Ketamine, but not phencyclidine, selectively modulates cerebellar GABA A receptors containing α6 and δ subunits

Journal of Neuroscience

Volumn 28, Issue 20, 2008, Pages 5383-5393

  Hevers, Wulf ^a,c   Hadley, Stephen H ^b   Lüddens, Hartmut ^a   Amin, Jahanshah ^b  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

6 2 3 GABAA receptors; Cerebellum; Granule neurons; Ketamine; Slice recording; Tonic conductance; Transgenic mice

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ALPHA ADRENERGIC RECEPTOR; DELTA OPIATE RECEPTOR; DIZOCILPINE; KETAMINE; PHENCYCLIDINE; PROTEIN SUBUNIT; RECOMBINANT RECEPTOR; ALPHA6 SUBUNIT, GABA A RECEPTOR; ALPHA6 SUBUNIT, GABA-A RECEPTOR; AMINO ACID RECEPTOR BLOCKING AGENT; ANESTHETIC AGENT; DELTA SUBUNIT, GABA A RECEPTOR; DELTA SUBUNIT, GABA-A RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION SYSTEM; GRANULE CELL; MALE; MOUSE; NERVE CELL; NERVE CONDUCTION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; RECEPTOR SENSITIVITY; TRANSGENIC MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MEMBRANE POTENTIAL; CEREBELLUM CORTEX; DOSE RESPONSE; DRUG EFFECT; FEMALE; GENETICS; METABOLISM; MOUSE MUTANT; NERVE CELL INHIBITION; ORGAN CULTURE TECHNIQUE; PATCH CLAMP; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT; SYNAPTIC TRANSMISSION; XENOPUS LAEVIS;

ANESTHETICS, DISSOCIATIVE; ANIMALS; CELLS, CULTURED; CEREBELLAR CORTEX; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; KETAMINE; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURAL INHIBITION; NEURONS; OOCYTES; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PHENCYCLIDINE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION; XENOPUS LAEVIS;

EID: 45549096136     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5443-07.2008     Document Type: Article

References (80)

1. Anis NA, Berry SC, Burton NR, Lodge D (1983) The dissociative anaesthetics, ketamine and phencyclidine, selectively reduce excitation of central mammalian neurones by N-methylaspartate. Br J Pharmacol 79:565-575.
2. Arenz A, Margrie R, Silver R (2006) The effects of barbiturate and ketamine anesthesia on excitatory synaptic transmission at the mossy fiber-granule cell synapse in the cerebellum. Soc Neurosci Abstr 32:795.4/D19.
3. Bellebaum C, Daum I (2007) Cerebellar involvement in executive control. Cerebellum 6:184-192.
4. Bengtsson F, Jorntell H (2007) Ketamine and xylazine depress sensory-evoked parallel fiber and climbing fiber responses. J Neurophysiol 98:1697-1705.
5. Bennett DA, Bernard PS, Amrick CL (1988) A comparison of PCP-like compounds for NMDA antagonism in two in vivo models. Life Sci 42:447-454.
6. Brau ME, Sander F, Vogel W, Hempelmann G (1997) Blocking mechanisms of ketamine and its enantiomers in enzymatically demyelinated peripheral nerve as revealed by single-channel experiments. Anesthesiology 86:394-404.
7. Brickley SG, Cull-Candy SG, Farrant M (1996) Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol (Lond) 497:753-759.
8. Chen G (1965) Evaluation of phencyclidine-type cataleptic activity. Arch Int Pharmacodyn Ther 157:193-201.
9. Chen G, Ensor CR, Russell D, Bohner B (1959) The pharmacology of 1-(1-phenylcyclohexyl) piperidine-HCl. J Pharmacol Exp Ther 127:241-250.
10. Cohen ML, Trevor AJ (1974) Onthe cerebral accumulation of ketamine and the relationship between metabolism of the drug and its pharmacological effects. J Pharmacol Exp Ther 189:351-358.
11. Collins VJ, Gorospe CA, Rovenstine EA (1960) Intravenous nonbarbiturate, nonnarcotic analgesics: preliminary studies. 1. Cyclohexylamines. Anesth Analg 39:302-306.
12. Corssen G, Domino EF (1966) Dissociative anesthesia: further pharmacologic studies and first clinical experience with the phencyclidine derivative CI-581. Anesth Analg 45:29-40.
13. Domino EF, Chodoff P, Corssen G (1965) Pharmacologic effects of Ci-581, a new dissociative anesthetic, in man. Clin Pharmacol Ther 6:279-291.
14. Dravid SM, Erreger K, Yuan H, Nicholson K, Le P, Lyuboslavsky P, Almonte A, Murray E, Mosely C, Barber J, French A, Balster R, Murray TF, Traynelis SF (2007) Subunit-specific mechanisms and proton sensitivity of NMDA receptor channel block. J Physiol (Lond) 581:107-128.
15. ffrench-Mullen JM, Rogawski MA (1989) Interaction of phencyclidine with voltage-dependent potassium channels in cultured rat hippocampal neurons: comparison with block of the NMDA receptor-ionophore complex. J Neurosci 9:4051-4061.
16. Finck AD, Ngai SH (1982) Opiate receptor mediation of ketamine analgesia. Anesthesiology 56:291-297.
17. Flood P, Krasowski MD (2000) Intravenous anesthetics differentially modulate ligand-gated ion channels. Anesthesiology 92:1418-1425.
18. Franks NP, Lieb WR (1994) Molecular and cellular mechanisms of general anaesthesia. Nature 367:607-614.
19. Furuya R, Oka K, Watanabe I, Kamiya Y, Itoh H, Andoh T (1999) The effects of ketamine and propofol on neuronal nicotinic acetylcholine receptors and P2x purinoceptors in PC12 cells. Anesth Analg 88:174-180.
20. Gage PW, Robertson B (1985) Prolongation of inhibitory postsynaptic currents by pentobarbitone, halothane and ketamine in CA1 pyramidal cells in rat hippocampus. Br J Pharmacol 85:675-681.
21. Garthwaite J, Brodbelt AR (1990) Glutamate as the principal mossy fibre transmitter in rat cerebellum: pharmacological evidence. Eur J Neurosci 2:177-180.
22. Greifenstein FE, Devault M, Yoshitake J, Gajewski JE (1958) A study of a 1-aryl cyclo hexyl amine for anesthesia. Anesth Analg 37:283-294.
23. Haarmeier T, Thier P (2007) The attentive cerebellum - myth or reality? Cerebellum 6:177-183.
24. A receptors exhibit two distinct and separable agonist affinities. J Physiol (Lond) 581:1001-1018.
25. Halliwell RF, Peters JA, Lambert JJ (1989) The mechanism of action and pharmacological specificity of the anticonvulsant NMDA antagonist MK-801: a voltage clamp study on neuronal cells in culture. Br J Pharmacol 96:480-494.
26. Hamann M, Rossi DJ, Attwell D (2002) Tonic and spillover inhibition of granule cells control information flow through cerebellar cortex. Neuron 33:625-633.
27. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85-100.
28. Hevers W, Luddens H (2002) Pharmacological heterogeneity of gamma-aminobutyric acid receptors during development suggests distinct classes of rat cerebellar granule cells in situ. Neuropharmacology 42:34-47.
29. Hirota K, Lambert DG (1996) Ketamine: its mechanism(s) of action and unusual clinical uses. Br J Anaesth 77:441-444.
30. Huettner JE, Bean BP (1988) Block of N-methyl-D- aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc Natl Acad Sci USA 85:1307-1311.
31. Hustveit O, Maurset A, Oye I (1995) Interaction of the chiral forms of ketamine with opioid, phencyclidine, sigma and muscarinic receptors. Pharmacol Toxicol 77:355-359.
32. Irifune M, Shimizu T, Nomoto M, Fukuda T (1992) Ketamine-induced anesthesia involves the N-methyl-D-aspartate receptor-channel complex in mice. Brain Res 596:1-9.
33. A receptor agonistic properties of ketamine: convulsive and anesthetic behavioral models in mice. Anesth Analg 91:230-236.
34. Irifune M, Katayama S, Takarada T, Shimizu Y, Endo C, Takata T, Morita K, Dohi T, Sato T, Kawahara M (2007) MK-801 enhances gabaculine-induced loss of the righting reflex in mice, but not immobility. Can J Anaesth 54:998-1005.
35. Johnstone M, Evans V, Baigel S (1959) Sernyl (CI-395) in clinical anaesthesia. Br J Anaesth 31:433-439.
36. A receptor alpha6 subunit gene inactivation inhibits delta subunit expression. J Neurosci 17:1350-1362.
37. Kaneda M, Farrant M, Cull-Candy SG (1995) Whole-cell and single-channel currents activated by GABA and glycine in granule cells of the rat cerebellum. J Physiol (Lond) 485:419-435.
38. Kelland MD, Soltis RP, Boldry RC, Walters JR (1993) Behavioral and electrophysiological comparison of ketamine with dizocilpine in the rat. Physiol Behav 54:547-554.
39. Klepstad P, Maurset A, Moberg ER, Oye I (1990) Evidence of a role for NMDA receptors in pain perception. Eur J Pharmacol 187:513-518.
40. Koek W, Woods JH, Jacobson AE, Rice KC (1987a) Phencyclidine (PCP)-like discriminative stimulus effects of metaphit and of 2-amino-5-phosphonovalerate in pigeons: generality across different training doses of PCP. Psychopharmacology (Berl) 93:437-442.
41. Koek W, Woods JH, Mattson MV, Jacobson AE, Mudar PJ (1987b) Excitatory amino acid antagonists induce a phencyclidine-like catalepsy in pigeons: structure-activity studies. Neuropharmacology 26:1261-1265.
42. Koek W, Woods JH, Winger GD (1988) MK-801, a proposed noncompetitive antagonist of excitatory amino acid neurotransmission, produces phencyclidine-like behavioral effects in pigeons, rats and rhesus monkeys. J Pharmacol Exp Ther 245:969-974.
43. A receptors. Br J Pharmacol 120:741-748.
44. Korpi ER, Kuner T, Seeburg PH, Luddens H (1995) Selective antagonist for the cerebellar granule cell-specific gamma-aminobutyric acid type A receptor. Mol Pharmacol 47:283-289.
45. Kress HG (1997) [Mechanisms of action of ketamine]. Anaesthesist 46 [Suppl 1]:S8-S19.
46. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development. J Neurosci 12:4151-4172.
47. Lin LH, Chen LL, Zirrolli JA, Harris RA (1992) General anesthetics potentiate gamma-aminobutyric acid actions on gamma-aminobutyric acidA receptors expressed by Xenopus oocytes: lack of involvement of intracellular calcium. J Pharmacol Exp Ther 263:569-578.
48. Lodge D, Anis NA (1982) Effects of phencyclidine on excitatory amino acid activation of spinal interneurones in the cat. Eur J Pharmacol 77:203-204.
49. MacDonald JF, Nowak LM (1990) Mechanisms of blockade of excitatory amino acid receptor channels. Trends Pharmacol Sci 11:167-172.
50. MacDonald JF, Miljkovic Z, Pennefather P (1987) Use-dependent block of excitatory amino acid currents in cultured neurons by ketamine. J Neurophysiol 58:251-266.
51. MacDonald JF, Bartlett MC, Mody I, Pahapill P, Reynolds JN, Salter MW, Schneiderman JH, Pennefather PS (1991) Actions of ketamine, phencyclidine and MK-801 on NMDA receptor currents in cultured mouse hippocampal neurones. J Physiol (Lond) 432:483-508.
52. A receptor channels. Annu Rev Neurosci 17:569-602.
53. Martin P, Albers M (1995) Cerebellum and schizophrenia: a selective review. Schizophr Bull 21:241-250.
54. McCarthy DA, Chen G, Kaump DH, Ensor C (1965) General anesthetic and other pharmacological properties of 2-(O-chlorophenyl)-2-methylamino cyclohexanone HCl (Ci-58l). J New Drugs 28:21-33.
55. A receptor alpha 6 subunit gene. J Neurosci 18:2822-2833.
56. Mihalek RM, Banerjee PK, Korpi ER, Quinlan JJ, Firestone LL, Mi ZP, Lagenaur C, Tretter V, Sieghart W, Anagnostaras SG, Sage JR, Fanselow MS, Guidotti A, Spigelman I, Li Z, DeLorey TM, Olsen RW, Homanics GE (1999) Attenuated sensitivity to neuroactive steroids in gamma-aminobutyrate type A receptor delta subunit knockout mice. Proc Natl Acad Sci USA 96:12905-12910.
57. Morris KD, Moorefield CN, Amin J (1999) Differential modulation of the gamma-aminobutyric acid type C receptor by neuroactive steroids. Mol Pharmacol 56:752-759.
58. Oye I, Paulsen O, Maurset A (1992) Effects of ketamine on sensory perception: evidence for a role of N-methyl-D-aspartate receptors. J Pharmacol Exp Ther 260:1209-1213.
59. Ramoa AS, Alkondon M, Aracava Y, Irons J, Lunt GG, Deshpande SS, Wonnacott S, Aronstam RS, Albuquerque EX (1990) The anticonvulsant MK-801 interacts with peripheral and central nicotinic acetylcholine receptor ion channels. J Pharmacol Exp Ther 254:71-82.
60. Rogawski MA, Wenk GL (2003) The neuropharmacological basis for the use of memantine in the treatment of Alzheimer's disease. CNS Drug Rev 9:275-308.
61. Rossi P, D'Angelo E, Magistretti J, Toselli M, Taglietti V (1994) Age-dependent expression of high-voltage activated calcium currents during cerebellar granule cell development in situ. Pflügers Arch 429:107-116.
62. Saarelainen KS, Ranna M, Rabe H, Sinkkonen ST, Möykkynen T, Uusi-Oukari M, Linden AM, Lüddens H, Korpi ER (2008) Enhanced behavioral sensitivity to the competitive GABA agonist, gaboxadol, in transgenic mice over-expressing hippocampal extrasynaptic alpha6beta GABA(A) receptors. J Neurochem 105:338-350.
63. Saxena NC, Macdonald RL (1996) Properties of putative cerebellar gamma-aminobutyric acid A receptor isoforms. Mol Pharmacol 49:567-579.
64. Scheller M, Bufler J, Hertle I, Schneck HJ, Franke C, Kochs E (1996) Ketamine blocks currents through mammalian nicotinic acetylcholine receptor channels by interaction with both the open and the closed state. Anesth Analg 83:830-836.
65. Schnoebel R, Wolff M, Peters SC, Brau ME, Scholz A, Hempelmann G, Olschewski H, Olschewski A (2005) Ketamine impairs excitability in superficial dorsal horn neurones by blocking sodium and voltage-gated potassium currents. Br J Pharmacol 146:826-833.
66. Scholfield CN (1980) Potentiation of inhibition by general anaesthetics in neurones of the olfactory cortex in vitro. Pflügers Arch 383:249-255.
67. Schonewille M, Khosrovani S, Winkelman BH, Hoebeek FE, De Jeu MT, Larsen IM, Van der Burg J, Schmolesky MT, Frens MA, De Zeeuw CI (2006) Purkinje cells in awake behaving animals operate at the upstate membrane potential. Nat Neurosci 9:459-461.
68. A receptors: functional selectivity for extrasynaptic receptors is dependent on the absence of gamma2. J Pharmacol Exp Ther 316:1351-1359.
69. Sultan F, Glickstein M (2007) The cerebellum: comparative and animal studies. Cerebellum 6:168-176.
70. Thach WT (2007) On the mechanism of cerebellar contributions to cognition. Cerebellum 6:163-167.
71. A receptor alpha 6 subunit. J Neurosci 16:3630-3640.
72. Timmann D, Daum I (2007) Cerebellar contributions to cognitive functions: a progress report after two decades of research. Cerebellum 6:159-162.
73. Tricklebank MD, Singh L, Oles RJ, Wong EH, Iversen SD (1987) A role for receptors of N-methyl-D-aspartic acid in the discriminative stimulus properties of phencyclidine. Eur J Pharmacol 141:497-501.
74. Tyrrell T, Willshaw D (1992) Cerebellar cortex: its simulation and the relevance of Marr's theory. Philos Trans R Soc Lond B Biol Sci 336:239-257.
75. Wakasugi M, Hirota K, Roth SH, Ito Y (1999) The effects of general anesthetics on excitatory and inhibitory synaptic transmission in area CA1 of the rat hippocampus in vitro. Anesth Analg 88:676-680.
76. Wall MJ, Usowicz MM (1997) Development of action potential-dependent and independent spontaneous GABAA receptor-mediated currents in granule cells of postnatal rat cerebellum. Eur J Neurosci 9:533-548.
77. A receptors via two distinct and separable mechanisms. Nat Neurosci 3:1274-1281.
78. A receptor diversity. Neuropharmacology 35:1139-1160.
79. Wong EH, Kemp JA, Priestley T, Knight AR, Woodruff GN, Iversen LL (1986) The anticonvulsant MK-801 is a potent N-methyl-D-aspartate antagonist. Proc Natl Acad Sci USA 83:7104-7108.
80. Yamakura T, Chavez-Noriega LE, Harris RA (2000) Subunit-dependent inhibition of human neuronal nicotinic acetylcholine receptors and other ligand-gated ion channels by dissociative anesthetics ketamine and dizocilpine. Anesthesiology 92:1144-1153.