'One-trial sensitization' to the anxiolytic-like effects of cannabinoid receptor antagonist SR141716A in the mouse elevated plus-maze

European Journal of Neuroscience

Volumn 17, Issue 6, 2003, Pages 1279-1286

  Rodgers, R J ^a   Haller, J ^b   Halasz, J ^b   Mikics, E ^b  

^a UNIVERSITY OF LEEDS   (United Kingdom)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Activity; Anxiety; CB1 receptor; Chlordiazepoxide; Novel cannabinoid receptor; One trial tolerance; Prior experience

Indexed keywords

BENZODIAZEPINE DERIVATIVE; CANNABINOID 1 RECEPTOR; CANNABINOID RECEPTOR ANTAGONIST; CHLORDIAZEPOXIDE; RIMONABANT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DRUG EFFECT; MALE; MAZE TEST; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; TRANQUILIZING ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; CHLORDIAZEPOXIDE; ENDOCANNABINOIDS; MALE; MAZE LEARNING; MICE; PIPERIDINES; PYRAZOLES; RECEPTORS, CANNABINOID; RECEPTORS, DRUG;

EID: 0037363831     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2003.02548.x     Document Type: Article

References (77)

1. Adams, I.B. & Martin, B.R. (1996) Cannabis: pharmacology and toxicology in animals and humans. Addiction, 91, 1585-1614.
2. Akinshola, B.E., Chakrabarti, A. & Onaivi, E.S. (1999) In vitro and in vivo action of cannabinoids. Neurochem. Res., 24, 1233-1240.
3. Ameri, A. (1999) The effects of cannabinoids on the brain. Prog. Neurobiol., 58, 315-348.
4. Arevalo, C., de Miguel, R. & Hernandez-Tristan, R. (2001) Cannabinoid effects on anxiety-related behaviours and hypothalamic neurotransmitters. Pharmacol. Biochem, Behav., 70, 123-131.
5. 9-tetrahydrocannabinol. Psychopharmacology, 163, 111-117.
6. Bertoglio, L.J. & Carobrez, A.P. (2000) Previous maze experience required to increase open arms avoidance in rats submitted to the elevated plus-maze model of anxiety. Behav. Brain Res., 108, 197-203.
7. Breivogel, C.S., Griffin, G., Di Marzo, V. & Martin, B.R. (2001) Evidence for a new G-protein-coupled cannabinoid receptor in mouse brain. Molec. Pharmacol., 60, 155-163.
8. 4 receptors and anxiety: behavioural profiles of clozapine, L-745,870 and L-741,742 in the mouse plus-maze. Eur. J. Pharmacol., 335, 117-125.
9. Chakrabarti, A., Ekuta, J.E. & Onaivi, E.S. (1998) Neurobehavioral effects of anandamide and cannabinoid receptor gene expression in mice. Brain Res. Bull., 45, 67-74.
10. Chaperon, F. & Thiebot, M.-H. (1999) Behavioral effects of cannabinoid agents in animals. Crit. Rev. Neurobiol., 13, 243-281.
11. Cole, J.C. & Rodgers, R.J. (1993) An ethological analysis of the effects of chlordiazepoxide and bretazenil (Ro 16-6028) in the murine elevated plusmaze. Behav. Pharmacol., 4, 573-580.
12. Cole, J.C. & Rodgers, R.J. (1995) 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, 473-478.
13. Cruz-Morales, S.E., Santos, N.R. & Brandao, M.L. (2002) One-trial tolerance to midazolam is due to enhancement of fear and reduction of anxiolytic-sensitive behaviors in the elevated plus-maze retest in the rat. Pharmacol. Biochem. Behav., 72, 973-978.
14. Davies, S.N., Pertwee, R.G. & Riedel, G. (2002) Functions of cannabinoid receptors in the hippocampus. Neuropharmacology, 42, 993-1007.
15. De Vries, T.J., Shaham, Y., Homberg, J.R., Crombag, H., Schuurman, K., Dieben, J., Vanderschuren, L.J.M.J. & Schoffelmeer, A.N.M. (2001) A cannabinoid mechanism in relapse to cocaine seeking. Nature Med., 7, 1151-1154.
16. Devane, W.A., Dysarz, F.A., Johnson, M.R., Melvin, L.S. & Howlett, A.C. (1988) Determination and characterisation of a cannabinoid receptor in the rat brain. Molec. Pharmacol., 34, 605-613.
17. Devane, W.A., Hanus, L., Breuer, A., Pertwee, R.G., Stevenson, L.A., Griffin, G., Gibson, D., Mandelbaum, A., Ettinger, A. & Mechoulam, R. (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science, 258, 1946-1949.
18. Di Marzo, V., Breivogel, C.S., Tao, Q., Bridgen, D.T., Razdan, R.K., Zimmer, A.M., Zimmer, A. & Martin, B.R. (2000) Levels, metabolism, and pharmacological activity of anandamide in CB (1) cannabinoid receptor knockout mice: evidence for non-CB (1), non-CB (2) receptor-mediated actions of anandamide in mouse brain. J. Neurochem., 75, 2434-2444.
19. Espejo, E.F. (1997) Effects of weekly or daily exposure to the elevated plus-maze in male mice. Behav. Brain Res., 87, 233-238.
20. Fernandes, C. & File, S.E. (1996) Influence of open arm ledges and maze experience in the elevated plus-maze. Pharmacol. Biochem. Behav., 54, 31-40.
21. File, S.E. (1990) One-trial tolerance to the anxiolytic effects of chlordiazepoxide in the plus-maze. Psychopharmacology, 100, 281-282.
22. File, S.E. (1993) The interplay of learning and anxiety in the elevated plus-maze. Behav. Brain Res., 58, 199-202.
23. File, S.E. & Zangrossi, H. (1993) One-trial tolerance to the anxioJytic actions of benzodiazepines in the elevated plus-maze, or the development of a phobic state? Psychopharmacology, 110, 240-244.
24. File, S.E., Zangrossi, H., Viana, M. & Graeff, F.G. (1993) Trial 2 in the elevated plus-maze: a different form of fear? Psychopharmacology, 111, 491-494.
25. Gonzalez, L.E. & File, S.E. (1997) A five minute experience in the elevated plus-maze alters the state of the benzodiazepine receptor in the dorsal raphe nucleus. J. Neurosci., 17, 1505-1511.
26. Gray, J.A. & McNaughton, N. (2000) The Neuropsychology of Anxiety: an Enquiry Into the Functions of the Septo-Hippocampal System, 2nd edn. Oxford University Press, Oxford.
27. Griebel, G., Moreau, J.-L., Jenck, F., Martin, J.R. & Misslin, R. (1993) Some critical determinants of the behaviour of rats in the elevated plus-maze. Behav. Proc., 29, 37-48.
28. 1A receptor antagonists in three rat models of anxiety. Neuropharmacology, 39, 1848-1857.
29. Hajos, N., Katona, I., Naiem, S.S., Mackie, K., Ledent, C., Mody, I. & Freund, T.F. (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci., 12, 3239-3249.
30. Hajos, N., Ledent, C. & Freund, T.F. (2001) Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience, 106, 1-4.
31. Hall, W. & Solowij, N. (1998) Adverse effects of cannabis. Lancet, 352, 1611-1616.
32. Haller, J., Bakos, N., Szirmay, M., Ledent, C. & Freund, T.F. (2002) The effects of genetic and pharmacological blockade of the CB1 cannabinoid receptor on anxiety. Eur. J. Neurosci., 16, 1395-1398.
33. Hanus, L., Abu-Lafi, S., Fride, E., Breuer, A., Vogel, Z., Shalev, D.E., Kustanovich, I. & Mechoulam, R. (2001) 1-Arachidonyl glyceryl ether, and endogenous agonist of the cannabinoid CB1 receptor. Proc. Natl Acad. Sci. USA, 98, 3662-3665.
34. Herkenham, M., Lynn, A.B., Johnson, M.R., Melvin, L.S., de Costa, B.R. & Rice, K.C. (1991) Characterization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiography study. J. Neurosci., 11, 63-583.
35. Hollister, L.E. (1986) Health aspects of cannabis. Pharmacol. Rev., 38, 2-20.
36. Holmes, A. & Rodgers, R.J. (1998) Responses of Swiss-Webster mice to repeated plus-maze experience: further evidence for a qualitative shift in emotional state? Pharmacol. Biochem. Behav., 60, 473-488.
37. Holmes, A. & Rodgers, R.J. (1999) Influence of spatial and temporal manipulations on the anxiolytic efficacy of chlordiazepoxide in mice previously exposed to the elevated plus-maze. Neurosci. Biobehav. Rev., 23, 971-980.
38. Huestis, M.A., Gorelick, D.A., Heishman, S.J., Preston, K.L., Nelson, R.A., Moolchan, E.T. & Frank, R.A. (2001) Blockade of effects of smoked marijuana by the CB1-selective cannabinoid receptor antagonist SR141716A. Arch. Gen. Psychiat., 58, 322-328.
39. Jarai, Z., Wagner, J.A., Varga, K., Lake, K.D., Compton, D.R., Martin, B.R., Zimmer, A.M., Bonner, T.I., Buckley, N.E., Mexey, E., Razdan, R.K., Zimmer, A. & Kunos, G. (1999) Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 and CB2 receptors. Proc. Natl Acad. Sci. USA, 96, 14136-14141.
40. Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N. & Freund, T.F. (2001) Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. J. Neurosci., 21, 9506-9518.
41. Katona, I., Sperlagh, B., Sik, A., Kafalvi, A., Vizi, E.S., Mackie, K. & Freund, T.F. (1999) Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci., 19, 4544-4558.
42. Kirkham, T.C. & Williams, C.M. (2001) Endogenous cannabinoids and appetite. Nutr. Res. Rev., 14, 65-86.
43. Lister, R.G. (1987) The use of the plus-maze to measure anxiety in the mouse. Psychopharmacology, 92, 180-185.
44. Low, K., Crestani, F., Keist, R., Benke, D., Brunig, I., Benson, J.A., Fritschy, J.M., Rulicke, T., Bluethmann, H., Mohler, H. & Rudolph, U. (2000) Molecular and neuronal substrate for the selective attenuation of anxiety. Science, 290, 131-134.
45. 1 cannabinoid receptor knockout mice: correlation with behaviour. Eur. J. Neurosci., 15, 1178-1186.
46. Marsicano, G., Wotjak, C.T., Azad, S.C., Bisogno, T., Rammes, G., Cascio, M.G., Hermann, H., Tang, J., Hofmann, C., Zieglgansberger, W., Di Marzo, V. & Lutz, B. (2002) The endogenous cannabinoid system controls extiinction of aversive memories. Nature, 418, 530-534.
47. Martin, M., Ledent, C., Parmentier, M., Maldonado, R. & Valverde, O. (2002) Involvement of CB1 cannabinoid receptors in emotional behaviour. Psychopharmacology, 159, 379-387.
48. Matsuda, L.A., Bonner, T.I. & Lolait, S.J. (1993) Localization of cannabinoid receptor mRNA in rat brain. J. Comp. Neurol., 327, 535-550.
49. McGregor, I.S., Dastur, F.N., McLellan, R.A. & Brown, R.E. (1996) Cannabinoid modulation of rat pup ultrasonic vocalizations. Eur. J. Pharmacol., 313, 43-49.
50. Mechoulam, R., Ben-Shabat, S., Hanus, L., Ligumsky, M., Kaminski, N.E., Schatz, A.R., Gopher, A., Almog, S., Martin, B.R., Compton, D.R., Pertwee, R.G., Griffin, G., Bayewitch, M., Barg, J. & Vogel, Z. (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol., 50, 83-90.
51. Meyer, R.E. (1978) Behavioral pharmacology of marijuana. In Lipton, M.A., DiMascio, A. & Killam, K.F. (eds), Psychopharmacology: a Generation of Progress. Raven Press, New York, pp. 1634-1652.
52. Munro, S., Thomas, K.L. & Abu-Shaar, M. (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature, 365, 61-65.
53. 1 cannabinoid receptor antagonist SR141716A induces anxiety-like responses in the rat. Neuroreport, 8, 491-496.
54. A receptors in synapses of hippocampal pyramidal cells of the rat. Eur. J. Neurosci., 13, 428-442.
55. 9-THC and cannabinoid (CB1) receptor gene expression in mice. Behav. Brain Res., 72, 115-125.
56. Onaivi, E.S., Green, M.R. & Martin, B.R. (1990) Pharmacological characterization of cannabinoids in the elevated plus-maze. J. Pharmacol. Exp. Ther., 253, 1002-1009.
57. Porter, A.C. & Felder, C.C. (2001) The endocannabinoid nervous system: unique opportunities for therapeutic intervention. Pharmacol. Ther., 90, 45-60.
58. Ramos, A. & Mormede, P. (1998) Stress and emotionality: a multidimensional and genetic approach. Neurosci. Biobehav. Rev., 22, 33-57.
59. Rinaldi-Carmona, M., Barth, F., Heaulme, M., Alonso, R., Shire, D., Congy, C., Soubrie, P., Breliere, J.C. & LeFur, G. (1995) Biochemical and pharmacological characterization of SR141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci., 56, 1941-1947.
60. Rodgers, R.J. (1997) Animal models of 'anxiety': where next? Behav. Pharmacol., 8, 477-496.
61. Rodgers, R.J. & Johnson, N.J.T. (1995) Factor analysis of spatiotemporal and ethological measures in the routine elevated plus-maze test of anxiety. Pharmacol. Biochem. Behav., 52, 297-303.
62. Rodgers, R.J. & Johnson, N.J.T. (1998) Behaviorally selective effects of neuroactive steroids on plus-maze anxiety in mice. Pharmacol. Biochem. Behav., 59, 221-232.
63. Rodgers, R.J., Johnson, N.J.T., Cole, J.C., Dewar, C.V., Kidd, G.R. & Kimpson, P.H. (1996) Plus-maze retest profile in mice: importance of initial stages of trial 1 and response to post-trial cholinergic receptor blockade. Pharmacol. Biochem. Behav., 54, 41-50.
64. Rodgers, R.J., Lee, C. & Shepherd, J.K. (1992) Effects of diazepam on behavioural and antinociceptive responses to the elevated plus-maze in male mice depend upon treatment regimen and prior maze experience. Psychopharmacology, 106, 101-110.
65. Rodgers, R.J. & Shepherd, J.K. (1993) Influence of prior maze experience on behaviour and response to diazepam in the elevated plus-maze and light/dark tests of anxiety in mice. Psychopharmacology, 113, 237-242.
66. Rodriguez de Fonseca, F., Carrera, M.R.A., Navarro, M., Koob, G.F. & Weiss, F. (1997) Activation of corticotropin-releasing factor in the limbic system during cannabinoid withdrawal. Science, 276, 2050-2054.
67. Rodriguez de Fonseca, F., Rubio, P., Menzaghi, F., Merlo-Pich, E., Rivier, J., Koob, G.F. & Navarro, M. (1996) Corticotropin-releasing factor (CRF) antagonist [D-Phe12,N-le21,38,C alpha MeLeu37]CRF attenuates the acute actions of the highly potent cannabinoid receptor agonist HU-210 on defensive-withdrawal behavior in rats. J. Pharmacol. Exp. Ther., 276, 56-64.
68. Schlicker, E. & Kathmann, M. (2001) Modulation of transmitter release via presynaptic cannabinoid receptors. Trends Pharmacol. Sci., 22, 565-572.
69. Setem, J., Pinheiro, A.P., Motta, V.A., Morato, S. & Cruz, A.P.M. (1999) Ethopharmacological analysis of 5-HT ligands on the rat elevated plus-maze. Pharmacol. Biochem. Behav., 62, 515-521.
70. Sulcova, A., Mechoulam, R. & Fride, E. (1998) Biphasic effects of anandamide. Pharmacol. Biochem. Behav., 59, 347-352.
71. Treit, D., Menard, J. & Royan, C. (1993) Anxiogenic stimuli in the elevated plus-maze. Pharmacol. Biochem. Behav., 40, 463-469.
72. Tsou, K., Mackie, K., Sanudo-Pena, M.C. & Walker, J.M. (1999) Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience, 93, 969-975.
73. Tunving, K. (1987) Psychiatric aspects of cannabis use in adolescents and young adults. Pediatrician, 14, 83-91.
74. 9-tetrahydrocannabinol and nicotine. Br. J. Pharmacol., 135, 564-578.
75. Weiss, S.M. (1995) Pharmacological and behavioural examination of the defensive reactions of laboratory mice to the calls of the Tawny Owl. PhD Thesis, University of Leeds, UK.
76. Zimmer, A., Zimmer, A.M., Hohmann, A.G., Herkenham, M. & Bonner, T.I. (1999) Increased mortality, hypoactivity and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc. Natl Acad. Sci. USA, 96, 5780-5785.
77. 9-THC in normal subjects. Psychopharmacology, 76, 245-250.