Divergent short- and long-term effects of acute stress in object recognition memory are mediated by endogenous opioid system activation

Neurobiology of Learning and Memory

Volumn 106, Issue , 2013, Pages 185-192

  Nava Mesa, Mauricio O ^a,b   Lamprea, Marisol R ^a   Múnera, Alejandro ^a  

^a UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

Author keywords

Acute stress; Endogenous opioid system; Naltrexone; Object recognition memory; Retroactive interference

Indexed keywords

DYNORPHIN; KAPPA OPIATE RECEPTOR; NALTREXONE; OPIATE;

ACUTE STRESS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; HABITAT; HUMAN; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LONG TERM MEMORY; MALE; MEMORY; MEMORY DISORDER; NONHUMAN; OPIOD SYSTEM; PATTERN RECOGNITION; PHYSICAL ACTIVITY; RAT; RECOGNITION; SHORT TERM MEMORY; TASK PERFORMANCE;

1MG/KG NALTREXONE; 1MG/KG NALTREXONE PLUS NO-STRESS; 1MG/KG NALTREXONE PLUS STRESS; 3MG/KG NALTREXONE; 3MG/KG NALTREXONE PLUS NO-STRESS; 3MG/KG NALTREXONE PLUS STRESS; ACTH; ACUTE STRESS; ADRENOCORTICOTROPIC HORMONE; ANALYSIS OF VARIANCE; ANOVA; DI; DISCRIMINATION INDEX; ENDOGENOUS OPIOID SYSTEM; FAMILIAR OBJECT; FO; N1NS; N1S; N3NS; N3S; NAL 1; NAL 3; NALTREXONE; NO; NOVEL OBJECT; OBJECT RECOGNITION MEMORY; OBJECT RECOGNITION TASK; ORM; ORT; RETROACTIVE INTERFERENCE; RI; SALINE PLUS NO-STRESS; SALINE PLUS STRESS; SEM; SNS; SS; STANDARD ERROR OF THE MEAN; TFO; TIME SPENT EXPLORING THE FAMILIAR OBJECT; TIME SPENT EXPLORING THE NOVEL OBJECT; TNO; VEH; VEHICLE;

ANIMALS; MALE; MEMORY, LONG-TERM; MEMORY, SHORT-TERM; NALTREXONE; NARCOTIC ANTAGONISTS; OPIOID PEPTIDES; RATS; RATS, WISTAR; RECOGNITION (PSYCHOLOGY); RESTRAINT, PHYSICAL; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84884555706     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2013.09.002     Document Type: Article

References (64)

1. Aigner T.G., Mishkin M. Improved recognition memory in monkeys following naloxone administration. Psychopharmacology (Berl) 1988, 94(1):21-23.
2. Akil H., Madden J., Patrick R.L., Barchas J.D. Stress-induced increase in endogenous opiate peptides : Concurrent analgesia and its partial reversal by naloxone. Opiates and endogenous opioid peptides 1976, North Holland, Amsterdam. H.W. Kosterlitz (Ed.).
3. Baker K.B., Kim J.J. Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learning and Memory 2002, 9(2):58-65.
4. Bartko S.J., Cowell R.A., Winters B.D., Bussey T.J., Saksida L.M. Heightened susceptibility to interference in an animal model of amnesia: Impairment in encoding, storage, retrieval-or all three?. Neuropsychologia 2010, 48(10):2987-2997.
5. Bermudez-Rattoni F., Okuda S., Roozendaal B., McGaugh J.L. Insular cortex is involved in consolidation of object recognition memory. Learning and Memory 2005, 12(5):447-449.
6. Bienkowski P., Kostowski W., Koros E. Ethanol-reinforced behaviour in the rat: Effects of naltrexone. European Journal of Pharmacology 1999, 374(3):321-327.
7. Bodnar R.J. Endogenous opiates and behavior: 2011. Peptides 2012, 38(2):463-522.
8. Cardenas, F., Lamprea, M., & Morato, S. (2001). X-Plo-Rat: A free software for behavior recording. <>. http://scotty.ffclrp.usp.br.
9. Carey A.N., Lyons A.M., Shay C.F., Dunton O., McLaughlin J.P. Endogenous kappa opioid activation mediates stress-induced deficits in learning and memory. The Journal of Neuroscience 2009, 29(13):4293-4300.
10. Carrasco G.A., Van de Kar L.D. Neuroendocrine pharmacology of stress. European Journal of Pharmacology 2003, 463(1-3):235-272.
11. Celerier A., Pierard C., Rachbauer D., Sarrieau A., Beracochea D. Contextual and serial discriminations: A new learning paradigm to assess simultaneously the effects of acute stress on retrieval of flexible or stable information in mice. Learning and Memory 2004, 11(2):196-204.
12. Chaves M.L., Pezzin S., Jardim C.P., Izquierdo I. Diazepam inhibits retroactive interference of memory in humans: Pretreatment with naltrexone does not alter this effect. Brazilian Journal Of Medical and Biological Research 1990, 23(5):417-421.
13. Chen J.X., Li W., Zhao X., Yang J.X., Xu H.Y., Wang Z.F., et al. Changes of mRNA expression of enkephalin and prodynorphin in hippocampus of rats with chronic immobilization stress. World Journal of Gastroenterology 2004, 10(17):2547-2549.
14. Conrad C.D. The Relationship between Acute Glucocorticoid Levels and Hippocampal Function Depends Upon Task Aversiveness and Memory Processing Stage. Nonlinearity in Biology, Toxicology, Medicine 2005, 3(1):57-78.
15. Conrad C.D., Lupien S.J., McEwen B.S. Support for a bimodal role for Type II adrenal steroid receptors in spatial memory. Neurobiology of Learning and Memory 1999, 72(1):39-46.
16. Coventry T.L., Jessop D.S., Finn D.P., Crabb M.D., Kinoshita H., Harbuz M.S. Endomorphins and activation of the hypothalamo-pituitary-adrenal axis. The Journal of Endocrinology 2001, 169(1):185-193.
17. Daumas S., Betourne A., Halley H., Wolfer D.P., Lipp H.P., Lassalle J.M., et al. Transient activation of the CA3 Kappa opioid system in the dorsal hippocampus modulates complex memory processing in mice. Neurobiology of Learning and Memory 2007, 88(1):94-103.
18. de Quervain D.J., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394(6695):787-790.
19. Drolet G., Dumont E.C., Gosselin I., Kinkead R., Laforest S., Trottier J.F. Role of endogenous opioid system in the regulation of the stress response. Progress in Neuro-psychopharmacology and Biological Psychiatry 2001, 25(4):729-741.
20. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behavioural Brain Research 1988, 31(1):47-59.
21. Gallagher M., King R.A., Young N.B. Opiate antagonists improve spatial memory. Science 1983, 221(4614):975-976.
22. Hebb A.L., Zacharko R.M., Gauthier M., Trudel F., Laforest S., Drolet G. Brief exposure to predator odor and resultant anxiety enhances mesocorticolimbic activity and enkephalin expression in CD-1 mice. The European Journal of Neuroscience 2004, 20(9):2415-2429.
23. Ignar D.M., Kuhn C.M. Effects of specific mu and kappa opiate tolerance and abstinence on hypothalamo-pituitary-adrenal axis secretion in the rat. Journal of Pharmacology and Experimental Therapeutics 1990, 255(3):1287-1295.
24. Jamot L., Matthes H.W., Simonin F., Kieffer B.L., Roder J.C. Differential involvement of the mu and kappa opioid receptors in spatial learning. Genes, Brain, and Behavior 2003, 2(2):80-92.
25. Kart-Teke E., De Souza Silva M.A., Huston J.P., Dere E. Wistar rats show episodic-like memory for unique experiences. Neurobiology of Learning and Memory 2006, 85(2):173-182.
26. Katzen-Perez K.R., Jacobs D.W., Lincoln A., Ellis R.J. Opioid blockade improves human recognition memory following physiological arousal. Pharmacology Biochemistry and Behavior. 2001, 70(1):77-84.
27. Li S., Fan Y.X., Wang W., Tang Y.Y. Effects of acute restraint stress on different components of memory as assessed by object-recognition and object-location tasks in mice. Behavioural Brain Research 2012, 227(1):199-207.
28. Lupien S.J., McEwen B.S. The acute effects of corticosteroids on cognition: Integration of animal and human model studies. Brain Research. Brain Research Reviews 1997, 24(1):1-27.
29. Mansouri F.A., Motamedi F., Fathollahi Y. Chronic in vivo morphine administration facilitates primed-bursts-induced long-term potentiation of Schaffer collateral-CA1 synapses in hippocampal slices in vitro. Brain Research 1999, 815(2):419-423.
30. Marinelli P.W., Quirion R., Gianoulakis C. An in vivo profile of beta-endorphin release in the arcuate nucleus and nucleus accumbens following exposure to stress or alcohol. Neuroscience 2004, 127(3):777-784.
31. Martinez J.L., Rigter H. Endorphins alter acquisition and consolidation of an inhibitory avoidance response in rats. Neuroscience Letters 1980, 19(2):197-201.
32. Martins de Lima M.N., Presti-Torres J., Dornelles A., Bromberg E., Schroder N. Differential effects of low and high doses of topiramate on consolidation and retrieval of novel object recognition memory in rats. Epilepsy and Behavior 2007, 10(1):32-37.
33. McEwen B.S. The neurobiology of stress: From serendipity to clinical relevance. Brain Research 2000, 886(1-2):172-189.
34. McEwen B.S., Sapolsky R.M. Stress and cognitive function. Current Opinion in Neurobiology 1995, 5(2):205-216.
35. McGaugh J.L. Hormonal influences on memory. Annual Review of Psychology 1983, 34:297-323.
36. McLaughlin J.P., Marton-Popovici M., Chavkin C. Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. The Journal of Neuroscience 2003, 23(13):5674-5683.
37. Meilandt W.J., Barea-Rodriguez E., Harvey S.A., Martinez J.L. Role of hippocampal CA3 mu-opioid receptors in spatial learning and memory. The Journal of Neuroscience 2004, 24(12):2953-2962.
38. Messing R.B., Jensen R.A., Martinez J.L., Spiehler V.R., Vasquez B.J., Soumireu-Mourat B., et al. Naloxone enhancement of memory. Behavioral and Neural Biology 1979, 27(3):266-275.
39. Messing R.B., Jensen R.A., Vasquez B.J., Martínez J.L., Spiehler V.R., McGaugh J.L. Opiate Modulation of Memory. Endogenous Peptides and Learning and Memory Processes 1981, 431-443. Academic Press, New York. J.L. Martínez, R.A. Jensen, R.B. Messing, H. Rigter, J.L. McGaugh (Eds.).
40. Moreno C., Vivas O., Lamprea N.P., Lamprea M.R., Munera A., Troncoso J. Vibrissal paralysis unveils a preference for textural rather than positional novelty in the one-trial object recognition task in rats. Behavioural Brain Research 2010, 211(2):229-235.
41. Morris R.G. Distinctive computations and relevant associative processes: Hippocampal role in processing, retrieval, but not storage of allocentric spatial memory. Hippocampus 1991, 1(3):287-290.
42. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
43. Morris B.J., Johnston H.M. A role for hippocampal opioids in long-term functional plasticity. Trends in Neurosciences 1995, 18(8):350-355.
44. Morrow B.A., Roth R.H., Elsworth J.D. TMT, a predator odor, elevates mesoprefrontal dopamine metabolic activity and disrupts short-term working memory in the rat. Brain Research Bulletin 2000, 52(6):519-523.
45. Mousa S., Miller C.H., Couri D. Dexamethasone and stress-induced analgesia. Psychopharmacology (Berl) 1983, 79(2-3):199-202.
46. Mumby D.G., Tremblay A., Lecluse V., Lehmann H. Hippocampal damage and anterograde object-recognition in rats after long retention intervals. Hippocampus 2005, 15(8):1050-1056.
47. Okuda S., Roozendaal B., McGaugh J.L. Glucocorticoid effects on object recognition memory require training-associated emotional arousal. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(3):853-858.
48. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: Implications for stress-related disorders. Endocrine Reviews 2001, 22(4):502-548.
49. Pinheiro A.D., Wright D.C. Naloxone eliminates passive avoidance retention deficits produced by pretest exposure to novelty in rats. Behavioral and Neural Biology 1991, 55(3):270-288.
50. Rashidy-Pour A., Sadeghi H., Taherain A.A., Vafaei A.A., Fathollahi Y. The effects of acute restraint stress and dexamethasone on retrieval of long-term memory in rats: An interaction with opiate system. Behavioural Brain Research 2004, 154(1):193-198.
51. Rezvanfard M., Zarrindast M.R., Ownegh V. Systemic opioid receptor antagonism blocks swim stress-induced retention impairment independently from CA1 and BLA opioidergic pathways. Life Sciences 2011, 89(9-10):320-326.
52. Richardson D.K., Reynolds S.M., Cooper S.J., Berridge K.C. Endogenous opioids are necessary for benzodiazepine palatability enhancement: Naltrexone blocks diazepam-induced increase of sucrose-'liking'. Pharmacology, Biochemistry, and Behavior 2005, 81(3):657-663.
53. Roozendaal B. Stress and memory: Opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiology of Learning and Memory 2002, 78(3):578-595.
54. Roozendaal B., Okuda S., Van der Zee E.A., McGaugh J.L. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(17):6741-6746.
55. Sajadi A.A., Samaei S.A., Rashidy-Pour A. Blocking effects of intra-hippocampal naltrexone microinjections on glucocorticoid-induced impairment of spatial memory retrieval in rats. Neuropharmacology 2007, 52(2):347-354.
56. Sandin J., Nylander I., Georgieva J., Schott P.A., Ogren S.O., Terenius L. Hippocampal dynorphin B injections impair spatial learning in rats: A kappa-opioid receptor-mediated effect. Neuroscience 1998, 85(2):375-382.
57. Selden N.R., Everitt B.J., Jarrard L.E., Robbins T.W. Complementary roles for the amygdala and hippocampus in aversive conditioning to explicit and contextual cues. Neuroscience 1991, 42(2):335-350.
58. Shirayama Y., Ishida H., Iwata M., Hazama G.I., Kawahara R., Duman R.S. Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects. Journal of Neurochemistry 2004, 90(5):1258-1268.
59. Simmons M.L., Chavkin C. Endogenous opioid regulation of hippocampal function. International Review of Neurobiology 1996, 39:145-196.
60. Terman G.W., Wagner J.J., Chavkin C. Kappa opioids inhibit induction of long-term potentiation in the dentate gyrus of the guinea pig hippocampus. The Journal of Neuroscience 1994, 14(8):4740-4747.
61. Vargas-López, V., Torres-Berrio, A., González-Martínez, L., Múnera, A., & Lamprea, M. R. (2013). Acute restraint stress- or corticosterone-induced impaired performance in object recognition task is due to neophobia instead of retrieval impairment. Unpublished results.
62. Wagner J.J., Etemad L.R., Thompson A.M. Opioid-mediated facilitation of long-term depression in rat hippocampus. The Journal of Pharmacology and Experimental Therapeutics 2001, 296(3):776-781.
63. Winters B.D., Bussey T.J. Glutamate receptors in perirhinal cortex mediate encoding, retrieval, and consolidation of object recognition memory. The Journal of Neuroscience 2005, 25(17):4243-4251.
64. Zhao H., Xu H., Xu X. Effects of naloxone on the long-term potentiation of EPSPs from the pathway of Schaffer collateral to CA1 region of hippocampus in aged rats with declined memory. Brain Research 2004, 996(1):111-116.