Chapter 6.2 Involvement of the amygdala in the neuroendocrine and behavioral consequences of stress

Techniques in the Behavioral and Neural Sciences

Volumn 15, Issue PART 1, 2005, Pages 793-805

  Akirav, Irit ^a   Richter Levin, Gal ^a  

^a UNIVERSITY OF HAIFA   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 70349899048     PISSN: 09210709     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0921-0709(05)80042-2     Document Type: Chapter

References (128)

1. Adolphs R., Cahill L., Schul R., and Babinsky R. Impaired declarative memory for emotional material following bilateral amygdala damage in humans. Learn. Mem. 4 (1997) 291-300
2. Adolphs R., Tranel D., and Denburg N. Impaired emotional declarative memory following unilateral amygdala damage. Learn Mem. 73 (2000) 180-186
3. Akirav, I., Kozenicky, M., Tal, D., Sandi, C., Venero, C. and Richter-Levin, G. A facilitative role for corticosterone in the acquisition of a spatial task under moderate stress. Learn and Mem., in press.
4. Akirav I., and Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J. Neurosci. 1 (1999) 10530-10535
5. Akirav I., and Richter-Levin G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 15 (2002) 9912-9921
6. Akirav I., Sandi C., and Richter-Levin G. Differential activation of hippocampus and amygdala following spatial learning under stress. Eur. J. Neurosci. 14 (2001) 719-725
7. Alvarez P., Zola-Morgan S., and Squire L.R. Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J. Neurosci. 15 (1995) 3796-3807
8. Anderson C.R. Coping behaviors as intervening mechanisms in the inverted U stress-performance relationship. J. Appl. Psychol. 61 (1976) 30-34
9. Atkins C.M., Selcher J.C., Petraitis J.J., Trzaskos J.M., and Sweatt J.D. The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1 (1998) 602-609
10. Bartolomucci A., de Biurrun G., Czeh B., van Kampen M., and Fuchs E. Selective enhancement of spatial learning under chronic psychosocial stress. Eur. J. Neurosci. 15 (2002) 1863-1866
11. Bennett M.C., Diamond D.M., Fleshner M., and Rose G.M. Serum corticosterone level predicts the magnitude of hippocampal primed burst potentiation and depression in urethane-anesthetized rats. Psychobiol. 19 (1991) 301-307
12. Berman D.E., Hazvi S., Rosenblum K., Seger R., and Dudai Y. Specific and differential activation of mitogen-activated protein kinase cascades by unfamiliar taste in the insular cortex of the behaving rat. J. Neurosci. 1 (1998) 10037-10044
13. Bianchin M., Mello e Souza T., Medina J.H., and Izquierdo I. The amygdala is involved in the modulation of long-term memory, but not in working or short-term memory. Neurobiol. Learn. Mem. 71 (1999) 127-131
14. Bliss T.V.P., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
15. Blum S., Moore A.N., Adams F., and Dash P.K. A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J. Neurosci. 1 (1999) 3535-3544
16. Bohus B., De Kloet E.R., and Veldhuis H.D. Adrenal steroids and behavioral adaptation: relationship to brain corticoid receptors. In: Ganten D., and Pfaff D. (Eds). Current Topics in Neuroendocrinology: Adrenal Actions on Brain (1982), Springer, New York 107-148
17. Bunsey M., and Eichenbaum H. Conservation of hippocampal memory function in rats and humans. Nature 18 (1996) 255-257
18. Cahill L., and McGaugh J.L. Amygdaloid complex lesions differentially affect retention of tasks using appetitive and aversive reinforcement. Behav. Neurosci. 104 (1990) 532-543
19. Cahill L., and McGaugh J.L. Modulation of memory storage. Curr. Opin. Neurobiol. 6 (1996) 237-242
20. Cahill L., and McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21 (1998) 294-299
21. Cahill L., Prins B., Weber M., and McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 20 (1994) 702-704
22. Charney D.S., Deutch A.Y., Southwick S.M., and Krystal J.H. Neural circuits and mechanisms of post traumatic stress disorder. In: Freiedman M.J., Charney D.S., and Deutch A.Y. (Eds). Neurobiological and Clinical Consequences of Stress: from Normal Adaptation to PTSD (1995), Lipoincott-Raven publishers, Berlin 271-290
23. Chiba A.A., Kesner R.P., and Reynolds A.M. Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. Behav. Neural. Biol. 61 (1994) 123-131
24. Conrad C.D., Galea L.A., Kuroda Y., and McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 110 (1996) 1321-1334
25. Conrad C.D., Lupien S.J., and McEwen B.S. Support for a bimodal role for type II adrenal steroid receptors in spatial memory. Neurobiol. Learn. Mem. 72 (1999) 39-46
26. Conrad C.D., Lupien S.J., Thanasoulis L.C., and McEwen B.S. The effects of type I and type II corticosteroid receptor agonists on exploratory behavior and spatial memory in the Y-maze. Brain Res. 6 (1997) 76-83
27. Cordero M.I., and Sandi C. A role for brain glucocorticoid receptors in contextual fear conditioning: dependence upon training intensity. Brain Res. 9 (1998) 11-17
28. Davis M. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15 (1992) 353-375
29. Diamond D.M., Bennett M.C., Fleshner M., and Rose G.M. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2 (1992) 421-430
30. Diamond D.M., Fleshner M., Ingersoll N., and Rose G.M. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav. Neurosci. 110 (1996) 661-772
31. Diamond D.M., Fleshner M., and Rose G.M. Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats. Behav. Brain Res. 30 (1994) 1-9
32. Diamond D.M., and Park C.R. Predator exposure produces retrograde amnesia and blocks synaptic plasticity. Progress toward understanding how the hippocampus is affected by stress. Ann. NY Acad. Sci. USA 911 (2000) 453-455
33. Diamond D.M., Park C.R., Heman K.L., and Rose G.M. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus. 9 (1999) 542-552
34. Diamond D.M., Park C.R., Puls M.J., and Rose G.M. Differential effects of stress on hippocampal and amygdaloid LTP. In: Holscher C. (Ed). Neuronal Mechanism of Memory Formation (2001), Cambridge UP, Philadelphia 379-403
35. Diamond D.M., and Rose G.M. Stress impairs LTP and hippocampal-dependent memory. Ann. NY Acad. Sci. 30 (1994) 411-414
36. Dunn L.T., and Everitt B.J. Double dissociations of the effects of amygdala and insular cortex lesions on conditioned taste aversion, passive avoidance, and neophobia in the rat using the excitotoxin ibotenic acid. Behav. Neurosci. 102 (1988) 3-23
37. Easterbrook J.A. The effect of emotion on cue utilization and the organization of behavior. Psychol. Rev. 66 (1959) 183-201
38. Eichenbaum H. The hippocampal formation and declarative memory in animals. J. Cog. Neurosci. 4 (1992) 217-231
39. Eichenbaum H. The hippocampus and mechanisms of declarative memory. Behav. Brain Res. 103 (1999) 123-133
40. Ferry B., and McGaugh J.L. Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiol. Learn. Mem. 72 (1999) 8-12
41. Flood J.F., Vidal D., Bennett E.L., Orme A.E., Vasquez S., and Jarvik M.E. Memory facilitating and antiamnesic effects of corticosteroids. Pharmacol. Biochem. Behav. 8 (1978) 81-87
42. Gold P.E., and van Buskirk R. Facilitation of time-dependent memory processes with posttrail epinephrine injections. Behav. Biol. 13 (1975) 145-153
43. Gold P.E., Delanoy R.L., and Merrin J. Modulation of long-term potentiation by peripherally administered amphetamine and epinephrine. Brain Res. 2 (1984) 103-107
44. Gold P.E., Hankins L., Edwards R.M., Chester J., and McGaugh J.L. Memory interference and facilitation with posttrial amygdala stimulation: effect on memory varies with footshock level. Brain Res. 28 (1975) 509-513
45. Gold P.E., and McGaugh J.L. A single-trace, two process view of memory storage processes. In: Deutsch D., and Deutsch J.A. (Eds). Short-term Memory (1975), Academic Press, UK 355-378
46. Hall J., Thomas K.L., and Everitt B.J. Fear memory retrieval induces CREB phosphorylation and Fos expression within the amygdala. Eur. J. Neurosci. 13 (2001) 1453-1458
47. Hamann S.B., Cahill L., McGaugh J.L., and Squire L.R. Intact enhancement of declarative memory for emotional material in amnesia. Learn Mem. 4 (1997) 301-309
48. Hamann S.B., Ely T.D., Grafton S.T., and Kilts C.D. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nat. Neurosci. 2 (1999) 289-293
49. Hatfield T., and McGaugh J.L. Norepinephrine infused into the basolateral amygdala posttraining enhances retention in a spatial water maze task. Neurobiol. Learn. Mem. 71 (1999) 232-239
50. Hitchcock J.M., and Davis M. Fear-potentiated startle using an auditory conditioned stimulus: effect of lesions of the amygdala. Physiol. Behav. 39 (1987) 403-408
51. Introini-Collison I.B., and McGaugh J.L. Epinephrine modulates long-term retention of an aversively motivated discrimination. Behav. Neural Biol. 45 (1986) 358-365
52. Izquierdo I., and Dias R.D. Influence on memory of posttraining or pre-test injections of ACTH, vasopressin, epinephrine, and beta-endorphin, and their interaction with naloxone. Psychoneuroendocrinol. 10 (1985) 165-172
53. Jellestad F.K., and Bakke H.K. Passive avoidance after ibotenic acid and radio frequency lesions in the rat amygdala. Physiol. Behav. 34 (1985) 299-305
54. Kesner R.P., Hunt M.E., Williams J.M., and Long J.M. Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb Cortex. 6 (1996) 311-318
55. Kim J.J., and Diamond D.M. The stressed hippocampus, synaptic plasticity and lost memories. Nat. Rev. Neurosci. 3 (2002) 453-462
56. Kim J.J., Foy M.R., and Thompson R.F. Behavioral stress modifies hippocampal plasticity through NMDA receptor activation. Proc. Natl. Acad. Sci. USA 93 (1996) 4750-4753
57. Kim J.J., Lee H.J., Han J.S., and Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J. Neurosci. 15 (2001) 5222-5228
58. de Kloet E.R., Grootendorst J., Karssen A.M., and Oitzl M.S. Gene x environment interaction and cognitive performance: animal studies on the role of corticosterone. Neurobiol. Learn Mem. 78 (2002) 570-577
59. de Kloet E.R., Oitzl M.S., and Joels M. Stress and cognition: are corticosteroids good or bad guys?. Trends Neurosci. 22 (1999) 422-426
60. de Kloet E.R., Reul J.M., and Sutanto W. Corticosteroids and the brain. J. Steroid. Biochem. Mol. Biol. 20 (1990) 387-394
61. de Kloet E.R., Vreugdenhil E., Oitzl M.S., and Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 (1998) 269-301
62. Van der Kolk B.A. The psychobiology of posttraumatic stress disorder. J. Clin. Psychiatry 58 Suppl 9 (1997) 16-24
63. Layton B., and Krikorian R. Memory mechanisms in posttraumatic stress disorder. J. Neuropsychiatry Clin. Neurosci. 14 (2002) 254-261
64. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 23 (2000) 155-184
65. LeDoux J.E., Iwata J., Cicchetti P., and Reis D.J. Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear. J. Neurosci. 8 (1988) 2517-2529
66. Liang K.C., Juler R.G., and McGaugh J.L. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res. 12 (1986) 125-133
67. Liang K.C., McGaugh J.L., and Yao H.Y. Involvement of amygdala pathways in the influence of posttraining intra-amygdala norepinephrine and peripheral epinephrine on memory storage. Brain Res. 5 (1990) 225-233
68. Liu L., Tsuji M., Takeda H., Takada K., and Matsumiya T. Adrenocortical suppression blocks the enhancement of memory storage produced by exposure to psychological stress in rats. Brain Res. 6 (1999) 134-140
69. Lupien S.J., and McEwen B.S. The acute effect of corticosteroids on cognition: integration of animal and human model studies. Brain Res. Rev. 24 (1997) 1-27
70. Maguire E.A., Burgess N., and O'Keefe J. Human spatial navigation: cognitive maps, sexual dimorphism, and neural substrates. Curr. Opin. Neurobiol. 9 (1999) 171-177
71. Martin S.J., Grimwood P.D., and Morris R.G. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23 (2000) 649-711
72. McEwen B.S. Stressful experience, brain, and emotions: developmental, genetic, and hormonal influences. In: Gazzagnia M. (Ed). The Cognitive Neurosciences (1995), MIT Press, NY 1117-1135
73. McEwen B.S., De Kloet E.R., and Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol. Rev. 66 (1986) 1121-1188
74. McGaugh J.L. Memory-a century of consolidation. Science 14 (2000) 248-251
75. McGaugh J.L. Memory consolidation and the amygdala: a systems perspective. Trends Neurosci. 25 (2000) 456
76. McGaugh J.L., Cahill L., and Roozendaal B. Involvement of the amygdala in memory storage: interaction with other brain systems. Proc. Natl. Acad. Sci. USA 26 (1996) 13508-13514
77. McGaugh J.L., Introini-Collison I.B., Nagahara A.H., Cahill L., Brioni J.D., and Castellano C. Involvement of the amygdaloid complex in neuromodulatory influences on memory storage. Neurosci. Biobehav. Rev. 14 (1990) 425-431
78. McGaugh J.L., McIntyre C.K., and Power A.E. Amygdala modulation of memory consolidation: interaction with other brain systems. Neurobiol. Learn. Mem. 78 (2002) 539-552
79. McGaugh J.L., and Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr. Opin. Neurobiol. 12 (2002) 205-210
80. McKernan M.G., and Shinnick-Gallagher P. Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390 (1997) 607-611
81. Morris R.G., Garrud P., Rawlins J.N., and O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 24 (1982) 681-683
82. Moser E., Moser M.B., and Andersen P. Spatial learning impairment parallels the magnitude of dorsal hippocampal lesions, but is hardly present following ventral lesions. J. Neurosci. 13 (1993) 3916-3925
83. Oitzl M.S., Fluttert M., Sutanto W., and de Kloet E.R. Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur. J. Neurosci. 10 (1998) 3759-3766
84. Oitzl M.S., Fluttert M., and de Kloet E.R. The effect of corticosterone on reactivity to spatial novelty is mediated by central mineralocorticosteroid receptors. Eur. J. Neurosci. 1 (1994) 1072-1079
85. Oitzl M.S., van Haarst A.D., and de Kloet E.R. Behavioral and neuroendocrine responses controlled by the concerted action of central mineralocorticoid (MRS) and glucocorticoid receptors (GRS). Psychoneuroendocrinology 22 (1997) S87-S93
86. Oitzl M.S., and de Kloet E.R. Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106 (1992) 62-71
87. O'Keefe J. Do hippocampal pyramidal cells signal nonspatial as well as spatial information?. Hippocampus 9 (1999) 352-364
88. Packard M.G., and Cahill L. Affective modulation of multiple memory systems. Curr. Opin. Neurobiol. 11 (2001) 752-756
89. Packard M.G., Cahill L., and McGaugh J.L. Amygdala modulation of hippocampal-dependent and caudate nucleus-dependent memory processes. Proc. Natl. Acad. Sci. USA 30 (1994) 8477-8481
90. Packard M.G., and Chen S.A. The basolateral amygdala is a co-factor in memory enhancement produced by intra-hippocampal glutamate injections. Psychobiol. 27 (1999) 377-385
91. Packard M.G., and Teather L.A. Amygdala modulation of multiple memory systems: hippocampus and caudate-putamen. Neurobiol. Learn. Mem. 69 (1998) 163-203
92. Pare D. Role of the basolateral amygdala in memory consolidation. Prog. Neurobiol. 70 (2003) 409-420
93. Pavlides C., Nivon L.G., and McEwen B.S. Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12 (2000) 245-257
94. Pavlides C., Watanabe Y., and McEwen B.S. Effects of glucocorticoids on hippocampal long-term potentiation. Hippocampus 3 (1993) 183-192
95. Phelps E.A., and Anderson A.K. Emotional memory: what does the amygdala do?. Curr. Biol. 1 (1997) R311-R314
96. Pikkarainen M., Ronkko S., Savander V., Insausti R., and Pitkanen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 11 (1999) 229-260
97. Pugh C.R., Tremblay D., Fleshner M., and Rudy J.W. A selective role for corticosterone in contextual-fear conditioning. Behav. Neurosci. 111 (1997) 503-511
98. de Quervain D.J., Roozendaal B., and McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 20 (1998) 787-790
99. Radwanska K., Nikolaev E., Knapska E., and Kaczmarek L. Differential response of two subdivisions of lateral amygdala to aversive conditioning as revealed by c-Fos and P-ERK mapping. Neuroreport 3 (2002) 2241-2246
100. Ressler K.J., Paschall G., Zhou X.L., and Davis M. Regulation of synaptic plasticity genes during consolidation of fear conditioning. J. Neurosci. 15 (2002) 7892-7902
101. Rey M., Carlier E., Talmi M., and Soumireu-Mourat B. Corticosterone effects on long-term potentiation in mouse hippocampal slices. Neuroendocrinol. 60 (1994) 36-41
102. Richter-Levin G., and Akirav I. Amygdala-hippocampus dynamic interaction in relation to memory. Mol. Neurobiol. 22 (2000) 11-20
103. Richter-Levin G., and Akirav I. Emotional tagging of memory formation-in the search for neural mechanisms. Brain Res. Rev. 43 (2003) 247-256
104. Rogan M.T., Staubli U.V., and LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390 (1997) 604-607
105. Roozendaal B. Glucocorticoids and the regulation of memory consolidation. Psychoneuroendocrinol 25 (2000) 213-238
106. Roozendaal B., Griffith Q.K., Buranday J., De Quervain D.J., and McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. USA 4 (2003) 1328-1333
107. Roozendaal B., and McGaugh J.L. Amygdaloid nuclei lesions differentially affect glucocorticoid-induced memory enhancement in an inhibitory avoidance task. Neurobiol. Learn. Mem. 65 (1996) 1-8
108. Roozendaal B., and McGaugh J.L. Basolateral amygdala lesions block the memory-enhancing effect of glucocorticoid administration in the dorsal hippocampus of rats. Eur. J. Neurosci. 9 (1997) 76-83
109. Roozendaal B., Nguyen B.T., Power A.E., and McGaugh J.L. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc. Natl. Acad. Sci. USA 28 (1999) 11642-11647
110. Roozendaal B., Portillo-Marquez G., and McGaugh J.L. Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. Behav. Neurosci. 110 (1996) 1074-1083
111. Roozendaal B., Sapolsky R.M., and McGaugh J.L. Basolateral amygdala lesions block the disruptive effects of long-term adrenalectomy on spatial memory. Neurosci. 84 (1998) 453-465
112. Sandi C., Loscertales M., and Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 9 (1997) 637-642
113. Sandi C., and Rose S.P. Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm. Brain Res. 30 (1994) 106-112
114. Sandi C., and Rose S.P. Corticosteroid receptor antagonists are amnestic for passive avoidance learning in day-old chicks. Eur. J. Neurosci. 1 (1994) 1292-1297
115. Schafe G.E., Atkins C.M., Swank M.W., Bauer E.P., Sweatt J.D., and LeDoux J.E. Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J. Neurosci. 1 (2000) 8177-8187
116. Seidenbecher T., Reymann K.G., and Balschun D. A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc. Natl. Acad. Sci. USA 18 (1997) 1494-1499
117. Selcher J.C., Atkins C.M., Trzaskos J.M., Paylor R., and Sweatt J.D. A necessity for MAP kinase activation in mammalian spatial learning. Learn. Mem. 6 (1999) 470-478
118. Selden N.R., Cole B.J., Everitt B.J., and Robbins T.W. Damage to ceruleo-cortical noradrenergic projections impairs locally cued but enhances spatially cued water maze acquisition. Behav. Brain Res. 18 (1990) 29-51
119. Shors T.J., Foy M.R., Levine S., and Thompson R.F. Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus. Brain Res. Bull. 24 (1990) 663-667
120. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99 (1992) 195-231
121. Squire L.R. Memory systems. C. R. Acad. Sci. III 321 (1998) 153-156
122. Stork O., Stork S., Pape H.C., and Obata K. Identification of genes expressed in the amygdala during the formation of fear memory. Learn. Mem. 8 (2001) 209-219
123. Vaher P.R., Luine V.N., Gould E., and McEwen B.S. Effects of adrenalectomy on spatial memory performance and dentate gyrus morphology. Brain Res. 5 (1994) 71-78
124. Vroom V.H. Work and Motivation (1964), Wiley, Cambridge, MA
125. Yaniv D., Schafe G.E., LeDoux J.E., and Richter-Levin G. A gradient of plasticity in the amygdala revealed by cortical and subcortical stimulation, in vivo. Neuroscience 106 (2001) 613-620
126. Yau J.L., Olsson T., Morris R.G., Meaney M.J., and Seckl J.R. Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats. Neuroscience 66 (1995) 571-581
127. de Wied D., and Croiset G. Stress modulation of learning and memory processes. Methods Achiev. Exp. Pathol. 15 (1991) 167-199
128. Wang J., Akirav I., and Richter-Levin G. Short-term behavioral and electrophysiological consequences of underwater trauma. Physiol. Behav. 70 (2000) 327-332