Stress-induced impairments in prefrontal-mediated behaviors and the role of the N-methyl-d-aspartate receptor

Neuroscience

Volumn 211, Issue , 2012, Pages 28-38

  Graybeal, C ^a   Kiselycznyk, C ^a   Holmes, A ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

Author keywords

Cognition; Extinction; Glutamate; N methyl D aspartate; Prefrontal cortex; Stress

Indexed keywords

CLOZAPINE; GLUTAMIC ACID; IFENPRODIL; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; PHENCYCLIDINE; RISPERIDONE; RO 256981; SERTINDOLE; UNCLASSIFIED DRUG;

ATTENTION; BRAIN REGION; COGNITION; COGNITIVE DEFECT; MENTAL DISEASE; MENTAL STRESS; MOLECULAR MECHANICS; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; REVIEW; RODENT; WORKING MEMORY;

ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; PREFRONTAL CORTEX; RECEPTORS, N-METHYL-D-ASPARTATE; STRESS, PSYCHOLOGICAL;

EID: 84860617196     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.02.042     Document Type: Review

References (160)

1. Abdul-Monim Z., Neill J.C., Reynolds G.P. Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat. J Psychopharmacol 2007, 21:198-205.
2. Abdul-Monim Z., Reynolds G.P., Neill J.C. The effect of atypical and classical antipsychotics on sub-chronic PCP-induced cognitive deficits in a reversal-learning paradigm. Behav Brain Res 2006, 169:263-273.
3. Amat J., Aleksejev R.M., Paul E., Watkins L.R., Maier S.F. Behavioral control over shock blocks behavioral and neurochemical effects of later social defeat. Neuroscience 2010, 165:1031-1038.
4. Amat J., Baratta M.V., Paul E., Bland S.T., Watkins L.R., Maier S.F. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 2005, 8:365-371.
5. Amat J., Paul E., Zarza C., Watkins L.R., Maier S.F. Previous experience with behavioral control over stress blocks the behavioral and dorsal raphe nucleus activating effects of later uncontrollable stress: role of the ventral medial prefrontal cortex. J Neurosci 2006, 26:13264-13272.
6. Amitai N., Markou A. Increased impulsivity and disrupted attention induced by repeated phencyclidine are not attenuated by chronic quetiapine treatment. Pharmacol Biochem Behav 2009, 93:248-257.
7. Amitai N., Markou A. Disruption of performance in the five-choice serial reaction time task induced by administration of N-methyl-d-aspartate receptor antagonists: relevance to cognitive dysfunction in schizophrenia. Biol Psychiatry 2010, 68:5-16.
8. Amitai N., Semenova S., Markou A. Cognitive-disruptive effects of the psychotomimetic phencyclidine and attenuation by atypical antipsychotic medications in rats. Psychopharmacol (Berl) 2007, 193:521-537.
9. Anisman H., Matheson K. Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 2005, 29:525-546.
10. Arnsten A.F. Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 2009, 10:410-422.
11. Arnsten A.F., Pliszka S.R. Catecholamine influences on prefrontal cortical function: relevance to treatment of attention deficit/hyperactivity disorder and related disorders. Pharmacol Biochem Behav 2011, 99:211-216.
12. Aura J., Riekkinen P. Blockade of NMDA receptors located at the dorsomedial prefrontal cortex impairs spatial working memory in rats. Neuroreport 1999, 10:243-248.
13. Bannerman D.M., Niewoehner B., Lyon L., Romberg C., Schmitt W.B., Taylor A., Sanderson D.J., Cottam J., Sprengel R., Seeburg P.H., Köhr G., Rawlins J.N. NMDA receptor subunit NR2A is required for rapidly acquired spatial working memory but not incremental spatial reference memory. J Neurosci 2008, 28:3623-3630.
14. Baran S.E., Armstrong C.E., Niren D.C., Hanna J.J., Conrad C.D. Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem 2009, 91:323-332.
15. Baratta M.V., Christianson J.P., Gomez D.M., Zarza C.M., Amat J., Masini C.V., Watkins L.R., Maier S.F. Controllable versus uncontrollable stressors bi-directionally modulate conditioned but not innate fear. Neuroscience 2007, 146:1495-1503.
16. Baratta M.V., Lucero T.R., Amat J., Watkins L.R., Maier S.F. Role of the ventral medial prefrontal cortex in mediating behavioral control-induced reduction of later conditioned fear. Learn Mem 2008, 15:84-87.
17. Bardgett M.E., Boeckman R., Krochmal D., Fernando H., Ahrens R., Csernansky J.G. NMDA receptor blockade and hippocampal neuronal loss impair fear conditioning and position habit reversal in C57Bl/6 mice. Brain Res Bull 2003, 60:131-142.
18. Barha C.K., Pawluski J.L., Galea L.A. Maternal care affects male and female offspring working memory and stress reactivity. Physiol Behav 2007, 92:939-950.
19. Barkus C., McHugh S.B., Sprengel R., Seeburg P.H., Rawlins J.N., Bannerman D.M. Hippocampal NMDA receptors and anxiety: at the interface between cognition and emotion. Eur J Pharmacol 2010, 626:49-56.
20. Barnett J.H., Robbins T.W., Leeson V.C., Sahakian B.J., Joyce E.M., Blackwell A.D. Assessing cognitive function in clinical trials of schizophrenia. Neurosci Biobehav Rev 2010, 34:1161-1177.
21. Baviera M., Invernizzi R.W., Carli M. Haloperidol and clozapine have dissociable effects in a model of attentional performance deficits induced by blockade of NMDA receptors in the mPFC. Psychopharmacology (Berl) 2008, 196:269-280.
22. Belforte J.E., Zsiros V., Sklar E.R., Jiang Z., Yu G., Li Y., Quinlan E.M., Nakazawa K. Postnatal NMDA receptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 2010, 13:76-83.
23. Berman R.M., Cappiello A., Anand A., Oren D.A., Heninger G.R., Charney D.S., Krystal J.H. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry 2000, 47:351-354.
24. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 2000, 20:4320-4324.
25. Bissonette G.B., Martins G.J., Franz T.M., Harper E.S., Schoenbaum G., Powell E.M. Double dissociation of the effects of medial and orbital prefrontal cortical lesions on attentional and affective shifts in mice. J Neurosci 2008, 28:11124-11130.
26. Blundell J., Blaiss C.A., Lagace D.C., Eisch A.J., Powell C.M. Block of glucocorticoid synthesis during re-activation inhibits extinction of an established fear memory. Neurobiol Learn Mem 2011, 95:453-460.
27. Bondi C.O., Jett J.D., Morilak D.A. Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by [alpha]1-adrenergic receptors in medial prefrontal cortex. Prog Neuro-Psychopharmacol Biol Psychiatry 2010, 34:913-923.
28. Bondi C.O., Rodriguez G., Gould G.G., Frazer A., Morilak D.A. Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 2008, 33:320-331.
29. Boulougouris V., Dalley J.W., Robbins T.W. Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behav Brain Res 2007, 179:219-228.
30. Boyce-Rustay J.M., Holmes A. Genetic inactivation of the NMDA receptor NR2A subunit has anxiolytic- and antidepressant-like effects in mice. Neuropsychopharmacology 2006, 31:2405-2414.
31. Brenhouse H.C., Andersen S.L. Nonsteroidal anti-inflammatory treatment prevents delayed effects of early life stress in rats. Biol Psychiatry 2011, 70:434-440.
32. Brigman J.L., Feyder M., Saksida L.M., Bussey T.J., Mishina M., Holmes A. Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learn Mem 2008, 15:50-54.
33. Brigman J.L., Graybeal C., Holmes A. Predictably irrational: assaying cognitive inflexibility in mouse models of schizophrenia. Front Neurosci 2010, 4(1):19-28.
34. Brinks V., de Kloet E.R., Oitzl M.S. Corticosterone facilitates extinction of fear memory in BALB/c mice but strengthens cue related fear in C57BL/6 mice. Exp Neurol 2009, 216:375-382.
35. Buchanan J.B., Sparkman N.L., Chen J., Johnson R.W. Cognitive and neuroinflammatory consequences of mild repeated stress are exacerbated in aged mice. Psychoneuroendocrinology 2008, 33:755-765.
36. Burgos-Robles A., Vidal-Gonzalez I., Santini E., Quirk G.J. Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 2007, 53:871-880.
37. Butts K.A., Weinberg J., Young A.H., Phillips A.G. Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad Sci U S A 2011, 108:18459-18464.
38. Callaghan B.L., Richardson R. Maternal separation results in early emergence of adult-like fear and extinction learning in infant rats. Behav Neurosci 2011, 125:20-28.
39. 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.
40. Cerqueira J.J., Pêgo J.M., Taipa R., Bessa J.M., Almeida O.F., Sousa N. Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J Neurosci 2005, 25:7792-7800.
41. Chang C.H., Maren S. Early extinction after fear conditioning yields a context-independent and short-term suppression of conditional freezing in rats. Learn Mem 2009, 16:62-68.
42. Choy K.H., de Visser Y., Nichols N.R., van den Buuse M. Combined neonatal stress and young-adult glucocorticoid stimulation in rats reduce BDNF expression in hippocampus: effects on learning and memory. Hippocampus 2008, 18:655-667.
43. Christian K.M., Miracle A.D., Wellman C.L., Nakazawa K. Chronic stress-induced hippocampal dendritic retraction requires CA3 NMDA receptors. Neuroscience 2011, 174:26-36.
44. Christianson J.P., Paul E.D., Irani M., Thompson B.M., Kubala K.H., Yirmiya R., Watkins L.R., Maier S.F. The role of prior stressor controllability and the dorsal raphe nucleus in sucrose preference and social exploration. Behav Brain Res 2008, 193:87-93.
45. Christianson J.P., Thompson B.M., Watkins L.R., Maier S.F. Medial prefrontal cortical activation modulates the impact of controllable and uncontrollable stressor exposure on a social exploration test of anxiety in the rat. Stress 2009, 12:445-450.
46. Chudasama Y. Animal models of prefrontal-executive function. Behav Neurosci 2011, 125:327-343.
47. Chudasama Y., Robbins T.W. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol 2006, 73:19-38.
48. Cools R., Robbins T.W. Chemistry of the adaptive mind. Philos Transact A Math Phys Eng Sci 2004, 362:2871-2888.
49. Cryan J.F., Dev K.K. Role of glutamate in anxiety. Handbook of fear and anxiety 2008, 269-301. Elsevier, London. D.C. Blanchard, R.M. Blanchard (Eds.).
50. Cui Y., Jin J., Zhang X., Xu H., Yang L., Du D., Zeng Q., Tsien J.Z., Yu H., Cao X. Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PLoS One 2011, 6:e20312.
51. Cull-Candy S., Brickley S., Farrant M. NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 2001, 11:327-335.
52. Dalton G.L., Ma L.M., Phillips A.G., Floresco S.B. Blockade of NMDA GluN2B receptors selectively impairs behavioral flexibility but not initial discrimination learning. Psychopharmacology (Berl) 2011, 216:525-535.
53. Dalton G.L., Wu D.C., Wang Y.T., Floresco S.B., Phillips A.G. NMDA GluN2A and GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology 2011, 62:797-806.
54. Danet M., Lapiz-Bluhm S., Morilak D.A. A cognitive deficit induced in rats by chronic intermittent cold stress is reversed by chronic antidepressant treatment. Int J Neuropsychopharmacol 2010, 13:997-1009.
55. Del Arco A., Segovia G., de Blas M., Garrido P., Acuña-Castroviejo D., Pamplona R., Mora F. Prefrontal cortex, caloric restriction and stress during aging: studies on dopamine and acetylcholine release, BDNF and working memory. Behav Brain Res 2011, 216:136-145.
56. Del Arco A., Segovia G., Garrido P., de Blas M., Mora F. Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 2007, 176:267-273.
57. 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, 9:542-552.
58. 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.
59. Didriksen M., Skarsfeldt T., Arnt J. Reversal of PCP-induced learning and memory deficits in the Morris' water maze by sertindole and other antipsychotics. Psychopharmacology (Berl) 2007, 193:225-233.
60. Duffy S., Labrie V., Roder J.C. d-serine augments NMDA-NR2B receptor-dependent hippocampal long-term depression and spatial reversal learning. Neuropsychopharmacology 2008, 33:1004-1018.
61. Farrell M.R., Sayed J.A., Underwood A.R., Wellman C.L. Lesion of infralimbic cortex occludes stress effects on retrieval of extinction but not fear conditioning. Neurobiol Learn Mem 2010, 94:240-246.
62. Floresco S.B., Zhang Y., Enomoto T. Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav Brain Res 2009, 204:396-409.
63. Francis D.D., Zaharia M.D., Shanks N., Anisman H. Stress-induced disturbances in Morris water-maze performance: interstrain variability. Physiol Behav 1995, 58:57-65.
64. Fraser C.M., Cooke M.J., Fisher A., Thompson I.D., Stone T.W. Interactions between ifenprodil and dizocilpine on mouse behaviour in models of anxiety and working memory. Eur Neuropsychopharmacol 1996, 6:311-316.
65. Fritts M.E., Asbury E.T., Horton J.E., Isaac W.L. Medial prefrontal lesion deficits involving or sparing the prelimbic area in the rat. Physiol Behav 1998, 64:373-380.
66. Furr A., Lapiz-Bluhm M.D., Morilak D.A. 5-HT2A receptors in the orbitofrontal cortex facilitate reversal learning and contribute to the beneficial cognitive effects of chronic citalopram treatment in rats. Int J Neuropsychopharmacol 2011, 1-11.
67. Gamo N.J., Arnsten A.F. Molecular modulation of prefrontal cortex: rational development of treatments for psychiatric disorders. Behav Neurosci 2011, 125:282-296.
68. Gisquet-Verrier P., Delatour B. The role of the rat prelimbic/infralimbic cortex in working memory: not involved in the short-term maintenance but in monitoring and processing functions. Neuroscience 2006, 141:585-596.
69. Goswami S., Cascardi M., Rodríguez-Sierra O.E., Duvarci S., Paré D. Impact of predatory threat on fear extinction in Lewis rats. Learn Mem 2010, 17:494-501.
70. Gourley S.L., Kedves A.T., Olausson P., Taylor J.R. A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacology 2009, 34:707-716.
71. Graybeal C., Feyder M., Schulman E., Saksida L.M., Bussey T.J., Brigman J.L., Holmes A. Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF. Nat Neurosci 2011, 14:1507-1509.
72. Green M.K., Rani C.S., Joshi A., Soto-Piña A.E., Martinez P.A., Frazer A., Strong R., Morilak D.A. Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress. Neuroscience 2011, 192:438-451.
73. Hains A.B., Vu M.A., Maciejewski P.K., van Dyck C.H., Gottron M., Arnsten A.F. Inhibition of protein kinase C signaling protects prefrontal cortex dendritic spines and cognition from the effects of chronic stress. Proc Natl Acad Sci U S A 2009, 106:17957-17962.
74. Higgins G.A., Ballard T.M., Enderlin M., Haman M., Kemp J.A. Evidence for improved performance in cognitive tasks following selective NR2B NMDA receptor antagonist pre-treatment in the rat. Psychopharmacology (Berl) 2005, 179:85-98.
75. Higgins G.A., Ballard T.M., Huwyler J., Kemp J.A., Gill R. Evaluation of the NR2B-selective NMDA receptor antagonist Ro 63-1908 on rodent behaviour: evidence for an involvement of NR2B NMDA receptors in response inhibition. Neuropharmacology 2003, 44:324-341.
76. Hill M.N., Patel S., Carrier E.J., Rademacher D.J., Ormerod B.K., Hillard C.J., Gorzalka B.B. Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 2004, 30:508-515.
77. Holmes A., Wellman C.L. Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci Biobehav Rev 2009, 33:773-783.
78. Holt D.J., Lebron-Milad K., Milad M.R., Rauch S.L., Pitman R.K., Orr S.P., Cassidy B.S., Walsh J.P., Goff D.C. Extinction memory is impaired in schizophrenia. Biol Psychiatry 2009, 65:455-463.
79. Izquierdo A., Wellman C.L., Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 2006, 26:5733-5738.
80. Jentsch J.D., Tran A., Le D., Youngren K.D., Roth R.H. Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat. Neuropsychopharmacology 1997, 17:92-99.
81. Joels M., Karst H., Krugers H.J., Lucassen P.J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front Neuroendocrinol 2007, 28:72-96.
82. 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.
83. Judo C., Matsumoto M., Yamazaki D., Hiraide S., Yanagawa Y., Kimura S., Shimamura K., Togashi H. Early stress exposure impairs synaptic potentiation in the rat medial prefrontal cortex underlying contextual fear extinction. Neuroscience 2010, 169:1705-1714.
84. Kiselycznyk C.L., Svenningsson P., Delpire E., Holmes A. Genetic, pharmacological and lesion analyses reveal a selective role for corticohippocampal GLUN2B in a novel repeated swim stress paradigm. Neuroscience 2011, 193:259-268.
85. Ko T., Evenden J. The effects of psychotomimetic and putative cognitive-enhancing drugs on the performance of a n-back working memory task in rats. Psychopharmacology (Berl) 2009, 202:67-78.
86. Kos T., Nikiforuk A., Rafa D., Popik P. The effects of NMDA receptor antagonists on attentional set-shifting task performance in mice. Psychopharmacology (Berl) 2011, 214:911-921.
87. Krystal J.H., Bennett A., Abi-Saab D., Belger A., Karper L.P., D'Souza D.C., Lipschitz D., Abi-Dargham A., Charney D.S. Dissociation of ketamine effects on rule acquisition and rule implementation: possible relevance to NMDA receptor contributions to executive cognitive functions. Biol Psychiatry 2000, 47:137-143.
88. Krystal J.H., Karper L.P., Seibyl J.P., Freeman G.K., Delaney R., Bremner J.D., Heninger G.R., Bowers M.B., Charney D.S. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 1994, 51:199-214.
89. Lapiz-Bluhm M.D., Soto-Pina A.E., Hensler J.G., Morilak D.A. Chronic intermittent cold stress and serotonin depletion induce deficits of reversal learning in an attentional set-shifting test in rats. Psychopharmacology (Berl) 2009, 202:329-341.
90. Lee S.Y., Kang J.S., Song G.Y., Myung C.S. Stress induces the expression of heterotrimeric G protein beta subunits and the phosphorylation of PKB/Akt and ERK1/2 in rat brain. Neurosci Res 2006, 56:180-192.
91. Li N., Lee B., Liu R.J., Banasr M., Dwyer J.M., Iwata M., Li X.Y., Aghajanian G., Duman R.S. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science 2010, 329:959-964.
92. Li N., Liu R.J., Dwyer J.M., Banasr M., Lee B., Son H., Li X.Y., Aghajanian G., Duman R.S. Glutamate N-methyl-d-aspartate receptor antagonists rapidly reverse behavioral and synaptic deficits caused by chronic stress exposure. Biol Psychiatry 2011, 69:754-761.
93. 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.
94. Lupien S.J., McEwen B.S., Gunnar M.R., Heim C. Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 2009, 10:434-445.
95. Maeng S., Zarate C.A., Du J., Schloesser R.J., McCammon J., Chen G., Manji H.K. Cellular mechanisms underlying the antidepressant effects of ketamine: role of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptors. Biol Psychiatry 2008, 63:349-352.
96. 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.
97. Maier S.F., Watkins L.R. Role of the medial prefrontal cortex in coping and resilience. Brain Res 2010, 1355:52-60.
98. Martin K.P., Wellman C.L. NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb Cortex 2011, 21:2366-2373.
99. Matsuda S., Matsuzawa D., Nakazawa K., Sutoh C., Ohtsuka H., Ishii D., Tomizawa H., Iyo M., Shimizu E. d-serine enhances extinction of auditory cued fear conditioning via ERK1/2 phosphorylation in mice. Prog Neuropsychopharmacol Biol Psychiatry 2010, 34:895-902.
100. Matsumoto M., Togashi H., Konno K., Koseki H., Hirata R., Izumi T., Yamaguchi T., Yoshioka M. Early postnatal stress alters the extinction of context-dependent conditioned fear in adult rats. Pharmacol Biochem Behav 2008, 89:247-252.
101. McLean A., Dowson J., Toone B., Young S., Bazanis E., Robbins T.W., Sahakian B.J. Characteristic neurocognitive profile associated with adult attention-deficit/hyperactivity disorder. Psychol Med 2004, 34:681-692.
102. Mehta M., Schmauss C. Strain-specific cognitive deficits in adult mice exposed to early life stress. Behav Neurosci 2011, 125:29-36.
103. Mineur Y.S., Belzung C., Crusio W.E. Functional implications of decreases in neurogenesis following chronic mild stress in mice. Neuroscience 2007, 150:251-259.
104. Miracle A.D., Brace M.F., Huyck K.D., Singler S.A., Wellman C.L. Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 2006, 85:213-218.
105. Mizoguchi K., Yuzurihara M., Ishige A., Sasaki H., Chui D.H., Tabira T. Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 2000, 20:1568-1574.
106. 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 Res Bull 2000, 52:519-523.
107. Mozhui K., Karlsson R.M., Kash T.L., Ihne J., Norcross M., Patel S., Farrell M.R., Hill E.E., Graybeal C., Martin K.P., Camp M., Fitzgerald P.J., Ciobanu D.C., Sprengel R., Mishina M., Wellman C.L., Winder D.G., Williams R.W., Holmes A. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 2010, 30:5357-5367.
108. Murphy E.R., Fernando A.B., Urcelay G.P., Robinson E.S., Mar A.C., Theobald D.E., Dalley J.W., Robbins T.W. Impulsive behaviour induced by both NMDA receptor antagonism and GABA(A) receptor activation in rat ventromedial prefrontal cortex. Psychopharmacology (Berl) 2012, 219:401-410.
109. Murphy F.C., Michael A., Robbins T.W., Sahakian B.J. Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychol Med 2003, 33:455-467.
110. Nakazawa T., Komai S., Watabe A.M., Kiyama Y., Fukaya M., Arima-Yoshida F., Horai R., Sudo K., Ebine K., Delawary M., Goto J., Umemori H., Tezuka T., Iwakura Y., Watanabe M., Yamamoto T., Manabe T. NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J 2006, 25:2867-2877.
111. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., Snigdha S., Rajagopal L., Harte M.K. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol Ther 2010, 128:419-432.
112. Neyton J., Paoletti P. Relating NMDA receptor function to receptor subunit composition: limitations of the pharmacological approach. J Neurosci 2006, 26:1331-1333.
113. Nikiforuk A. Selective blockade of 5-HT7 receptors facilitates attentional set-shifting in stressed and control rats. Behav Brain Res 2012, 226:118-123.
114. Nikiforuk A., Gołembiowska K., Popik P. Mazindol attenuates ketamine-induced cognitive deficit in the attentional set shifting task in rats. Eur Neuropsychopharmacol 2010, 20:37-48.
115. Nikiforuk A., Popik P. Long-lasting cognitive deficit induced by stress is alleviated by acute administration of antidepressants. Psychoneuroendocrinology 2011, 36:28-39.
116. Ohmura Y., Yamaguchi T., Futami Y., Togashi H., Izumi T., Matsumoto M., Yoshida T., Yoshioka M. Corticotropin releasing factor enhances attentional function as assessed by the five-choice serial reaction time task in rats. Behav Brain Res 2009, 198:429-433.
117. Park C.R., Zoladz P.R., Conrad C.D., Fleshner M., Diamond D.M. Acute predator stress impairs the consolidation and retrieval of hippocampus-dependent memory in male and female rats. Learn Mem 2008, 15:271-280.
118. Preskorn S.H., Baker B., Kolluri S., Menniti F.S., Krams M., Landen J.W. An innovative design to establish proof of concept of the antidepressant effects of the NR2B subunit selective N-methyl-d-aspartate antagonist, CP-101,606, in patients with treatment-refractory major depressive disorder. J Clin Psychopharmacol 2008, 28:631-637.
119. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
120. Robbins T.W. Shifting and stopping: fronto-striatal substrates, neurochemical modulation and clinical implications. Philos Trans R Soc Lond B Biol Sci 2007, 362:917-932.
121. Rodrigues S.M., Schafe G.E., LeDoux J.E. Intra-amygdala blockade of the NR2B subunit of the NMDA receptor disrupts the acquisition but not the expression of fear conditioning. J Neurosci 2001, 21:6889-6896.
122. Roozendaal B., McEwen B.S., Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 2009, 10:423-433.
123. Rosenmund C., Stern-Bach Y., Stevens C.F. The tetrameric structure of a glutamate receptor channel. Science 1998, 280:1596-1599.
124. Sandstrom N.J. Sex differences in the long-term effect of preweanling isolation stress on memory retention. Horm Behav 2005, 47:556-562.
125. Sandstrom N.J., Hart S.R. Isolation stress during the third postnatal week alters radial arm maze performance and corticosterone levels in adulthood. Behav Brain Res 2005, 156:289-296.
126. Santini E., Muller R.U., Quirk G.J. Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J Neurosci 2001, 21:9009-9017.
127. Schwabe K., Enkel T., Klein S., Schütte M., Koch M. Effects of neonatal lesions of the medial prefrontal cortex on adult rat behaviour. Behav Brain Res 2004, 153:21-34.
128. Schwabe L., Wolf O.T. Stress prompts habit behavior in humans. J Neurosci 2009, 29:7191-7198.
129. Schwabe L., Wolf O.T. Stress-induced modulation of instrumental behavior: from goal-directed to habitual control of action. Behav Brain Res 2011, 219:321-328.
130. Shansky R.M., Morrison J.H. Stress-induced dendritic remodeling in the medial prefrontal cortex: effects of circuit, hormones and rest. Brain Res 2009, 1293:108-113.
131. Sinha R. Chronic stress, drug use, and vulnerability to addiction. Ann N Y Acad Sci 2008, 1141:105-130.
132. Sloan H.L., Good M., Dunnett S.B. Double dissociation between hippocampal and prefrontal lesions on an operant delayed matching task and a water maze reference memory task. Behav Brain Res 2006, 171:116-126.
133. Smith J.W., Gastambide F., Gilmour G., Dix S., Foss J., Lloyd K., Malik N., Tricklebank M. A comparison of the effects of ketamine and phencyclidine with other antagonists of the NMDA receptor in rodent assays of attention and working memory. Psychopharmacology (Berl) 2011, 217:255-269.
134. Snyder K., Wang W.W., Han R., McFadden K., Valentino R.J. Corticotropin-releasing factor in the norepinephrine nucleus, locus coeruleus, facilitates behavioral flexibility. Neuropsychopharmacology 2011, 37:520-530.
135. Sotres-Bayon F., Bush D.E., LeDoux J.E. Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacology 2007, 32:1929-1940.
136. Sotres-Bayon F., Diaz-Mataix L., Bush D.E., LeDoux J.E. Dissociable roles for the ventromedial prefrontal cortex and amygdala in fear extinction: NR2B contribution. Cereb Cortex 2009, 19:474-482.
137. Stevenson C.W., Meredith J.P., Spicer C.H., Mason R., Marsden C.A. Early life programming of innate fear and fear learning in adult female rats. Behav Brain Res 2009, 198:51-57.
138. Stevenson C.W., Spicer C.H., Mason R., Marsden C.A. Early life programming of fear conditioning and extinction in adult male rats. Behav Brain Res 2009, 205:505-510.
139. Tagliari B., Scherer E.B., Machado F.R., Ferreira A.G., Dalmaz C., Wyse A.T. Antioxidants prevent memory deficits provoked by chronic variable stress in rats. Neurochem Res 2011, 36:2373-2380.
140. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 1999, 401:63-69.
141. Thomson D.M., McVie A., Morris B.J., Pratt J.A. Dissociation of acute and chronic intermittent phencyclidine-induced performance deficits in the 5-choice serial reaction time task: influence of clozapine. Psychopharmacology (Berl) 2011, 213:681-695.
142. Trofimiuk E., Braszko J.J. Alleviation by Hypericum perforatum of the stress-induced impairment of spatial working memory in rats. Naunyn Schmiedebergs Arch Pharmacol 2008, 376:463-471.
143. van der Meulen J.A., Bilbija L., Joosten R.N., de Bruin J.P., Feenstra M.G. The NMDA-receptor antagonist MK-801 selectively disrupts reversal learning in rats. Neuroreport 2003, 14:2225-2228.
144. von Engelhardt J., Doganci B., Jensen V., Hvalby O., Göngrich C., Taylor A., Barkus C., Sanderson D.J., Rawlins J.N., Seeburg P.H., Bannerman D.M., Monyer H. Contribution of hippocampal and extra-hippocampal NR2B-containing NMDA receptors to performance on spatial learning tasks. Neuron 2008, 60:846-860.
145. Walker D.L., Ressler K.J., Lu K.T., Davis M. Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of d-cycloserine as assessed with fear-potentiated startle in rats. J Neurosci 2002, 22:2343-2351.
146. Waltz J.A., Gold J.M. Probabilistic reversal learning impairments in schizophrenia: further evidence of orbitofrontal dysfunction. Schizophr Res 2007, 93:296-303.
147. Wang L., Jiao J., Dulawa S.C. Infant maternal separation impairs adult cognitive performance in BALB/cJ mice. Psychopharmacology (Berl) 2011, 216:207-218.
148. Watanabe Y., Gould E., Cameron H.A., Daniels D.C., McEwen B.S. Phenytoin prevents stress- and corticosterone-induced atrophy of CA3 pyramidal neurons. Hippocampus 1992, 2:431-435.
149. Watson D.J., Stanton M.E. Intrahippocampal administration of an NMDA-receptor antagonist impairs spatial discrimination reversal learning in weanling rats. Neurobiol Learn Mem 2009, 92:89-98.
150. Watson D.J., Stanton M.E. Medial prefrontal administration of MK-801 impairs T-maze discrimination reversal learning in weanling rats. Behav Brain Res 2009, 205:57-66.
151. Watson D.J., Stanton M.E. Spatial discrimination reversal learning in weanling rats is impaired by striatal administration of an NMDA-receptor antagonist. Learn Mem 2009, 16:564-572.
152. Wilber A.A., Southwood C.J., Wellman C.L. Brief neonatal maternal separation alters extinction of conditioned fear and corticolimbic glucocorticoid and NMDA receptor expression in adult rats. Dev Neurobiol 2009, 69:73-87.
153. Wilber A.A., Walker A.G., Southwood C.J., Farrell M.R., Lin G.L., Rebec G.V., Wellman C.L. Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction. Neuroscience 2011, 174:115-131.
154. Willmore C.B., Krall D.M., Spears F.M., Makriyannis A., Elmer G.I. Cognitive effects of psychotomimetic drugs in rats discriminating number cues. Psychopharmacology (Berl) 2009, 206:653-664.
155. Woodson J.C., Macintosh D., Fleshner M., Diamond D.M. Emotion-induced amnesia in rats: working memory-specific impairment, corticosterone-memory correlation, and fear versus arousal effects on memory. Learn Mem 2003, 10:326-336.
156. Yamada D., Wada K., Sekiguchi M. Facilitating actions of an AMPA receptor potentiator upon extinction of contextually conditioned fear response in stressed mice. Neurosci Lett 2011, 488:242-246.
157. 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.
158. Yuen E.Y., Liu W., Karatsoreos I.N., Ren Y., Feng J., McEwen B.S., Yan Z. Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry 2011, 16:156-170.
159. Zarate C.A., Singh J.B., Carlson P.J., Brutsche N.E., Ameli R., Luckenbaugh D.A., Charney D.S., Manji H.K. A randomized trial of an N-methyl-d-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry 2006, 63:856-864.
160. Zhao M.G., Toyoda H., Lee Y.S., Wu L.J., Ko S.W., Zhang X.H., Jia Y., Shum F., Xu H., Li B.M., Kaang B.K., Zhuo M. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47:859-872.