Critical brain circuits at the intersection between stress and learning

Neuroscience and Biobehavioral Reviews

Volumn 34, Issue 8, 2010, Pages 1223-1233

  Bangasser, Debra A ^a   Shors, Tracey J ^b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

Amygdala; Associative learning; Bed nucleus of the stria terminalis; D cycloserine; Depression; Eyeblink conditioning; Hippocampus; Post traumatic stress disorder; Sex difference; Stress

Indexed keywords

AMPA RECEPTOR; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NERVE CELL ADHESION MOLECULE; NORADRENALIN; PROPRANOLOL; STRESS HORMONE;

AMYGDALOID NUCLEUS; BRAIN REGION; COGNITIVE DEFECT; DEPRESSION; DRUG MECHANISM; ENZYME ACTIVATION; GENERALIZED ANXIETY DISORDER; HIPPOCAMPUS; HORMONE ACTION; HORMONE RELEASE; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING; LIFE STRESS; LONG TERM POTENTIATION; MEMORY; MEMORY DISORDER; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; PERSONAL EXPERIENCE; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOTRAUMA; REVIEW; STIMULUS RESPONSE; STRIA TERMINALIS;

ANIMALS; BRAIN; HUMANS; LEARNING; MODELS, BIOLOGICAL; NEURAL PATHWAYS; STRESS, PSYCHOLOGICAL;

EID: 77954089168     PISSN: 01497634     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neubiorev.2010.02.002     Document Type: Review

References (146)

1. Aerni A., Traber R., Hock C., Roozendaal B., Schelling G., Papassotiropoulos A., Nitsch R.M., Schnyder U., de Quervain D.J. Low-dose cortisol for symptoms of posttraumatic stress disorder. Am. J. Psychiatry 2004, 161:1488-1490.
2. Aggleton J.P., Friedman D.P., Mishkin M. A comparison between the connections of the amygdala and hippocampus with the basal forebrain in the macaque. Exp. Brain Res. 1987, 67(3):556-568.
3. Anagnostaras S.G., Gale G.D., Fanselow M.S. Hippocampus and contextual fear conditioning: recent controversies and advances. Hippocampus 2001, 11(1):8-17.
4. Arnsten A.F. Catecholamine regulation of the prefrontal cortex. J. Psychopharmacol. 1997, 11:151-162.
5. Austin M.P., Mitchell P., Goodwin G.M. Cognitive deficits in depression: possible implications for functional neuropathology. Br. J. Psychiatry 2001, 178:200-206.
6. Bangasser D.A., Santollo J., Shors T.J. The bed nucleus of the stria terminalis is critically involved in enhancing associative learning after stressful experience. Behav. Neurosci. 2005, 119(6):1459-1466.
7. Bangasser D.A., Shors T.J. The hippocampus is necessary for enhancements and impairments of learning following stress. Nat. Neurosci. 2007, 10:1401-1403.
8. Bangasser D.A., Shors T.J. The bed nucleus of the stria terminalis modulates learning after stress in masculinized but not cycling females. J. Neurosci. 2008, 28:6383-6387.
9. Bangasser D.A., Waxler D.E., Santollo J., Shors T.J. Trace conditioning and the hippocampus: the importance of contiguity. J. Neurosci. 2006, 26(34):8702-8706.
10. Bemelmans K.J., Goekoop J.G., van Kempen G.M.J. Recall performance in acutely depressed patients and plasma cortisol. Biol. Psychiatry 1996, 39:750-752.
11. Berger T.W., Weikart C.L., Bassett J.L., Orr W.B. Lesions of the retrosplenial cortex produce deficits in reversal learning of the rabbit nictitating membrane response: implications for potential interactions between hippocampal and cerebellar brain systems. Behav. Neurosci. 1986, 100(6):802-809.
12. Beylin A.V., Gandhi C.C., Wood G.E., Talk A.C., Matzel L.D., Shors T.J. The role of the hippocampus in trace conditioning: temporal discontinuity or task difficulty?. Neurobiol. Learn. Mem. 2001, 76(3):447-461.
13. Beylin A.V., Shors T.J. Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Horm. Behav. 2003, 43(1):124-131.
14. Bisaz R., Conboy L., Sandi C. Learning under stress: a role for the neural cell adhesion molecule NCAM. Neurobiol. Learn. Mem. 2009, 91:333-342.
15. Buffalari D.M., Grace A.A. Noradrenergic modulation of basolateral amygdala neuronal activity: opposing influences of alpha-2 and beta receptor activation. J. Neurosci. 2007, 27:12358-12366.
16. Bukalo O., Fentrop N., Lee A.Y., Salmen B., Law J.W., Wotjak C.T., Schweizer M., Dityatev A., Schachner M. Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. J. Neurosci. 2004, 24:1565-1577.
17. Canteras N.S., Swanson L.W. Projections of the ventral subiculum to the amygdala, septum, and hypothalamus: a PHAL anterograde tract-tracing study in the rat. J. Comp. Neurol. 1992, 324(2):180-194.
18. Casada J.H., Dafny N. Restraint and stimulation of bed nucleus of the stria terminalis produce similar stress-like behaviors. Brain Res. Bull. 1991, 27(2):207-212.
19. Cerqueira J.J., Mailliet F., Almeida O.F., Jay T.M., Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J. Neurosci. 2007, 27:2781-2787.
20. Christian K.M., Thompson R.F. Neural substrates of eyeblink conditioning: acquisition and retention. Learn. Mem. Dec 2003, 10(6):427-455. [Review] [289 refs].
21. Conboy L., Sandi C. Stress at learning facilitates memory formation by regulating AMPA receptor trafficking through a glucocorticoid action. Neuropsychopharmacology 2009, 35(3):674-685.
22. Conrad C.D. Chronic stress-induced hippocampal vulnerability: the glucocorticoid vulnerability hypothesis. Rev. Neurosci. 2008, 19:395-411.
23. Conrad C.D., Galea L.A., Kuroda Y., McEwen B.S. Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. Behav. Neurosci. 1996, 110(6):1321-1334.
24. Conrad C.D., LeDoux J.E., Magarinos A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav. Neurosci. 1999, 113:902-913.
25. Cordero M.I., Kruyt N.D., Sandi C. Modulation of contextual fear conditioning by chronic stress in rats is related to individual differences in behavioral reactivity to novelty. Brain Res. 2003, 970:242-245.
26. Cordero M.I., Merino J.J., Sandi C. Correlational relationship between shock intensity and corticosterone secretion on the establishment and subsequent expression of contextual fear conditioning. Behav. Neurosci. 1998, 112:885-891.
27. Cordero M.I., Venero C., Kruyt N.D., Sandi C. Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm. Behav. 2003, 44:338-345.
28. Cullinan W.E., Herman J.P., Watson S.J. Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J. Comp. Neurol. 1993, 332(1):1-20.
29. Davis M. The role of the amygdala in emotional learning. Int. Rev. Neurobiol. 1994, 36:225-266. [Review] [205 refs].
30. Davis M., Shi C. The extended amygdala: are the central nucleus of the amygdala and the bed nucleus of the stria terminalis differentially involved in fear versus anxiety?. Ann. N. Y. Acad. Sci. 1999, 877:281-291. [Review] [40 refs].
31. Davis M., Walker D.L., Lee Y. Amygdala and bed nucleus of the stria terminalis: differential roles in fear and anxiety measured with the acoustic startle reflex. Philos. Trans. R. Soc. Lond. - Ser. B: Biol. Sci. 1997, 352(1362):1675-1687. [Review] [75 refs].
32. de Quervain D.J., Henke K., Aerni A., Treyer V., McGaugh J.L., Berthold T., Nitsch R.M., Buck A., Roozendaal B., Hock C. Glucocorticoid-induced impairment of declarative memory retrieval is associated with reduced blood flow in the medial temporal lobe. Eur. J. Neurosci. 2003, 17:1296-1302.
33. de Quervain D.J., Margraf J. Glucocorticoids for the treatment of post-traumatic stress disorder and phobias: a novel therapeutic approach. Eur. J. Pharmacol. 2008, 583:365-371.
34. del Abril A., Segovia S., Guillamon A. The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroids early after birth. Brain Res. 1987, 429(2):295-300.
35. Diamond D.M. Cognitive, endocrine and mechanistic perspectives on non-linear relationships between arousal and brain function. Nonlinearity Biol. Toxicol. Med. 2005, 3:1-7.
36. Diamond D.M., Park C.R., Heman K.L., Rose G.M. Exposing rats to a predator impairs spatial working memory in the radial arm water maze. Hippocampus 1999, 9(5):542-552.
37. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
38. Donley M.P., Schulkin J., Rosen J.B. Glucocorticoid receptor antagonism in the basolateral amygdala and ventral hippocampus interferes with long-term memory of contextual fear. Behav. Brain Res. 2005, 164:197-205.
39. Duncko R., Cornwell B., Cui L., Merikangas K.R., Grillon C. Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men. Learn. Mem. 2007, 14:329-335.
40. Egli R.E., Kash T.L., Choo K., Savchenko V., Matthews R.T., Blakely R.D., Winder D.G. Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropsychopharmacology 2005, 30:657-668.
41. 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. 1994, 108(1):210-212.
42. Ferry B., McGaugh J.L. Clenbuterol administration into the basolateral amygdala post-training enhances retention in an inhibitory avoidance task. Neurobiol. Learn. Mem. 1999, 72(1):8-12.
43. Ferry B., McGaugh J.L. Role of amygdala norepinephrine in mediating stress hormone regulation of memory storage. Acta Pharmacol. Sin. 2000, 21(6):481-493. [Review] [131 refs].
44. Gould E., Tanapat P. Stress and hippocampal neurogenesis. Biol. Psychiatry 1999, 46(11):1472-1479. [Review] [55 refs].
45. Gray T.S., Bingaman E.W. The amygdala: corticotropin-releasing factor, steroids, and stress. Crit. Rev. Neurobiol. 1996, 10:155-168.
46. Grillon C., Smith K., Haynos A., Nieman L.K. Deficits in hippocampus-mediated Pavlovian conditioning in endogenous hypercortisolism. Biol. Psychiatry 2004, 56:837-843.
47. Hains A.B., Arnsten A.F. Molecular mechanisms of stress-induced prefrontal cortical impairment: implications for mental illness. Learn. Mem. 2008, 15:551-564.
48. Han T.M., De Vries G.J. Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J. Neurobiol. 2003, 54(3):502-510.
49. Hofmann S.G., Meuret A.E., Smits J.A., Simon N.M., Pollack M.H., Eisenmenger K., Shiekh M., Otto M.W. Augmentation of exposure therapy with d-cycloserine for social anxiety disorder. Arch. Gen. Psychiatry 2006, 63:298-304.
50. Holstege G., Meiners L., Tan K. Projections of the bed nucleus of the stria terminalis to the mesencephalon, pons, and medulla oblongata in the cat. Exp. Brain Res. 1985, 58(2):379-391.
51. Howland J.G., Wang Y.T. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog. Brain Res. 2008, 169:145-158.
52. Jackson E.D., Payne J.D., Nadel L., Jacobs W.J. Stress differentially modulates fear conditioning in healthy men and women. Biol. Psychiatry 2006, 59(6):516-522.
53. Ji J.Z., Wang X.M., Li B.M. Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. Eur. J. Neurosci. 2003, 17:1947-1952.
54. Joels M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 2006, 27:244-250.
55. Joels M., Karst H., Alfarez D., Heine V.M., Qin Y., van Riel E., Verkuyl M., Lucassen P.J., Krugers H.J. Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 2004, 7:221-231.
56. Joels M., Pu Z., Wiegert O., Oitzl M.S., Krugers H.J. Learning under stress: how does it work?. Trends Cogn. Sci. 2006, 10:152-158.
57. Karst H., Nair S., Velzing E., Rumpff-van Essen L., Slagter E., Shinnick-Gallagher P., Joels M. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur. J. Neurosci. 2002, 16(6):1083-1089.
58. Kavushansky A., Richter-Levin G. Effects of stress and corticosterone on activity and plasticity in the amygdala. J. Neurosci. Res. 2006, 84:1580-1587.
59. Kavushansky A., Vouimba R.M., Cohen H., Richter-Levin G. Activity and plasticity in the CA1, the dentate gyrus, and the amygdala following controllable vs. uncontrollable water stress. Hippocampus 2006, 16(1):35-42.
60. Kim J.J., Koo J.W., Lee H.J., Han J.S. Amygdalar inactivation blocks stress-induced impairments in hippocampal long-term potentiation and spatial memory. J. Neurosci. 2005, 25(6):1532-1539.
61. Kirschbaum C., Wolf O.T., May M., Wippich W. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sci. 1996, 58:1475-1483.
62. Krettek J.E., Price J.L. Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J. Comp. Neurol. 1978, 178(2):225-254.
63. Kuhlmann S., Piel M., Wolf O.T. Impaired memory retrieval after psychosocial stress in healthy young men. J. Neurosci. 2005, 25:2977-2982.
64. Leuner B., Gould E., Shors T.J. Is there a link between adult neurogenesis and learning?. Hippocampus 2006, 16(3):216-224.
65. Leuner B., Mendolia-Loffredo S., Shors T.J. Males and females respond differently to controllability and antidepressant treatment. Biol. Psychiatry 2004, 56(12):964-970.
66. Leuner B., Shors T.J. New spines, new memories. Mol. Neurobiol. 2004, 29(2):117-130. [Review] [66 refs].
67. Liang K.C., Juler R.G., McGaugh J.L. Modulating effects of posttraining epinephrine on memory: involvement of the amygdala noradrenergic system. Brain Res. 1986, 368(1):125-133.
68. Liston C., Miller M.M., Goldwater D.S., Radley J.J., Rocher A.B., Hof P.R., Morrison J.H., McEwen B.S. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J. Neurosci. 2006, 26:7870-7874.
69. Luine V., Martinez C., Villegas M., Magarinos A.M., McEwen B.S. Restraint stress reversibly enhances spatial memory performance. Physiol. Behav. 1996, 59(1):27-32.
70. Lupien S.J., Fiocco A., Wan N., Maheu F., Lord C., Schramek T., Tu M.T. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 2005, 30(3):225-242.
71. Lupien S.J., Lepage M. Stress, memory, and the hippocampus: can't live with it, can't live without it. Behav. Brain Res. 2001, 127(1-2):137-158.
72. Magarinos A.M., McEwen B.S. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 1995, 69:89-98.
73. Maheu F.S., Joober R., Beaulieu S., Lupien S.J. Differential effects of adrenergic and corticosteroid hormonal systems on human short- and long-term declarative memory for emotionally arousing material. Behav. Neurosci. 2004, 118(2):420-428.
74. Mauk M.D., Thompson R.F. Retention of classically conditioned eyelid responses following acute decerebration. Brain Res. 1987, 403(1):89-95.
75. McEchron M.D., Disterhoft J.F. Hippocampal encoding of non-spatial trace conditioning. Hippocampus 1999, 9:385-396.
76. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005, 54:20-23.
77. McEwen B.S., Weiss J.M., Schwartz L.S. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968, 220:911-912.
78. McGaugh J.L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Ann. Rev. Neurosci. 2004, 27:1-28.
79. Miranda M.I., Lalumiere R.T., Buen T.V., Bermudez-Rattoni F., McGaugh J.L. Blockade of noradrenergic receptors in the basolateral amygdala impairs taste memory. Eur. J. Neurosci. 2003, 18(9):2605-2610.
80. Mirescu C., Gould E. Stress and adult neurogenesis. Hippocampus 2006, 16(3):233-238.
81. Mitra R., Sapolsky R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:5573-5578.
82. Mueller D., Porter J.T., Quirk G.J. Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J. Neurosci. 2008, 28:369-375.
83. Oei N.Y., Elzinga B.M., Wolf O.T., de Ruiter M.B., Damoiseaux J.S., Kuijer J.P., Veltman D.J., Scheltens P., Rombouts S.A. Glucocorticoids decrease hippocampal and prefrontal activation during declarative memory retrieval in young men. Brain Imaging Behav. 2007, 1:31-41.
84. Patel P.D., Katz M., Karssen A.M., Lyons D.M. Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 2008, 33:360-367.
85. Patel P.D., Lopez J.F., Lyons D.M., Burke S., Wallace M., Schatzberg A.F. Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. J. Psychiatr. Res. 2000, 34:383-392.
86. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106(2):274-285.
87. Pitman R.K., Sanders K.M., Zusman R.M., Healy A.R., Cheema F., Lasko N.B., Cahill L., Orr S.P. Pilot study of secondary prevention of posttraumatic stress disorder with propranolol. Biol. Psychiatry 2002, 51:189-192.
88. Radley J.J., Sisti H.M., Hao J., Rocher A.B., McCall T., Hof P.R., McEwen B.S., Morrison J.H. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004, 125:1-6.
89. Ressler K.J., Rothbaum B.O., Tannenbaum L., Anderson P., Graap K., Zimand E., Hodges L., Davis M. Cognitive enhancers as adjuncts to psychotherapy: use of d-cycloserine in phobic individuals to facilitate extinction of fear. Arch. Gen. Psychiatry 2004, 61:1136-1144.
90. Revest J.M., Di Blasi F., Kitchener P., Rouge-Pont F., Desmedt A., Turiault M., Tronche F., Piazza P.V. The MAPK pathway and Egr-1 mediate stress-related behavioral effects of glucocorticoids. Nat. Neurosci. 2005, 8:664-672.
91. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 2009, 32:289-313.
92. Rodriguez Manzanares P.A., Isoardi N.A., Carrer H.F., Molina V.A. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J. Neurosci. 2005, 25(38):8725-8734.
93. Roozendaal B. Stress and memory: opposing effects of glucocorticoids on memory consolidation and memory retrieval. Neurobiol. Learn. Mem. 2002, 78:578-595.
94. Roozendaal B. Systems mediating acute glucocorticoid effects on memory consolidation and retrieval. Prog. Neuro-Psychopharmacol. Biol. Psychiatry 2003, 27(8):1213-1223.
95. Roozendaal B., Brunson K.L., Holloway B.L., McGaugh J.L., Baram T.Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(21):13908-13913.
96. Roozendaal B., Griffith Q.K., Buranday J., de Quervain D.J., McGaugh J.L. The hippocampus mediates glucocorticoid-induced impairment of spatial memory retrieval: dependence on the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2003, 100(3):1328-1333.
97. Salinas J.A., Introini-Collison I.B., Dalmaz C., McGaugh J.L. Posttraining intraamygdala infusions of oxotremorine and propranolol modulate storage of memory for reductions in reward magnitude. Neurobiol. Learn. Mem. 1997, 68(1):51-59.
98. Sandi C. Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 2004, 5:917-930.
99. Sandi C., Loscertales M., Guaza C. Experience-dependent facilitating effect of corticosterone on spatial memory formation in the water maze. Eur. J. Neurosci. 1997, 9:637-642.
100. Sandi C., Merino J.J., Cordero M.I., Touyarot K., Venero C. Effects of chronic stress on contextual fear conditioning and the hippocampal expression of the neural cell adhesion molecule, its polysialylation, and L1. Neuroscience 2001, 102:329-339.
101. Sandi C., Pinelo-Nava M.T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast. 2007, 2007:78970.
102. Sarrieau A., Dussaillant M., Agid F., Philibert D., Agid Y., Rostene W. Autoradiographic localization of glucocorticosteroid and progesterone binding sites in the human post-mortem brain. J. Steroid Biochem. 1986, 25:717-721.
103. Servatius R.J., Shors T.J. Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav. Neurosci. 1994, 108(6):1101-1106.
104. Shepard J.D., Schulkin J., Myers D.A. Chronically elevated corticosterone in the amygdala increases corticotropin releasing factor mRNA in the dorsolateral bed nucleus of stria terminalis following duress. Behav. Brain Res. 2006, 174:193-196.
105. Shors T.J. Acute stress and re-exposure to the stressful context suppress spontaneous unit activity in the basolateral amygdala via NMDA receptor activation. Neuroreport 1999, 10:2811-2815.
106. Shors T.J. Acute stress rapidly and persistently enhances memory formation in the male rat. Neurobiol. Learn. Mem. 2001, 75(1):10-29.
107. Shors T.J. Learning during stressful times. Learn. Mem. Apr 2004, 11(2):137-144.
108. Shors T.J. Stressful experience and learning across the lifespan. Ann. Rev. Psychol. 2006, 57:55-85.
109. Shors T.J. Saving new brain cells. Sci. Am. 2009, 300:46-52. 54.
110. Shors T.J., Chua C., Falduto J. Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J. Neurosci. 2001, 21(16):6292-6297.
111. Shors T.J., Falduto J., Leuner B. The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor-dependent. Eur. J. Neurosci. 2004, 145-150.
112. Shors T.J., Mathew J., Sisti H.M., Edgecomb C., Beckoff S., Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol. Psychiatry 2007, 62:487-495.
113. Shors T.J., Mathew P.R. NMDA receptor antagonism in the lateral/basolateral but not central nucleus of the amygdala prevents the induction of facilitated learning in response to stress. Learn. Mem. Aug 1998, 5(3):220-230.
114. Shors T.J., Matzel L.D. Long-term potentiation: what's learning got to do with it?. Behavioral & Brain Sciences 1996, 597-614.
115. Shors T.J., Miesegaes G. Testosterone in utero and at birth dictates how stressful experience will affect learning in adulthood. Proc. Natl. Acad. Sci. U.S.A. 2002, 99(21):13955-13960.
116. Shors T.J., Miesegaes G., Beylin A., Zhao M., Rydel T., Gould E. Neurogenesis in the adult is involved in the formation of trace memories. Nature 2001, 410(6826):372-376.
117. Shors T.J., Seib T.B., Levine S., Thompson R.F. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989, 244(4901):224-226.
118. Shors T.J., Servatius R.J. The contribution of stressor intensity, duration, and context to the stress-induced facilitation of associative learning. Neurobiol. Learn. Mem. 1997, 68(1):92-96.
119. Shors T.J., Weiss C., Thompson R.F. Stress-induced facilitation of classical conditioning. Science 1992, 257(5069):537-539.
120. Smriga M., Saito H., Nishiyama N. Hippocampal long- and short-term potentiation is modulated by adrenalectomy and corticosterone. Neuroendocrinology 1996, 64(1):35-41.
121. Solomon P.R., Vander Schaaf E.R., Thompson R.F., Weisz D.J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 1986, 100(5):729-744.
122. Soravia L.M., Heinrichs M., Aerni A., Maroni C., Schelling G., Ehlert U., Roozendaal B., de Quervain D.J. Glucocorticoids reduce phobic fear in humans. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:5585-5590.
123. Starkman M.N., Gebarski S.S., Berent S., Schteingart D.E. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 1992, 32(9):756-765.
124. Starkman M.N., Giordani B., Berent S., Schork A., Schteingart D.E. Elevated cortisol levels in Cushing's disease are associated with cognitive decrements. Psychosom. Med. 2001, 63:985-993.
125. Starkman M.N., Giordani B., Gebarski S.S., Schteingart D.E. Improvement in learning associated with increase in hippocampal formation volume. Biol. Psychiatry 2003, 53:233-238.
126. Steinmetz J.E., Logan C.G., Rosen D.J., Thompson J.K., Lavond D.G., Thompson R.F. Initial localization of the acoustic conditioned stimulus projection system to the cerebellum essential for classical eyelid conditioning. Proc. Natl. Acad. Sci. U.S.A. 1987, 84(10):3531-3535.
127. Swanson L.W., Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J. Comp. Neurol. 1977, 172:49-84.
128. Thompson R.F. In search of memory traces. Ann. Rev. Psychol. 2005, 56:1-23.
129. Tracy J.A., Thompson J.K., Krupa D.J., Thompson R.F. Evidence of plasticity in the pontocerebellar conditioned stimulus pathway during classical conditioning of the eyeblink response in the rabbit. Behav. Neurosci. 1998, 112(2):267-285.
130. Tronel S., Alberini C.M. Persistent disruption of a traumatic memory by postretrieval inactivation of glucocorticoid receptors in the amygdala. Biol. Psychiatry 2007, 62:33-39.
131. Veldhuis H.D., Van Koppen C., Van Ittersum M., De Kloet E.R. Specificity of the adrenal steroid receptor system in rat hippocampus. Endocrinology 1982, 110:2044-2051.
132. Venero C., Tilling T., Hermans-Borgmeyer I., Schmidt R., Schachner M., Sandi C. Chronic stress induces opposite changes in the mRNA expression of the cell adhesion molecules NCAM and L1. Neuroscience 2002, 115:1211-1219.
133. Waddell J., Bangasser D.A., Shors T.J. The basolateral nucleus of the amygdala is necessary to induce the opposing effects of stressful experience on learning in males and females. J. Neurosci. 2008, 28(20):5290-5294.
134. Waddell J., Mallimo E., Shors T. d-cycloserine reverses the detrimental effects of stress on learning in females and enhances retention in males. Neurobiol. Learn. Mem. 2010, 93(1):31-36.
135. Watanabe Y., Gould E., McEwen B.S. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res. 1992, 588(2):341-345.
136. Weiss C., Sametsky E., Sasse A., Spiess J., Disterhoft J.F. Acute stress facilitates trace eyeblink conditioning in C57BL/6 male mice and increases the excitability of their CA1 pyramidal neurons. Learn. Mem. Apr 2005, 12(2):138-143.
137. Weller K.L., Smith D.A. Afferent connections to the bed nucleus of the stria terminalis. Brain Res. 1982, 232(2):255-270.
138. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 2001, 49:245-253.
139. Whalen P.J., Kapp B.S. Contributions of the amygdaloid central nucleus to the modulation of the nictitating membrane reflex in the rabbit. Behav. Neurosci. 1991, 105(1):141-153.
140. Wilhelm S., Buhlmann U., Tolin D.F., Meunier S.A., Pearlson G.D., Reese H.E., Cannistraro P., Jenike M.A., Rauch S.L. Augmentation of behavior therapy with d-cycloserine for obsessive-compulsive disorder. Am. J. Psychiatry 2008, 165:335-341.
141. Wood G.E., Beylin A.V., Shors T.J. The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning in males versus females. Behav. Neurosci. 2001, 115(1):175-187.
142. Wood G.E., Shors T.J. Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc. Natl. Acad. Sci. U.S.A. 1998, 95(7):4066-4071.
143. Wright R.L., Conrad C.D. Chronic stress leaves novelty-seeking behavior intact while impairing spatial recognition memory in the Y-maze. Stress 2005, 8:151-154.
144. Yang Y.L., Chao P.K., Lu K.T. Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear. Neuropsychopharmacology 2006, 31:912-924.
145. Yuen E.Y., Liu W., Karatsoreos I.N., Feng J., McEwen B.S., Yan Z. Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:14075-14079.
146. Zorawski M., Cook C.A., Kuhn C.M., LaBar K.S. Sex, stress, and fear: individual differences in conditioned learning. Cogn. Affect. Behav. Neurosci. 2005, 5:191-201.