MB. Teaching an old GABA receptor new tricks. Anesth Analg 2012;115:270-3
5. Maciver MB, Bronte-Stewart HM, Henderson JM, Jaffe RA, Brock-Utne JG. Human subthalamic neuron spiking exhibits subtle responses to sedatives. Anesthesiology 2011;115:254-64
6. Nishikawa K, MacIver MB. Membrane and synaptic actions of halothane on rat hippocampal pyramidal neurons and inhibitory interneurons. J Neurosci 2000;20:5915-23
7. Galarreta M, Hestrin S. Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci U S A 2002;99:12438-43
8. Banke TG, McBain CJ. GABAergic input onto CA3 hippocampal interneurons remains shunting throughout development. J Neurosci 2006;26:11720-5
9. Jurd R, Arras M, Lambert S, Drexler B, Siegwart R, Crestani F, Zaugg M, Vogt KE, Ledermann B, Antkowiak B, Rudolph U. General anesthetic actions in vivo strongly attenuated by a point mutation in the GABA(A) receptor beta3 subunit. FASEB J 2003;17:250-2
10. Zhang Y, Sonner JM, Eger EI 2nd, Stabernack CR, Laster MJ, Raines DE, Harris RA. Gamma-Aminobutyric acidA receptors do not mediate the immobility produced by isoflurane. Anesth Analg 2004;99:85-90
11. Werner DF, Swihart A, Rau V, Jia F, Borghese CM, McCracken ML, Iyer S, Fanselow MS, Oh I, Sonner JM, Eger EI 2nd, Harrison NL, Harris RA, Homanics GE. Inhaled anesthetic responses of recombinant receptors and knockin mice harboring α2(S270H/L277A) GABA(A) receptor subunits that are resistant to isoflurane. J Pharmacol Exp Ther 2011;336:134-44
12. Capogna M, Pearce RA. GABA A, slow: Causes and consequences. Trends Neurosci 2011;34:101-12
13. Mody I, Pearce RA. Diversity of inhibitory neurotransmission through GABA(A) receptors. Trends Neurosci 2004;27:569-75
14. Pearce RA. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 1993;10:189-200
15. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA. Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-Aminobutyric acid(A) receptors in hippocampal neurons. Mol Pharmacol 2001;59:814-24
16. Bieda MC, MacIver MB. Major role for tonic GABAA conductances in anesthetic suppression of intrinsic neuronal excitability. J Neurophysiol 2004;92:1658-67
17. Caraiscos VB, Elliott EM, You-Ten KE, Cheng VY, Belelli D, Newell JG, Jackson MF, Lambert JJ, Rosahl TW, Wafford KA, MacDonald JF, Orser BA. Tonic inhibition in mouse hippocampal CA1 pyramidal neurons is mediated by alpha5 subunitcontaining gamma-Aminobutyric acid type A receptors. Proc Natl Acad Sci U S A 2004;101:3662-7
18. Orser BA. Lifting the fog around anesthesia. Sci Am 2007;296:54-61
19. Dai S, Perouansky M, Pearce RA. Isoflurane enhances both fast and slow synaptic inhibition in the hippocampus at amnestic concentrations. Anesthesiology 2012;116:816-23
20. Hentschke H, Benkwitz C, Banks MI, Perkins MG, Homanics GE, Pearce RA. Altered GABAA,slow inhibition and network oscillations in mice lacking the GABAA receptor beta3 subunit. J Neurophysiol 2009;102:3643-55
21. Wallner M, Hanchar HJ, Olsen RW. Ethanol enhances alpha 4 beta 3 delta and alpha 6 beta 3 delta gamma-Aminobutyric acid type A receptors at low concentrations known to affect humans. Proc Natl Acad Sci U S A 2003;100:15218-23
22. Wei W, Faria LC, Mody I. Low ethanol concentrations selectively augment the tonic inhibition mediated by delta subunit-containing GABAA receptors in hippocampal neurons. J Neurosci 2004;24:8379-82
23. Bieda MC, Su H, Maciver MB. Anesthetics discriminate between tonic and phasic gamma-Aminobutyric acid receptors on hippocampal CA1 neurons. Anesth Analg 2009;108:484-90
24. Winters WD. Effects of drugs on the electrical activity of the brain: Anesthetics. Annu Rev Pharmacol Toxicol 1976;16:413-26
25. 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
26. Mikulec AA, Pittson S, Amagasu SM, Monroe FA, MacIver MB. Halothane depresses action potential conduction in hippocampal axons. Brain Res 1998;796:231-8
27. Hagan CE, Pearce RA, Trudell JR, MacIver MB. Concentration measures of volatile anesthetics in the aqueous phase using calcium sensitive electrodes. J Neurosci Methods 1998;81:177-84
28. Gredell JA, Turnquist PA, Maciver MB, Pearce RA. Determination of diffusion and partition coefficients of propofol in rat brain tissue: Implications for studies of drug action in vitro. Br J Anaesth 2004;93:810-7
29. Chesney MA, Perouansky M, Pearce RA. Differential uptake of volatile agents into brain tissue in vitro. Measurement and application of a diffusion model to determine concentration profiles in brain slices. Anesthesiology 2003;99:122-30
30. Benkwitz C, Liao M, Laster MJ, Sonner JM, Eger EI 2nd, Pearce RA. Determination of the EC50 amnesic concentration of etomidate and its diffusion profile in brain tissue: Implications for in vitro studies. Anesthesiology 2007;106:114-23
31. Eger EI 2nd, Xing Y, Laster M, Sonner J, Antognini JF, Carstens E. Halothane and isoflurane have additive minimum alveolar concentration (MAC) effects in rats. Anesth Analg 2003;96:1350-3
32. Pearce RA. Volatile anaesthetic enhancement of paired-pulse depression investigated in the rat hippocampus in vitro. J Physiol 1996;492 (Pt 3):823-40
33. Pittson S, Himmel AM, MacIver MB. Multiple synaptic and membrane sites of anesthetic action in the CA1 region of rat hippocampal slices. BMC Neurosci 2004;5:52
34. Perouansky M, Baranov D, Salman M, Yaari Y. Effects of halothane on glutamate receptor-mediated excitatory postsynaptic currents. A patch-clamp study in adult mouse hippocampal slices. Anesthesiology 1995;83:109-19
35. MacIver MB, Mikulec AA, Amagasu SM, Monroe FA. Volatile anesthetics depress glutamate transmission via presynaptic actions. Anesthesiology 1996;85:823-34
36. Baudoux S, Empson RM, Richards CD. Pentobarbitone modulates calcium transients in axons and synaptic boutons of hippocampal CA1 neurons. Br J Pharmacol 2003;140:971-9
37. 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
38. Simon W, Hapfelmeier G, Kochs E, Zieglgänsberger W, Rammes G. Isoflurane blocks synaptic plasticity in the mouse hippocampus. Anesthesiology 2001;94:1058-65
39. Perouansky M, Pearce RA. How we recall (or don't): The hippocampal memory machine and anesthetic amnesia. Can J Anaesth 2011;58:157-66
40. Ma J, Shen B, Stewart LS, Herrick IA, Leung LS. The septohippocampal system participates in general anesthesia. J Neurosci 2002;22:RC200
41. Luo T, Leung LS. Involvement of tuberomamillary histaminergic neurons in isoflurane anesthesia. Anesthesiology 2011;115:36-43
42. Schlame M, Hemmings Jr. H.C. Inhibition by volatile anesthetics of endogenous glutamate release from synaptosomes by a presynaptic mechanism. Anesthesiology 1995;82:1406-16
43. Sonner JM, Zhang Y, Stabernack C, Abaigar W, Xing Y, Laster MJ. GABA(A) receptor blockade antagonizes the immobilizing action of propofol but not ketamine or isoflurane in a doserelated manner. Anesth Analg 2003;96:706-12
44. Richards CD. The action of anaesthetics on synaptic transmission. Gen Pharmacol 1978;9:287-93
45. Banks MI, Pearce RA. Kinetic differences between synaptic and extrasynaptic GABA(A) receptors in CA1 pyramidal cells. J Neurosci 2000;20:937-48
46. Lukatch HS, MacIver MB. Voltage-clamp analysis of halothane effects on GABA(A fast) and GABA(A slow) inhibitory currents. Brain Res 1997;765:108-12.