Behavioral effects of diazepam in the murine plus-maze: Flumazenil antagonism of enhanced head dipping but not the disinhibition of open-arm avoidance

Pharmacology Biochemistry and Behavior

Volumn 62, Issue 4, 1999, Pages 727-734

  Dalvi, A ^a   Rodgers, R J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Animal models; Anxiety; Benzodiazepines; Diazepam; Flumazenil; Mice; Plus maze

Indexed keywords

BENZODIAZEPINE RECEPTOR; DIAZEPAM; FLUMAZENIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG ANTAGONISM; INTRAPERITONEAL DRUG ADMINISTRATION; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANQUILIZING ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; DIAZEPAM; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FLUMAZENIL; GABA MODULATORS; GROOMING; MALE; MICE; MICE, INBRED DBA; MOTOR ACTIVITY;

ANIMALIA; MURINAE;

EID: 0033056501     PISSN: 00913057     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0091-3057(98)00220-2     Document Type: Article

References (95)

1. Ansseau M., von Frenckell R., Cerfontaine J.L., Papart P. Pilot study of PK 11195, a selective ligand for the peripheral-type benzodiazepine binding sites, in inpatients with anxious or depressive symptomology. Pharmacopsychiatry. 24:1991;8-12.
2. Assie M.-B., Chopin P., Stenger A. Neuropharmacology of a new potential anxiolytic compound, F-2692, 1-(3′-trifluoromethyl phenyl) 1,4-dihydro 3-amino 4-oxo 6 methyl pyrdiazine. I. Acute and in vitro effects. Psychopharmacology (Berlin). 110:1993;13-18.
3. A receptors, exhibits low tolerance and dependence liabilities in the rat. J. Pharmacol. Exp. Ther. 270:1994;1262-1269.
4. Belzung C., Misslin R., Vogel E., Dodd R.H., Chapoutier G. Anxiogenic effects of methyl-β-carboline-3 carboxylate in a light/dark choice situation. Pharmacol. Biochem. Behav. 29:1987;29-33.
5. Benjamin D., Lal H., Meyerson L.R. The effects of 5-HT(1B) characterizing agents in the mouse elevated plus-maze. Life Sci. 47:1990;195-203.
6. Berg W.K., Davis M. Diazepam blocks fear-enhanced startle elicited electrically from the brainstem. Physiol. Behav. 32:1984;333-336.
7. Bold J.M., Gardner C.R., Walker R.J. Central effects of nicotinamide and inosine which are not mediated through benzodiazepine receptors. Br. J. Pharmacol. 84:1985;689-696.
8. Bonetti E.P., Pieri L., Cumin R., Schaffner R., Pieri M., Gamzu E.R., Müller K.M., Haefely W. Benzodiazepine antagonist Ro 15-1788. Neurological and behavioral effects Psychopharmacology (Berlin). 78:1982;8-18.
9. A receptor subtypes. From pharmacology to molecular biology FASEB J. 5:1991;2916-2923.
10. 4 receptor and anxiety. Behavioural profiles of clozapine, L-745,870 and L-741,742 in the mouse plus-maze Eur. J. Pharmacol. 335:1997;117-125.
11. 1A receptor antagonism on plus-maze behaviour in mice. I. Pindolol enantiomers and pindobind. 5-HT1A.(Pharmacol. Biochem. Behav. 58):1997;583-591.
12. 1A receptor antagonism on plus-maze behaviour in mice. II. WAY 100635, SDZ 216-525 and NAN-190. Pharmacol. Biochem. Behav. 58:1997;593-603.
13. Chojnacka-Wojcik E., Tatarczynska E., Wiczynska B., Lewandowska A., Przegalinski E. The pharmacological profile of chlordesmethyldiazepam and other benzodiazepines. Pol. J. Pharmacol. Pharm. 38:1986;207-213.
14. Chopin P., Briley M. The benzodiazepine antagonist, flumazenil blocks the effects of CCK receptor agonists and antagonists in the elevated plus-maze. Psychopharmacology (Berlin). 110:1993;409-414.
15. Cole J.C., Rodgers R.J. An ethological analysis of the effects of chlordiazepoxide and bretazenil (Ro 16-6028) in the murine elevated plus-maze. Behav. Pharmacol. 4:1993;573-580.
16. Cole J.C., Rodgers R.J. Ethological comparison of the effects of diazepam and acute/chronic imipramine on the behaviour of mice in the elevated plus-maze. Pharmacol. Biochem. Behav. 52:1995;473-478.
17. Corbett R., Fielding S., Cornfelt M., Dunn R.W. GABAmimetic agents display anxiolytic-like effects in the social interaction and elevated plus-maze procedures. Psychopharmacology (Berlin). 104:1991;312-316.
18. Corda M.G., Blaker W.D., Mendelson W.B., Guidotti A., Costa E. β-Carbolines enhance shock-induced suppression of drinking in rats. Proc. Natl. Acad. Sci. USA. 80:1983;2072-2076.
19. Crawley J.N., Skolnick P., Paul S.M. Absence of intrinsic antagonist actions of benzodiazepine antagonists on an exploratory model of anxiety in the mouse. Neuropharmacology. 23:1984;531-537.
20. Cruz A.P.M., Frei F., Graeff F.G. Ethopharmacological analysis of behavior on the elevated plus-maze. Pharmacol. Biochem. Behav. 49:1994;171-176.
21. Curran H.V., Birch B. Differentiating the sedative, psychomotor and amnesic effects of benzodiazepines. A study with midazolam and the benzodiazepine antagonist, flumazenil Psychopharmacology (Berlin). 103:1991;519-523.
22. Dalvi A., Rodgers R.J. GABAergic influences on plus-maze behaviour in mice. Psychopharmacology (Berlin). 128:1996;380-397.
23. Darragh A., Lambe R., O'Boyle C., Kenny M., Brick I. Absence of central effects in man of the benzodiazepine antagonist Ro 15-1788. Psychopharmacology (Berlin). 80:1983;192-195.
24. de Angelis L., File S.E. Acute and chronic effects of three benzodiazepines in the social interaction anxiety test in mice. Psychopharmacologia. 64:1979;127-129.
25. B receptor antagonist CI-988 and diazepam in the four-plate test. Psychopharmacology (Berlin). 112:1993;452-454.
26. Duka T., Ackenheil M., Noderer J., Doenicke A., Dorow R. Changes in noradrenaline plasma levels and behavioural responses induced by benzodiazepine agonists with the benzodiazepine antagonist Ro 15-1788. Psychopharmacology (Berlin). 90:1986;351-357.
27. Espejo E.F. Structure of mouse behavior on the elevated plus-maze test of anxiety. Behav. Brain Res. 86:1997;105-112.
28. Fernandes C., File S.E. The influence of open arm ledges and maze experience in the elevated plus-maze. Pharmacol. Biochem. Behav. 54:1996;31-40.
29. Fernández-Guasti A., Picazo O. Flumazenil blocks the anxiolytic action of allopregnanolone. Eur. J. Pharmacol. 281:1995;113-115.
30. File S.E. Behavioural detection of anxiolytic action. Elliot J.M., Heal D.J., Marsden C.A. Experimental approaches to anxiety and depression. 1992;25-44 Wiley, Chichester.
31. File S.E., Baldwin H.A. Effects of β-carbolines in animal models of anxiety. Brain Res. Bull. 19:1987;293-299.
32. File S.E., Hitchcott P.K. A theory of benzodiazepine dependence that can explain whether flumazenil will enhance or reverse the phenomenon. Psychopharmacology (Berlin). 101:1990;525-532.
33. File S.E., Lister R.G. The anxiogenic action of Ro 5-4864 is reversed by phenytoin. Neurosci. Lett. 35:1983;93-96.
34. File S.E., Lister R.G., Nutt D.J. Intrinsic actions of benzodiazepine antagonists. Neurosci. Lett. 32:1982;165-168.
35. File S.E., Pellow S. The anxiogenic action of FG-7142 in the social interaction test is reversed by chlordiazepoxide and Ro 15-1788 but not by CGS 8216. Arch. Int. Pharmacodyn. Ther. 271:1984;198-205.
36. File S.E., Pellow S. The anxiogenic action of Ro 5-4864 in the social interaction test - Effect of chlordiazepoxide, Ro 15-1788 and CGS 8216. Naunyn Schmiedebergs Arch. Pharmacol. 328:1985;225-228.
37. File S.E., Pellow S. The effects of PK 11195, a ligand for benzodiazepine binding sites, in animal tests of anxiety and stress. Pharmacol. Biochem. Behav. 23:1985;737-741.
38. Gardner C.R., Budhram P. Effects of agents which interact with central benzodiazepine binding sites on stress-induced ultrasounds in rat pups. Eur. J. Pharmacol. 134:1987;275-283.
39. Gentil V., Tavares S., Gorenstein C., Bello C. Acute reversal of flunitrazepam effects by Ro 15-1788 and Ro 15-3505. Inverse agonism, tolerance, and rebound Psychopharmacology (Berlin). 100:1990;54-59.
40. González L.E., File S.E. A five minute experience in the elevated plus-maze alters the state of the benzodiazepine receptor in the dorsal raphe nucleus. J. Neurosci. 17:1997;1505-1511.
41. Hendel J., Elsass P., Sorensen K.H., Moller I.W., Hvidberg E.F., Hansen T. Anxiety and sedation during a stressful situation after a single dose of diazepam versus N-desmethyldiazepam - A controlled trial. Psychopharmacology (Berlin). 70:1980;303-305.
42. Hoffman D.K., Britton D.R. Anxiogenic-like properties of benzodiazepine antagonists. Soc. Neurosci. Abstr. 9:1983;129.
43. Hommer D., Weingartner H., Breier A. Dissociation of benzoziazepine-induced amnesia from sedation by flumazenil pretreatment. Psychopharmacology (Berlin). 112:1993;455-460.
44. Howell D.C. Statistical methods for psychology. 1992;Duxbury Press, Wadsworth.
45. Hunkeler W., Möhler H., Pieri L., Polc P., Bonetti E.P., Cumin R., Schaffner R., Haefely W. Selective antagonists of benzodiazepines. Nature. 290:1981;514-516.
46. Insel T.R., Hill J.L., Mayor R.B. Rat pup ultrasonic isolation calls. Possible mediation by the benzodiazepine receptor complex Pharmacol. Biochem. Behav. 24:1986;1263-1267.
47. Ishizawa Y., Furuya K., Yamagishi S., Dohi S. Non-GABAergic effects of midazolam, diazepam and flumazenil on voltage-dependent ion currents in NG108-15 cells. Neuroreport. 8:1997;2635-2638.
48. Johnson N.J.T., Rodgers R.J. Ethological analysis of cholecystokinin (CCKA and CCKB) receptor ligands in the elevated plus-maze test of anxiety in mice. Psychopharmacology (Berlin). 124:1996;355-364.
49. Kapczinski F., Curran H.V., Gray J., Lader M. Flumazenil has an anxiolytic effect in simulated stress. Psychopharmacology (Berlin). 114:1994;187-189.
50. Kavaliers M., Colwell D.D. Decreased predator avoidance in parasitised mice. Neuromodulatory correlates Parasitology. 111:1995;257-263.
51. Kurishingal, H.: Relating the behavioural teratological effects of benzodiazepines to their actions on membrane fluidity. PhD Thesis, University of Wales; 1994.
52. Lee C., Rodgers R.J. Effects of benzodiazepine receptor antagonist, flumazenil, on antinociceptive and behavioural responses to the elevated plus-maze in mice. Neuropharmacology. 30:1991;1263-1267.
53. Liljequist S., Engel J.A. The effects of GABA and benzodiazepine receptor antagonists on the anti-conflict actions of diazepam or ethanol. Pharmacol. Biochem. Behav. 21:1984;521-525.
54. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology (Berlin). 92:1987;180-185.
55. Lloyd K.G., Bovier P., Broekkamp C.L., Worms P. Reversal of the antiaversive and anticonvulsant actions of diazepam, but not of progabide, by a selective antagonist of benzodiazepine receptors. Eur. J. Pharmacol. 75:1981;77-78.
56. Malizia A.L., Nutt D.J. The effects of flumazenil in neuropsychiatric disorders. Clin. Neuropharmacol. 18:1995;215-232.
57. Marcucci F., Fanelli R., Mussini E., Grattini S. Further studies on species difference in diazepam metabolism. Eur. J. Pharmacol. 9:1970;253-256.
58. Marcucci F., Guaitani A., Kvetina J., Mussini E., Grattini S. Species difference in diazepam metabolism and anticonvulsant effect. Eur. J. Pharmacol. 4:1968;467-470.
59. McCreary A.C., McBlane J.W., Spooner H.A., Handley S.L. 5HT systems and anxiety. Multiple mechanisms in the elevated X-maze Pol. J. Pharmacol. 48:1996;1-12.
60. Moy S.S., Knapp D.J., Criswell H.E., Breese G.R. Fumazenil blockade of anxiety following ethanol withdrawal in rats. Psychopharmacology (Berlin). 131:1997;354-360.
61. Nastiti K., Benton D., Brain P.F. The effects of compounds acting at the benzodiazepine receptor complex on the ultrasonic calling of mouse pups. Behav. Pharmacol. 2:1991;121-128.
62. Nutt D.J., Glue P., Lawson C., Wilson S. Flumazenil provocation of panic attacks. Arch. Gen. Psychiatry. 47:1990;917-925.
63. Patel J.B., Martin C., Malick J.B. Differential antagonism of the anticonflict effects of typical and atypical anxiolytics. Eur. J. Pharmacol. 86:1983;295-298.
64. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods. 14:1985;149-167.
65. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze. As novel test of anxiety in rat Pharmacol. Biochem. Behav. 24:1986;525-529.
66. Pokk P., Zharkovsky A. The effects of flumazenil, Ro15-4523 and β-CCM on the behaviour of control and stressed mice in the plus-maze test. J. Physiol. Pharmacol. 48:1997;253-261.
67. Polc P. GABA-independent mechanisms of benzodiazepine action. File S.E., Briley M. New concepts in anxiety. 1991;211-236 MacMillan Publishers, London.
68. Prado de Carvalho L., Venault P., Rossier J., Chapouthier G. Anxiogenic properties of convulsive agents. Soc. Neurosci. Abstr. 9:1983;128.
69. Quintero S., Henney H., Lawson P., Mellanby J., Gray J.A. The effects of compounds related to γ-aminobutyrate and benzodiazepine receptors on behavioural responses to anxiogenic stimuli in the rat. Punished barpressing Psychopharmacology (Berlin). 85:1985;244-251.
70. Quock R.M., Wetzel P.J., Maillefer R.H., Hodges B.L., Curtis B.A., Czech D.A. Benzodiazepine receptor-mediated behavioral effects of nitrous oxide in rat social inteaction test. Pharmacol. Biochem. Behav. 46:1993;161-165.
71. Randall P.K., Bremner J.D., Krystal J.H., Nagy L.M., Heninger G.R., Nicolaou A.L., Charney D.S. Effects of the benzodiazepine antagonist flumazenil in PTSD. Biol. Psychiatry. 38:1995;319-324.
72. Rex A., Marsden C.A., Fink H. Effect of diazepam on cortical 5-HT release and behaviour in the guinea pig on exposure to the elevated plus-maze. Psychopharmacology (Berlin). 110:1993;490-496.
73. Rex A., Stephens D.N., Fink H. "Anxiolytic" action of diazepam and abecarnil in a modified open field test. Pharmacol. Biochem. Behav. 53:1996;1005-1011.
74. Richards J.G., Möhler H., Haefely W. Benzodiazepine binding sites. Receptors or acceptors? Trends Pharmacol. Sci. 3:1982;233.
75. Rodgers R.J. Animal models of anxiety - Where next? Behav. Pharmacol. 8:1997;477-496.
76. Rodgers R.J., Cao B.-J., Dalvi A., Holmes A. Animal models of anxiety. An ethological perspective Braz. J. Med. Biol. Res. 30:1997;289-304.
77. Rodgers R.J., Cole J.C. The elevated plus-maze. Pharmacology, methodology and ethology Cooper S.J., Hendrie C.A. Ethology and psychopharmacology. 1994;8-44 Wiley, Chichester.
78. Rodgers R.J., Cole J.C., Aboualfa K., Stephenson L.H. Ethopharmacological analysis of the effects of putative 'anxiogenic' agents in the mouse elevated plus-maze. Pharmacol. Biochem. Behav. 52:1995;805-813.
79. Rodgers R.J., Johnson N.J.T. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol. Biochem. Behav. 52:1995;297-303.
80. Rodgers R.J., Randall J.I. Benzodiazepine ligands, nociception and 'defeat' analgesia in male mice. Psychopharmacology (Berlin). 91:1987;305-315.
81. Russo A.S., Guimaraes F.S., De Aguiar J.C., Graeff F.G. Role of benzodiazepine receptors located in the dorsal periaqueductal grey of rats in anxiety. Psychopharmacology (Berlin). 110:1993;198-202.
82. Salonen M., Onaivi E.S., Maze M. Dexmedetomidine synergism with midazolam in the elevated plus-maze test in rats. Psychopharmacology (Berlin). 108:1992;229-234.
83. Sarter M., Berntson G.G., Bruno J.P., Givens B.S. Agonizing over antagonizing. What do benzodiazepine receptor antagonists demonstrate? Psychopharmacology (Berlin). 126:1996;182-184.
84. Sayin U., Purali N., Ozkan T., Altung T., Buyukdevrim S. Vigabatrin has an anxiolytic effect in the elevated plus maze-test of anxiety. Pharmacol. Biochem. Behav. 43:1992;529-535.
85. Schmidt-Mutter C., Pain L., Sandner G., Gobaille S., Maitre M. The anxiolytic effect of γ-hydroxybutyrate in the elevated plus-maze is reversed by the benzodiazepine receptor antagonist, flumazenil. Eur. J. Pharmacol. 342:1998;21-27.
86. Shekhar A., Hingtgen J.N., DiMicco J.A. Anxiogenic effects of noreleagnine, a water soluble beta-carboline in rats. Neuropharmacology. 28:1989;539-542.
87. Sherif F., Oreland L. Effects of chronic treatment with the GABA-transaminase inhibitor vigabatrin on exploratory behaviour in rats. Behav. Brain Res. 63:1994;11-15.
88. A receptor subtypes. Pharmacol. Rev. 47:1995;181-234.
89. Slobodyansky E., Guidotti A., Wambebe C., Berkowich A., Costa E. Isolation and characterization of a rat brain triakontatetraneuropeptide, a posttranslational product of diazepam binding inhibitor. Specific action at the Ro5-4864 site J. Neurochem. 53:1989;1276-1284.
90. A/benzodiazepine chloride ionophore receptor complex in the 5,7-DHT induced anticonflict effect. Life Sci. 49:1991;139-153.
91. Stutzmann J., Böhme G.A., Cochon M., Roux M., Blanchard J. Proconflict and electrocorticographic effects of drugs modulating GABAergic neurotransmission. Psychopharmacology (Berlin). 91:1987;74-79.
92. Torres M.C., Morales A., Megías J.L., Cándido A., Maldonado A. Flumazenil antagonizes the effect of diazepam on negative contrast in one-way avoidance learning. Behav. Pharmacol. 5:1994;637-641.
93. Treit D., Menard J., Royan C. Anxiogenic stimuli in the elevated plus-maze. Pharmacol. Biochem. Behav. 44:1993;463-469.
94. Wada T., Fukuda N. Effects of DN-2327, a new anxiolytic, diazepam and buspirone on exploratory activity of in an elevated plus-maze. Psychopharmacology (Berlin). 104:1991;444-450.
95. Wilcox R.R. New designs in analysis of variance. Annu. Rev. Psychol. 38:1987;29-60.