Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning

Behavioral Neuroscience

Volumn 110, Issue 5, 1996, Pages 1074-1083

  Roozendaal, Benno ^a   Portillo Marquez, Grace ^a   McGaugh, James L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEXAMETHASONE; GLUCOCORTICOID;

ADRENALECTOMY; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; LEARNING; MALE; MEMORY CONSOLIDATION; NONHUMAN; RAT; SPATIAL MEMORY;

ADRENALECTOMY; AMYGDALA; ANIMALS; BRAIN MAPPING; CORTICOSTERONE; DEXAMETHASONE; GLUCOCORTICOIDS; INJECTIONS, INTRAVENTRICULAR; MALE; MAZE LEARNING; MENTAL RECALL; ORIENTATION; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0029992567     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.110.5.1074     Document Type: Article

References (65)

1. Allen, J. P., & Allen, C. F. (1974). Role of the amygdaloid complexes in the stress-induced release of ACTH in the rat. Neuroendocrinology, 15, 220-230.
2. Arriza, J. L, Simerly, R. B., Swanson, L. W., & Evans, R. M. (1988). The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. Neuron, 1, 887-900.
3. Beaulieu, S., DiPaolo, T., & Barden, N. (1986). Control of ACTH secretion by the central nucleus of the amygdala: Implications of the serotoninergic system and its relevance to the glucocorticoid delayed negative feedback system. Neuroendocrinology, 44, 247-254.
4. Bohus, B. (1994). Humoral modulation of learning and memory processes: Physiological significance of brain and peripheral mechanisms. In J. Delacour (Ed.), The memory system of the brain: Advanced series in neuroscience (Vol. 4, pp. 337-364). Singapore: World Scientific.
5. Bohus, B., & de Kloet, E. R. (1981). Adrenal steroids and extinction behavior: Antagonism by progesterone, deoxycorticosterone and dexamethasone of a specific corticosterone effect. Life Science, 28, 433-440.
6. Cahill, L., & McGaugh, J. L. (1990). Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behavioral Neuroscience, 104, 532-543.
7. Conrad, C. D., & Roy, E. J. (1995). Dentate gyrus destruction and spatial learning impairment after corticosteroid removal in young and middle-aged rats. Hippocampus, 5, 1-15.
8. Corodimas, K. P., LeDoux, J. E., Gold, P. W., & Schulkin, J. (1994). Corticosterone potentiation of conditioned fear in rats. In E. R. de Kloet, E. C. Azmitia, & P. W. Landfield (Eds.), Annals of the New York Academy of Sciences: Vol. 746. Brain corticosteroid receptors: Studies on the mechanism, function, and neurotoxicity of corticosteroid action (pp. 392-393), New York: New York Academy of Sciences.
9. Cottrell, G. A., & Nakajima, S. (1977). Effect of corticosteroids in the hippocampus on passive avoidance behavior in the rat. Pharmacology, Biochemistry and Behavior, 7, 277-280.
10. de Boer, S. F., Koopmans, S. J., Slangen, J. L., & van der Gugten, J. (1990). Plasma catecholamine, corticosterone and glucose responses to repeated stress in rats: Effect of interstressor interval length. Physiology & Behavior, 47, 1117-1124.
11. de Kloet, E. R. (1991). Brain corticosteroid receptor balance and homeostatic control. Frontiers in Neuroendocrinology 12, 95-164.
12. de Kloet, E. R., Kovacs, G. L., Szabo, G., Telegdy, G., Bohus, B., & Versteeg, D. H. G. (1982). Decreased serotonin turnover in the dorsal hippocampus of rat brain shortly after adrenalectomy: Selective normalization after corticosterone substitution. Brain Research, 239, 659-663.
13. Evans, R. M., & Arriza, J. L. (1989). A molecular framework for the actions of glucocorticoid hormones in the nervous system. Neuron, 2, 1105-1112.
14. Feldman, S., Conforti, N., & Saphier, D. (1990). The preoptic area and bed nucleus of the stria terminalis are involved in the effects of the amygdala on adrenocortical secretion. Neuroscience, 37, 775-779.
15. Flood, J. F., Vidal, D., Bennett, E. L., Orme, A. E. Vasquez, S., & Jarvik, M. E. (1978). Memory facilitating and anti-amnestic effects of corticosteroids. Pharmacology, Biochemistry and Behavior, 8, 81-87.
16. Fuxe, K., Wikström, A. C., Okret, S., Agnati, L. F., Härfstrand, A., Yu, Z. Y., Granholm, L., Zoli, M., Vale, W., & Gustafsson, J. Å. (1985). Mapping of glucocorticoid receptor immunoreactive neurons in the rat telen diencephalon using a monoclonal antibody against rat liver glucocorticoid receptors. Endocrinology, 117, 1803-1812.
17. Härfstrand, A., Fuxe, K., Cintra, A., Agnati, L. F., Zini, I., Wikström, A. C., Okret, S., Yu, Z. Y., Goldstein, M., Steinbusch, H., Verhofstad, A., & Gustafsson, J.-Å. (1986). Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proceedings of the National Academy of Sciences,. 83, 9779-9783.
18. Herman, J. P., Patel, P. D., Akil, H., & Watson, S. J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Molecular Endocrinology 3, 1886-1894.
19. Hitchcock, J. M., Sananes, C. B., & Davis, M. (1989). Sensitization of the startle reflex by footshock: Blockade by lesions of the central nucleus of the amygdala or its efferent pathway to the brainstem. Behavioral Neuroscience, 103, 509-518.
20. Honkaniemi, J., Pelto-Huikko, M., Rechardt, L., Isola, J., Lammi, A., Fuxe, K., Gustafsson, J. A., Wikström, A. C., & Hökfelt, T. (1992). Colocalization of peptide and glucocorticoid receptor immunoreactivities in the rat central amygdaloid nucleus. Neuroendocrinology, 55, 451-459.
21. Ikegaya, Y., Saito, H., & Abe, K. (1994). Attenuated hippocampal long-term potentiation in basolateral amygdala-lesioned rats. Brain Research, 656, 157-174.
22. Introini-Collison, I. B., Miyazaki, B., & McGaugh, J. L. (1991). Involvement of the amygdala in the memory-enhancing effects of clenbuterol. Psychopharmacology, 104, 541-544.
23. Joëls, M., & de Kloet, E. R. (1992). Control of neuronal excitability by corticosteroid hormones. Trends in Neurosciences, 15, 25-30.
24. Kesner, R. P. (1992). Learning and memory in rats with an emphasis on the role of the amygdala. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 379-399). New York: Wiley-Liss.
25. Korte, S. M., de Boer, S. F., de Kloet, E. R., & Bohus, B. (1995). Anxiolytic-like effects of selective mineralocorticoid and glucocorticoid antagonists on fear-enhanced behavior in the elevated plusmaze. Psychoneuroendocrinology, 20, 385-394.
26. LeDoux, J. E. (1995). Emotion: Clues from the brain. Annual Reviews in Psychology, 46, 209-235.
27. Lee, Y., Schulkin, J., & Davis, M. (1994). Effects of corticosterone on the enhancement of the acoustic startle reflex by corticotropin releasing factor (CRF). Brain Research, 666, 93-98.
28. Liang, K. C., Juler, R. G., & McGaugh, J. L. (1986). Modulating effects of posttraining epinephrine on memory: Involvement of the amygdala noradrenergic system. Brain Research, 368, 125-133.
29. Liang, K. C., McGaugh, J. L., & Yao, H.-Y. (1990). Involvement of amygdala pathways in the influence of post-training intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Research, 508, 225-233.
30. McEwen, B. S., & Sapolsky, R. M. (1995). Stress and cognitive function. Current Opinion in Neurobiology, 5, 205-216.
31. McGaugh, J. L., Introini-Collison, I. B., Cahill, L., Kim, M., & Liang, K. C. (1992). Involvement of the amygdala in neuromodulatory influences on memory storage. In J. P. Aggleton (Ed.), The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 431-451). New York: Wiley-Liss.
32. Mitchell, J. B., & Meaney, M. J. (1991). Effects of corticosterone on response consolidation and retrieval in the forced swim test. Behavioral Neuroscience, 105, 798-803.
33. Morris, R. G. M., Garrud, P., Rawlins, J. N. P., & O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297, 681-683.
34. Moser, E., Moser, M.-B., & Andersen, P. (1993). Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. Journal of Neuroscience, 13, 3916-3925.
35. Oitzl, M. S., & de Kloet, E. R. (1992). Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behavioral Neuroscience, 106, 62-71.
36. Olton, D. S., Becker, J. T., & Handelmann, G. E. (1979). Hippocampus, space and memory. Behavioral and Brain Sciences, 2, 313-365.
37. Olton, D. S., Walker, J. A., & Wolf, W. A. (1982). A disconnection analysis of hippocampal function. Brain Research, 233, 241-253.
38. Packard, M. G., Cahill, L., & McGaugh, J. L. (1994). Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proceedings of the National Academy of Sciences, 91, 8477-8481.
39. Packard, M. G., Williams, C. L., Cahill, L., & McGaugh, J. L. (1995). The anatomy of a memory modulatory system: From periphery to brain. In N. E. Spear, L. P. Spear, & M. L. Woodruff (Eds.), Neurobehavioral plasticity: Learning, development, and response to brain insults (pp. 149-184). Hillsdale, NJ: Erlbaum.
40. Parent, M. B., & McGaugh, J. L. (1994). Posttraining infusion of lidocaine into the amygdala basolateral complex impairs retention of inhibitory avoidance training. Brain Research, 661, 97-103.
41. Paxinos, G., & Watson, C. (1986). The rat brain in stereotaxic coordinates (2nd ed.). San Diego, CA: Academic Press.
42. Pavlides, C., Kimura, A., Magarinos, A. M., & McEwen, B. S. (1994). Type I adrenal steroid receptors prolong hippocampal long-term potentiation. Neuroreport, 20, 2673-2677.
43. Perroteau, I., Netchitailo, P., Delarue, C., Leboulenger, F., Philibert, D., Deraedt, R., & Vaudry, H. (1984). The effect of the antimineralocorticoid RU 28318 on aldosterone biosynthesis in vitro. Journal of Steroid Biochemistry, 20, 853-856.
44. Philibert, D., Costerousse, G., Gaillard-Moguilewsky, M., Nedelec, L., Nique, F., Tournemine, C., & Teutsch, G. (1991). From RU 38486 towards dissociated antiglucocorticoid and antiprogesterone. In M. K. Agarwal (Ed.), Antihormones in health and disease: Frontiers in Hormonal Research (pp. 1-17). Basel, Switzerland: Karger.
45. Racine, R. J., Mingram, N. W., & Hafner, S. (1983). Long-term potentiation phenomena in the rat limbic forebrain. Brain Research, 260, 915-922.
46. Reul, J. M. H. M., & de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: Microdistribution and differential occupation. Endocrinology, 117, 2505-2512.
47. Reul, J. M. H. M., de Kloet, E. R., van Sluys, F. J., Rijnberk, A., & Rothuizen, J. (1990). Binding characteristics of mineralocorticoid and glucocorticoid receptors in dog brain and pituitary. Endocrinology, 127, 907-915.
48. Roozendaal, B., Bohus, B., & McGaugh, J. L. (in press). Dose-dependent suppression of adrenocortical activity with metyrapone: Effects on emotion and memory. Psychoneuroendocrinology.
49. Roozendaal, B., Koolhaas, J. M., & Bohus, B. (1991). Attenuated cardiovascular, neuroendocrine, and behavioral responses after a single footshock in central amygdaloid lesioned male rats. Physiology and Behavior, 50, 771-775.
50. Roozendaal, B., Koolhaas, J. M., & Bohus, B. (1992). Central amygdaloid involvement in neuroendocrine correlates of conditioned stress responses. Journal of Neuroendocrinology, 4, 483-489.
51. Roozendaal, B., Koolhaas, J. M., & Bonus, B. (1993). The central amygdala is involved in conditioning but not in retention of active and passive shock avoidance in male rats. Behavioral and Neural Biology, 59, 143-149.
52. Roozendaal, B., Koolhaas, J. M., & Bohus, B. (1995). The central amygdala as integrator of cognition and physiological stress responses to ensure adaptation and coping. Manuscript submitted for publication.
53. Roozendaal, B., & McGaugh, J. L. (1996). Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiology of Learning and Memory, 65, 1-8.
54. Sandi, C., & Rose, S. P. R. (1994). Corticosterone enhances long-term potentiation in one day-old chicks trained in a weak passive avoidance learning paradigm. Brain Research, 647, 106-112.
55. Sarter, M., & Markowitsch, H. J. (1985). Involvement of the amygdala in learning and memory: A critical review, with emphasis on anatomical relations. Behavioral Neuroscience, 99, 342-380.
56. Silverman, R. W., Chang. A. S., & Russell, R. W. (1988). Measurement of activity in small animals using a microcomputer-controlled system. Behavior Research Methods, Instruments, and Computers, 20, 537-540.
57. Sloviter, R. S., Valiquette, G., Abrams, G. M., Ronk, E. C., Sollas, A. L., Paul, L. A., & Neubort, S. (1989, January 27). Selective loss of hippocampal granule cells in the mature rat brain after adrenalectomy. Science, 243, 535-538.
58. Sutanto, W., & de Kloet, E. R., (1987). Species-specificity of corticosteroid receptors in hamster and rat brains. Endocrinology, 121, 1405-1411.
59. Sutherland, R. J., & McDonald, R. J. (1990). Hippocampus, amygdala, and memory deficits in rats. Behavioral Brain Research, 37, 57-79.
60. Sutherland, R. J., Whishaw, I. Q., & Kolb, B. (1983). A behavioural analysis of spatial localization following electrolytic, kainate or colchicine-induced damage to the hippocampal formation in the rat. Behavioral Brain Research, 7, 133-153.
61. Thomas, S. R., Assaf, S. Y., & Iversen, S. D. (1984). Amygdaloid complex modulates neurotransmission from the entorhinal cortex to the dentate gyrus of the rat. Brain Research, 307, 363-365.
62. Tomaz, C., Dickinson-Anson, H., & McGaugh, J. L. (1992). Basolateral amygdala lesions block the diazepam-induced anterograde amnesia in an inhibitory avoidance task. Proceedings of the National Academy of Sciences, 89, 3615-3619.
63. Vaher, P. R., Luine, V. N., Gould, E., & McEwen, B. S. (1994). Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Research, 656, 71-78.
64. van Eekelen, J. A. M., Jiang, W., de Kloet, E. R., & Bohn, M. C. (1988). Distribution of the mineralocorticoid and the glucocorticoid receptor mRNAs in the rat hippocampus. Journal of Neuroscience Research, 21, 88-94.
65. Vochteloo, J. D., & Koolhaas, J. M. (1987). Medial amygdala lesions in male rats reduce aggressive behavior: Interference with experience. Physiology & Behavior, 41, 99-102.