Morphine state-dependent learning: Interactions with α2-adrenoceptors and acute stress

Behavioural Pharmacology

Volumn 14, Issue 1, 2003, Pages 41-48

  Homayoun, H ^a   Khavandgar, S ^a   Zarrindast, M R ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

Morphine; Mouse; Passive avoidance; Restraint stress; State dependent learning; 2 adrenergic receptors

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; CLONIDINE; MORPHINE; MU OPIATE RECEPTOR; YOHIMBINE;

AMNESIA; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOSE CALCULATION; DRUG EFFECT; LEARNING; MALE; MEMORY; MOUSE; NONHUMAN; PROTEIN INTERACTION; STRESS; TIME;

EID: 0037325887     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/00008877-200302000-00004     Document Type: Article

References (64)

1. Aghajanian GK (1978). Tolerance of focus coeruleus neurons to morphine and suppression of withdrawal response by clonidine. Nature 276:186-188.
2. Aley KO, Levine JD (1997). Multiple receptors involved in peripheral alpha2, mu, and A1 antinociception, tolerance, and withdrawal. J Neurosci 17:735-744.
3. Bats S, Thoumas JL, Lordi B, Tonon MC, Lalonde R, Caston J (2001). The effects of a mild stressor on spontaneous altenation in mice. Behav Brain Res 8:11-15.
4. Beylin AV, Shors TJ (1998). Stress enhances excitatory trace eyeblink conditioning and opposes acquisition of inhibitory conditionding. Behav Neurosci 112:1327-1338.
5. Bruins Slot LA, Colpaert FC (1999a). Opiate states of memory: receptor mechanisms. J Neurosci 19:10520-10529.
6. Bruins Slot LA, Colpaert FC (1999b). Recall rendered dependent on an opiate state. Behav Neurosci 113:337-344.
7. Cabib S, Castellano C (1997). Impairments produced by amphetamine and stress on memory storage reduced following a chronic stressful experience. Psychopharmacology 129:161-167.
8. Calcagnetti DJ, Holtzman SG (1990). Factors affecting restraint stress-induced potentiation of morphine analgesia. Brain Res 537:157-162.
9. Castellano C, Pavone F, Puglisi Allegra S (1984). Morphine and memory in DBA/2 mice: efects of stress and of prior experience. Behav Brain Res 11:3-10.
10. Castellano C, Cestari V, Cabib S, Puglisi-Allegra S (1994). The effects of morphine on memory consolidation in mice involve both D1 and D2 dopamine receptors. Behav Neural Biol 61:156-161.
11. Castellano C, Cestari V, Ciamei A, Pavone F (1999). MK-801-induced disruption of one-trial inhibitory avoidance are potentiated by stress and reversed by naltrexone. Neurobiol Learn Mem 72:215-229.
12. Chopin P, Colpaert FC, Marien M (2002). Effects of acute and subchronic administration of dexefaron, an alpha(2)-adrenoceptor antagonist, on memory performance in young adult and aged rodents. J Pharmacol Exp Ther 301:187-196.
13. Chugh Y, Saha N, Sankaranarayanan A, Sharma PL (1991). Possible mechanism of haloperidol-induced enhancement of memory retrieval. Methods Find Exp Clin Pharmacol 13:161-164.
14. Fendt M, Koch M, Schnitzler HU (1994). Amygdaloid noradrenaline is involved in the sensitization of the acoustic response in rats. Pharmacol Biochem Behav 48:307-314.
15. Ferry B, McGaugh JL (2000). Role of amygdala norepinephrine in mediating stress hormone regulation of memory storage. Acta Pharmacol Sin 21:481-493.
16. Freedman JE, Aghajanian GK (1985). Opiate and alpha 2-adrenecepter responses of rat amygdaloid neurons: co-localization and interactions during withdrawal. J Neurosci 5:3016-3024.
17. Genkova-Papazova M, Lazarova-Bakarova M, Petkov VD (1994). The 5-HT2 receptor antagonist ketanserine prevents electroconvulsive shock- and clonidine-induced amnesia. Pharmacol Biochem Behav 49:849-852.
18. Gold PE, van Burskirk RB (1978). Posttraining brain norepinephrine concentrations: correlation with retention performance of avoidance training and with peripheral epinephrine modulation of memory processing. Behav Biol 25:509-520.
19. Hawkins M, Monti M (1979). Effects of pretreatment with 6-OHDA or NA-ergic receptor blockers on the clonidine-induced disruption of conditioned avoidance responding. Eur J Pharmacol 58:53-58.
20. Hiramatsu M, Sasaki M, Kameyama T (1995). Effects of dynorphin A-(1-13) on carbon monoxide-induced delayed amnesia in mice studied in step-down type passive avoidance task. Eur J Pharmacol 282:185-191.
21. Introini-Collison IB, Saghafi D, Novack G, McGaugh JL (1992). Memory enhancing effects of posttraining dipivefrin and epinephrine: involvement of peripheral and central adrenergic receptors. Brain Res 572:81-86.
22. Izquierdo I (1980). Effect of β-endorphin and naloxone on acquisition, memory, and retrieval of shuttle avoidance and habituation learning in rats. Psychopharmacology 69:111-115.
23. Izquierdo I, Dias RD (1981). Retrograde amnesia caused by Met-, Leu- and des-Try-Met-enkaphalin in the rat and its reversal by naloxone. Neurosci Lett 22:189-193.
24. Izquierdo I, Dias RD (1984). Involvement of alpha-adrenergic receptors in the amnesic and anti-amnesic action of ACTH, beta-endorphin and epinephrine. Psychoneuroendocrinology 9:77-81.
25. Izquierdo I, Medina JH (1997). Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68:285-316.
26. Izquierdo I, Medina JH, Vianna MRM, Izquierdo LA, Barros DM (1999). Separate mechanisms for short- and long-term memory. Behav Brain Res 103:1-11.
27. Jellestad FK, Bakke HK (1985). Passive avoidance after ibotenic acid and radio frequency lesions in the rat amygdala. Physiol Behav 34:299-305.
28. Khavandgar S, Homayoun H, Torkaman-Boutorabi A, Zarrindast MR (2002). The effects of adenosine receptor agonists and antagonists on morphine state-dependent memory of passive avoidance. Neurobiol Learn Mem 78:390-405.
29. Kim JJ, Baxter MG (2001). Multiple brain memory systems: the whole does not equal the sum of its parts. Trends Neurosci 24:324-330.
30. Kim JJ, Lee HJ, Han JS, Packard MG (2001). Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21:5222-5228.
31. Lazarova-Bakarova MB, Genkova-Papazova MG (1989). Influence of nootropic drugs on the memory-impairing effect of clonidine in albino rats. Methods Find Exp Clin Pharmacol 11:235-239.
32. Lewis JW, Cannon JT, Liebeskind JC (1980). Opioid and nonopioid mechanisms of stress analgesia. Science 208:623-625.
33. Maier SF, Sherman JE, Lewis JW, Terman GW, Liebeskind JC (1983). The opioid/nonopioid nature of stress-induced analgesia and learned helplessness. J Exp Psych Animal Behav Process 9:80-90.
34. Maldonado R (1997). Participation of noradrenergic pathways in the expression of opiate withdrawal: biochemical and pharmacological evidence. Neurosci Biobehav Rev 21:91-104.
35. McGaugh JL, Baratti CM (1985). Pharmacological evidence of a central effect of naltrexone, morphine, and beta-endorphin and a peripheral effect of met- and leu-enkephalin on retention of an inhibitory response in mice. Behav Neural Biol 44:434-446.
36. McGaugh JL, Cahill (1997). Interaction of neuromodulatory systems in modulating memory storage. Behav Brain Res 83:31-38.
37. McGaugh JL, Cahill L, Roozendaal B (1996). Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci USA 93:13508-13514.
38. McIntyre CK, Pal S, Marriot LK, Gold PE (2002). Competition between memory systems: acetylcholine release in the hippocampus correlates negatively with good performance on an amygdala-dependent task. J Neurosci 22:1171-1176.
39. Meyer DR, Sparber SB (1976). A comparison of withdrawal in rats implanted with different types of morphine pellets. Pharmacol Biochem Behav 5:603-607.
40. Mizoguchi K, Yuzurihara M, Ishige A, Sasaki H, Tabira T (2001). Effect of chronic stress on cholinergic transmission in rat hippocampus. Brain Res 915:108-111.
41. Morales L, Perez-Garcia C, Alguacil LF (2001). Effects of yohimbine on the antinociceptive and place conditioning effects of opioid agonists in rodents. Br J Pharmacol 133:172-178.
42. Nishimura M, Shiigi Y, Kaneto H (1990). State dependent and/or direct memory retrieval by morphine in mice. Psychopharmacology 100:27-30.
43. Ossipov MH, Suarez U, Spaulding TC (1989). Antinociceptive interactions between alpha-2 adrenergic and opiate agonists at the spinal level in rodents. Anesth Analg 68:194-200.
44. Paul D, Tran JG (1995). Differential cross-tolerance between analgesia produced by alpha 2-adrenoceptor agonists and receptor subtype selective opioid treatments. Eur J Pharmacol 272:111-114.
45. Pavone F, Castellano C, Oliverio A (1986). Strain-dependent effects of shock-induced release of opioids: dissociation between analgesia and behavioral seizures. Brain Res 366:326-328.
46. Quirarte GL, Galvez R, Roozendaal B, McGaugh JL (1998). Nerephinephrine release in the amygdala in response to footshock and opioid peptidergic drugs. Brain Res 808:134-140.
47. Ragozzino ME, Gold PE (1994). Task-dependent effects of intra-amygdala morphine injections: attenuation by intra-amygdala glucose injections. J Neurosci 14:7478-7485.
48. Ragozzino ME, Wenk GL, Gold PE (1994). Glucose attenuates a morphine-induced decrease in hippocampal acetylcholine output: an in vivo micro-dialysis study in rats. Brain Res 655:77-82.
49. Roerig SC, Sizheng L, Kitto K, Hylden JKL, Wilcox GL (1992). Spinal interactions between opioid and noradrenergic agonists in mice: multiplicity involves delta and alpha-2 receptors. J Pharmacol Exp Ther 262:365-374.
50. Saha N, Datta H, Sharma PL (1991). Effects of morphine on memory: interactions with naloxone, propranolol and haloperidol. Pharmacology 42:10-14.
51. Schulteis G, Martinez JL Jr (1992). Peripheral modulation of learning and memory: enkephalins as a model system. Psychopharmacology 109:347-364.
52. Shulz DE, Sosnik R, Ego V, Haidarliu S, Ahissar E (2000). A neuronal analogue of state-dependent learning. Nature 403:549-552.
53. Siegfried B, Frischknecht HR (1989). Place avoidance learning and stress-induced analgesia in the attacked mouse: role of endogenous opioids. Behav Neural Biol 52:95-107.
54. Sirvio J, MacDonald E (1999). Central alpha 1-adrenoceptors: their role in the modulation of attention and memory formation. Pharmacol Ther 83:49-65.
55. Sternberg DB, Isaacs KR, Gold PE, McGaugh JL (1985). Epinephrine facilitation of appetitive learning: attenuation with adrenergic receptor antagonists. Behav Neural Biol 44:447-453.
56. Stillman MJ, Shukitt-Hale B, Levy A, Liberman HR (1998). Spatial memory under acute cold and restraint stress. Physiol Behav 64:605-609.
57. Svensson TH (1987). Stress, central neurotransmitters, and the mechanism of action of alpha 2-adrenoceptor agonists. J Cardiovasr Pharmacol 10:S88-S92.
58. Svensson TH, Bunney BS, Aghajanian G K (1975). Inhibition of both noradrenergic and serotonergic neurons in brain by the α-adrenergic agonist clonidine. Brain Res 92:291-306.
59. Talley C P, Arankowsky-Sandoval G, McCarty R, Gold PE (1999). Attenuation of morphine-induced behavioral changes in rodents by D- and L-glucose. Neurobiol Learn Mem 71:62-79.
60. 1-opioid receptors and cholinergic neurotransmission in the endomorphine-induced impairment of passive avoidance learning in mice. Behav Brain Res 129:197-201.
61. Vaccarino AL, Olson GA, Olson RD, Kastin AJ (1999). Endogenous opiates: 1998. Peptides 20:1527-1574.
62. Zarrindast MR, Fazli-Tabai S, Semnanian S, Fathollahi Y (1999). Influence of different adrenoceptor agonists and antagonists on physostigmine-induced yawning in rats. Pharmacol Biochem Behav 62:1-5.
63. Zarrindast MR, Homayoun H, Babaie A, Etminani A, Gharib B (2000). Involvement of adrenergic and cholinergic systems in nicotine-induced anxiogenesis in mice. Eur J Pharmacol 407:145-158.
64. Zarrindast MR, Homayoun H, Khavandgar S, Fayaz-Dastgerdi M, Fayaz-Dastgerdi M (2002). The effects of simultaneous administration of alpha2-adrenergic agents with L-NAME or L-arginine on the development and expression of morphine dependence in mice. Behav Pharmacol 13:117-125.