Midazolam impairs the acquisition of conditioned analgesia if rats are tested with an acute but not a chronic noxious stimulus

Brain Research Bulletin

Volumn 39, Issue 4, 1996, Pages 227-233

  Harris, J A ^a   Westbrook, R F ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Amnesia; Benzodiazepine; Conditioned fear; Formalin test; Hot plate; Retrieval deficit

Indexed keywords

BENZODIAZEPINE DERIVATIVE; FORMALDEHYDE; MIDAZOLAM; NALOXONE;

AMNESIA; AMYGDALOID NUCLEUS; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONDITIONING; CONTROLLED STUDY; DOSE RESPONSE; FEAR; LEARNING; NOCICEPTIVE STIMULATION; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT;

EID: 0029878215     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/0361-9230(95)02140-X     Document Type: Article

References (59)

1. Abbott, F. V.; Franklin, K. B. J.; Westbrook, R. F. The formalin test: Scoring properties of the first and second phases of the pain response in rats. Pain 60:91-102; 1995.
2. Alheid, G. F.; de Olmos, J. S.; Beltramino, C. A. Amygdala and extended amyygdala. In: Paxinos, G., ed. The rat nervous system. New York: Academic Press; 1995:495-578.
3. Balleine, B.; Ball, J.; Dickinson, A. Benzodiazepine-induced outcome revaluation and the motivational control of instrumental action in rats. Behav. Neurosci. 108:573-589; 1994.
4. Campeau, S.; Miserendino, M. J. D.; Davis, M. Intra-amygdala infusion of the N-methyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus. Behav. Neurosci. 106:569-574; 1992.
5. Carrive, P. The periaqueductal gray and defensive behavior: Functional representation and neuronal organization. Behav. Brain Res. 58:27-47; 1993.
6. Cole, B. J.; Hillmann, M. Effects of benzodiazepine receptor ligands on the performance of an operant delayed matching to position task in rats: Opposite effects of FG 7142 and lorazepam. Psychopharmacology (Berlin) 115:350-357; 1994.
7. Cooper, S. J. Benzodiazepines as appetite enhancing compounds. Appetite 1:7-19; 1980.
8. Cooper, S. J. Benzodiazepine receptor-mediated enhancement and inhibition of taste reactivity, food choice and intake. Ann. NY Acad. Sci. 575:321-337; 1989.
9. Cooper, S. J.; Yerbury, R. E. Midazolam-induced hyperphagia and FG 7142-induced anorexia: Behavioural characteristics in the rat. Pharmacol. Biochem. Behav. 25:99-106; 1986.
10. Davis, M. Diazepam and flurazepam: Effects on conditioned fear as measured with the potentiated startle paradigm. Psychopharmacology (Berlin) 62:1-7; 1979.
11. Davis, M. The role of the amygdala in conditioned fear. In: Aggleton, J. P., ed. The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction. New York: Wiley-Liss; 1992:255-305.
12. Depaulis, A.; Keay, K. A.; Bandler, R. Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp. Brain Res. 90:307-318; 1992.
13. Dickinson-Anson, H.; McGaugh, J. L. Midazolam administered into the amygdala impairs retention of an inhibitory avoidance task. Behav. Neural Biol. 60:84-87; 1993.
14. Dickinson-Anson, H.; Mesches, M. H.; Coleman, K.; McGaugh, J. L. Bicuculline administered into the amygdala blocks benzodiazepine-induced amnesia. Behav. Neural Biol. 60:1-4; 1993.
15. Dubuisson, D.; Dennis, S. G. The formalin test: A quantitative study of the analgesic effects of morphine, meperedine and brain stem stimulation in rats and cats. Pain 4:161-174; 1977.
16. Fanselow, M. S. The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In: Depaulis, A.; Bandler, R., eds. The periaqueductal gray matter. New York: Plenum Press; 1991:139-150.
17. Fanselow, M. S. Analgesia as a response to aversive Pavlovian conditional stimuli: Cognitive and emotional mediators. In: Denny, M. R., ed. Fear, avoidance, and phobias: A fundamental analysis. Hillsdale NJ: Lawrence Erlbaum; 1991:61-86.
18. Fanselow, M. S.; Helmstetter, F. J. Conditional analgesia, defensive freezing, and benzodiazepines. Behav. Neurosci. 102:233-243; 1988.
19. Fanselow, M. S.; Kim, J. J. Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphonovaleric acid to the basolateral amygdala. Behav. Neurosci. 108:210-212; 1994.
20. Flaherty, C. F. Effects of anxiolytics and antidepressants on extinction and negative contrast. Pharmacol. Ther. 46:309-320; 1990.
21. Gallagher, M.; Graham, P. W.; Holland, P. C. The amygdala central nucleus and appetitive Pavlovian conditioning : Lesions impair one class of conditioned behavior. J. Neurosci. 10:1906-1911; 1990.
22. Gray, J. A. Drug effects on fear and frustration: Possible limbic site of action of minor tranquilizers. In: Iversen, L. L.; Iversen, S. D.; Snyder, S. H., eds. Handbook of psychopharmacology, vol. 8: Drugs, neurotransmitters, and behavior. New York: Plenum Press; 1977:433-529.
23. Gray, J. A. The neuropsychology of anxiety: An enquiry into the functions of the septo-hippocampal system. Oxford University Press: Oxford; 1982.
24. Greeley, J. D.; Westbrook, R. F. Some effects of exposure to a heat sressor upon the rat's subsequent reactions to that sressor. Q. J. Exp. Psychol. 42B:241-265; 1990.
25. A-benzodiazepine receptor: Biology and pharmacology. In: Burrows, G. D.; Roth, M.; Noyes, R. Jr., eds. Handbook of anxiety, vol. 3: The neurobiology of anxiety. New York: Elsevier; 1990:165-188.
26. Harris, J. A.; McGregor, I. S.; Westbrook, R. F. Low and high doses of midazolam differentially affect hypoalgesia in rats conditioned to a heat stressor. Psychopharmacology (Berlin) 111: 62-68; 1993.
27. Harris, J. A.; Westbrook, R. F. Effects of midazolam and naloxone in rats tested for sensitivity/reactivity to formalin pain in a familiar, novel or aversively conditioned environment. Psychopharmacology (Berlin) 115:65-72; 1994.
28. Harris, J. A.; Westbrook, R. F. Effects of benzodiazepine microinjection into the amygdala or periaqueductal gray upon the expression of conditioned fear and hypoalgesia in rats. Behav. Neurosci. 109:295-304; 1995.
29. Hays, W. L. Statistics for the social sciences. New York: Holt, Rinehart, and Winston; 1972.
30. Hodges, H.; Green, S.; Glenn, B. Evidence that the amygdala is involved in benzodiazepine and serotonergic effects on punished responding but not discrimination. Psychopharmacology (Berlin) 92:491-504; 1987.
31. Holland, P. C. Conditioned stimulus as a determinant of the form of the Pavlovian conditioned response. J. Exp. Psychol. Anim. Behav. Proc. 3:77-104; 1977.
32. Kapp, B. S.; Whalen, P. J.; Supple, W. F.; Pascoe, J. P. Amygdaloid contributions to conditioned arousal and sensory information processing. In: Aggleton, J. P., ed. The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction. New York: Wiley-Liss; 1992:229-254.
33. Kaye, H.; Pearce, J. M. The strength of the orienting response during Pavlovian conditioning. J. Exp. Psychol. Anim. Behav. Proc. 10:90-109; 1984.
34. Lavond, D. G.; Kim; J. J.; Thompson, R. F. Mammalian brain substrates of aversive classical conditioning. Annu. Rev. Psychol. 44:317-342; 1993.
35. LeDoux, J. E. Brain mechanisms of emotion and emotionial learning. Curr. Opin. Neurobiol. 2:191-197; 1992.
36. McNaughton, N.; Morris, R. G. Chlordiazepoxide, an anxiolytic benzodiazepine, impairs place navigation in rats. Behav. Brain Res. 24:39-46; 1987.
37. Miserendino, M. J. D.; Sananes, C. B.; Melia, K. R.; Davis, M. Blocking the acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists into the amygdala. Nature 345:716-718; 1990.
38. Nagy, J.; Námbó, K.; Decsi, L. Anti-anxiety action of diazepam after intra-amygdaloid application in the rat. Neuropharmacology 18:573-576; 1979.
39. O'Brien, R. G.; Kaiser, M. K. MANOVA method for analyzing repeated measures designs: An extensive primer. Psychol. Bull. 97:316-333; 1985.
40. Petersen, E. N.; Braestrup, C.; Scheel-Krüger, J. Evidence that the anticonflict effect of midazolam in amygdala is mediated by the specific benzodiazepine receptors. Neurosci. Lett. 53:28-288; 1985.
41. Rescorla, R. A.; Wagner, A. R. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In: Black, A. H.; Prokasy, W. F., eds. Classical conditioning II: Current research and theory. New York: Appleton-Century -Crofts; 1972:64-99.
42. Rodger, R. S. Type II errors and their decision basis. Br. J. Math. Statist. Psychol. 20:187-204; 1967.
43. Rothschild, A. J. Disinhibition, amnestic reactions, and other adverse reactions secondary to triazolam: A review of the literature. J. Clin. Psychiatry 53 (Suppl.):69-79; 1992.
44. Salinas, J. A.; Dickinson-Anson, H.; McGaugh, J. L. Midazolam administered to rats induces anterograde amnesia for changes in reward magnitude. Behav. Neurosci. 108:1059-1064; 1994.
45. Scheel-Krüger, J.; Petersen, E. N. Anticonflict effect of the benzodiazepines mediated by a GABAergic mechanism in the amygdala. Eur. J. Pharmacol. 82:115-116; 1982.
46. Shibata, S.; Yamashita, K.; Yamamoto, E.; Ozaki, T.; Ueki, S. Effects of benzodiazapine and GABA antagonists on anticonflict effects of antianxiety drugs injected into the rat amygdala in a waterlick suppression test. Psychopharmacology (Berlin) 98:38-44; 1989.
47. Smith, C. G.; Beninger, R. J.; Mallet, P. E.; Jhamandas, K.; Boegman, R. J. Basal forebrain injections of the benzodiazepine partial inverse agonist FG 7142 enhance memory of rats in the double Y-maze. Brain Res. 666:61-67; 1994.
48. Stackman, R. W.; Walsh, T. J. Chlordiazepoxide-induced working memory impairments: Site specificity and reversal by flumazenil (RO15-1788). Behav. Neural Biol. 57:233-43; 1992.
49. Sutherland, N. S.; Mackintosh, N. J. Mechanisms of animal discrimination learning. New York: Academic Press; 1971.
50. Thiébot, M.-H. Some evidence for amnesic-like effects of benzodiazepines in animals. Neurosci. Biobehav. Rev. 9:95-100; 1985.
51. 3H]diazepam binding density with anxiolytic locus in the amygdaloid complex of the rat. Brain Res. 342:85-90; 1985.
52. Tohyama, K.; Nabeshima, T.; Ichihara, K.; Kameyama, T. Involvement of GABAergic systems in benzodiazepine-induced impairment of passive avoidance learning in mice. Psychopharmacology (Berlin) 105:22-26; 1991.
53. Tomaz, C.; Dickinson-Anson, H.; McGaugh, J. L. Amygdala lesion block the amnestic effects of diazepam. Brain Res. 568:85-91; 1991.
54. Tomaz, C.; Dickinson-Anson, H.; McGaugh, J. L. Basolateral amygdala lesion block diazepam-induced anterograde amnesia in an inhibitory avoidance task. Proc. Natl. Acad. Sci. USA 89:3615-3619; 1992.
55. Tomaz, C.; Dickinson-Anson, H.; McGaugh, J. L.; Souza-Silva, M. A.; Viana, M. B.; Graeff, F. G. Localization in the amygdala of the amnestic action of diazepam on emotional memory. Behav. Brain Res. 58:99-105; 1993.
56. Venault, P.; Chapouthier, G.; de Carvalho, L. P.; Simiand, J.; Morre, M.; Dodd, R. H.; Rossier, J. Benzodiazepine impairs and beta-carboline enhances performance in learning and memory tasks. Nature 321:864-866; 1986.
57. Wagner, A. R. SOP: A model of automatic memory processing in animal behavior. In: Spear, N. E.; Miller, R. R., eds. Information processing in animals: Memory mechanisms. Hillsdale, NJ: Erlbaum; 1981:5-47.
58. Wagner, A. R.; Brandon, S. E. Evolution of a structured connectionist model of Pavlovian conditioning (ÆSOP). In: Klein, S. B.; Mowrer, R. R., eds. Contemporary learning theories. Hillsdale, NJ: Erlbaum; 1989:149-189.
59. Westbrook, R. F.; Greeley, J. D.; Nabke, C. P.; Swinbourne, A. L. Aversive conditioning in the rat: Effects of a benzodiazepine and of an opioid agonist and antagonist on conditioned hypoalgesia and fear. J. Exp. Psychol. Anim. Behav. Proc. 17:219-230; 1991.