Mechanisms of stress in the brain

Nature Neuroscience

Volumn 18, Issue 10, 2015, Pages 1353-1363

  McEwen, Bruce S ^a   Bowles, Nicole P ^a   Gray, Jason D ^a   Hill, Matthew N ^b   Hunter, Richard G ^c   Karatsoreos, Ilia N ^d   Nasca, Carla ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF MASSACHUSETTS BOSTON   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; ENDOCANNABINOID; EXCITATORY AMINO ACID; GLUCOCORTICOID;

ADAPTATION; ANXIETY; ANXIETY DISORDER; ARTICLE; BRAIN; CELL SURFACE; CYTOSKELETON; DEPRESSION; EPIGENETICS; GENE EXPRESSION; GENETIC REGULATION; GENOMIC INSTABILITY; HISTONE MODIFICATION; HUMAN; HYDROXYMETHYLATION; METHYLATION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; RETROPOSON; STRESS; TRANSPOSON; ANIMAL; GENETIC EPIGENESIS; MENTAL STRESS; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; BRAIN; EPIGENESIS, GENETIC; HUMANS; NEURONAL PLASTICITY; STRESS, PSYCHOLOGICAL;

EID: 84942411681     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4086     Document Type: Article

References (141)

1. McEwen, B.S. Protective and damaging effects of stress mediators. N. Engl. J. Med. 338, 171-179 (1998)
2. McEwen, B.S. Protective and damaging effects of stress mediators: central role of the brain. Dialogues Clin. Neurosci. 8, 367-381 (2006)
3. McEwen, B.S. &Wingfield, J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 43, 2-15 (2003)
4. Shonkoff, J.P., Boyce, W.T. &McEwen, B.S. Neuroscience, molecular biology, and the childhood roots of health disparities. J. Am. Med. Assoc. 301, 2252-2259 (2009)
5. McEwen, B.S. Brain on stress: how the social environment gets under the skin. Proc. Natl. Acad. Sci. USA 109 (suppl. 2): 17180-17185 (2012)
6. Halfon, N., Larson, K., Lu, M., Tullis, E. &Russ, S. Lifecourse health development: past, present and future. Matern. Child Health J. 18, 344-365 (2014)
7. Felitti, V.J. et al. Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am. J. Prev. Med. 14, 245-258 (1998)
8. Tost, H., Champagne, F.A &Meyer-Lindenberg, A. Environmental influence in the brain, human welfare and mental health. Nat. Neurosci. 18, 1421-1431 (2015)
9. McEwen, B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105-122 (1999)
10. McEwen, B.S. &Chattarji, S. in Handbook of Neurochemistry and Molecular Neurobiology (A. Lajtha &G. Baker, eds.) 572-593 (Springer-Verlag, 2007)
11. Cameron, H.A. &Gould, E. in Receptor Dynamics in Neural Development Pharmacology and Toxicology: Basic and Clinical Aspects (ed. C.A. Shaw) 141-157 (CRC Press, 1996)
12. McEwen, B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904 (2007)
13. McEwen, B.S. Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. NY Acad. Sci. 1204 (suppl.): E38-E59 (2010)
14. Meaney, M.J. &Szyf, M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin. Neurosci. 7, 103-123 (2005)
15. Hunter, R.G., Gagnidze, K., McEwen, B.S. &Pfaff, D.W. Stress and the dynamic genome: steroids, epigenetics, and the transposome. Proc. Natl. Acad. Sci. USA 112, 6828-6833 (2015)
16. McEwen, B.S., Weiss, J. &Schwartz, L. Selective retention of corticosterone by limbic structures in rat brain. Nature 220, 911-912 (1968)
17. Rubin, T.G., Gray, J.D. &McEwen, B.S. Experience and the ever-changing brain: what the transcriptome can reveal. BioEssays 36, 1072-1081 (2014)
18. Gray, J.D., Rubin, T.G., Hunter, R.G. &McEwen, B.S. Hippocampal gene expression changes underlying stress sensitization and recovery. Mol. Psychiatry 19, 1171-1178 (2014)
19. Wang, K. et al. Transcriptome profiling analysis reveals region-distinctive changes of gene expression in the CNS in response to different moderate restraint stress. J. Neurochem. 113, 1436-1446 (2010)
20. Datson, N.A. et al. Previous history of chronic stress changes the transcriptional response to glucocorticoid challenge in the dentate gyrus region of the male rat hippocampus. Endocrinology 154, 3261-3272 (2013)
21. de Kloet, E.R., Fitzsimons, C.P., Datson, N.A., Meijer, O.C. &Vreugdenhil, E. Glucocorticoid signaling and stress-related limbic susceptibility pathway: about receptors, transcription machinery and microRNA. Brain Res. 1293, 129-141 (2009)
22. Goldwater, D.S. et al. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 164, 798-808 (2009)
23. Hunter, R.G. &McEwen, B.S. Stress and anxiety across the lifespan: structural plasticity and epigenetic regulation. Epigenomics 5, 177-194 (2013)
24. Griffiths, B.B. &Hunter, R.G. Neuroepigenetics of stress. Neuroscience 275, 420-435 (2014)
25. Reul, J.M. Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways. Frontiers Psychiatry 5, 5 (2014)
26. Tsankova, N.M. et al. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9, 519-525 (2006)
27. Reul, J.M.H.M. &Chandramohan, Y. Epigenetic mechanisms in stress-related memory formation. Psychoneuroendocrinology 32, S21-S25 (2007)
28. Heller, E.A. et al. Locus-specific epigenetic remodeling controls addiction-and depression-related behaviors. Nat. Neurosci. 17, 1720-1727 (2014)
29. Nasca, C. et al. l-Acetylcarnitine causes rapid antidepressant effects through the epigenetic induction of mGlu2 receptors. Proc. Natl. Acad. Sci. USA 110, 4804-4809 (2013)
30. Dyrvig, M., Gotzsche, C.R., Woldbye, D.P. &Lichota, J. Epigenetic regulation of Dnmt3a and Arc gene expression after electroconvulsive stimulation in the rat. Mol. Cell Neurosci. 67, 137-143 (2015)
31. Hunter, R.G., McCarthy, K.J., Milne, T.A., Pfaff, D.W. &McEwen, B.S. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc. Natl. Acad. Sci. USA 106, 20912-20917 (2009)
32. Popoli, M., Yan, Z., McEwen, B.S. &Sanacora, G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev. Neurosci. 13, 22-37 (2012)
33. Monteggia, L.M. &Zarate, C. Jr. Antidepressant actions of ketamine: from molecular mechanisms to clinical practice. Curr. Opin. Neurobiol. 30, 139-143 (2015)
34. Erwin, J.A., Marchetto, M.C. &Gage, F.H. Mobile DNA elements in the generation of diversity and complexity in the brain. Nat. Rev. Neurosci. 15, 497-506 (2014)
35. Reilly, M.T., Faulkner, G.J., Dubnau, J., Ponomarev, I. &Gage, F.H. The role of transposable elements in health and diseases of the central nervous system. J. Neurosci. 33, 17577-17586 (2013)
36. Hunter, R.G., McEwen, B.S. &Pfaff, D.W. Environmental stress and transposon transcription in the mammalian brain. Mob. Genet. Elements 3, e24555 (2013)
37. Khalil, A.M. et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc. Natl. Acad. Sci. USA 106, 11667-11672 (2009)
38. Johnson, R. &Guigo, R. The RIDL hypothesis: transposable elements as functional domains of long noncoding RNAs. RNA 20, 959-976 (2014)
39. Kelley, D. &Rinn, J. Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome Biol. 13, R107 (2012)
40. Khalil, A.M. &Rinn, J.L. RNA-protein interactions in human health and disease. Semin. Cell Dev. Biol. 22, 359-365 (2011)
41. Pauli, A., Rinn, J.L. &Schier, A.F. Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 12, 136-149 (2011)
42. McClintock, B. Chromosome organization and genic expression. Cold Spring Harb. Symp. Quant. Biol. 16, 13-47 (1951)
43. McClintock, B. The significance of responses of the genome to challenge. Science 226, 792-801 (1984)
44. Rusiecki, J.A. et al. DNA methylation in repetitive elements and post-traumatic stress disorder: a case-control study of US military service members. Epigenomics 4, 29-40 (2012)
45. Ponomarev, I., Rau, V., Eger, E.I., Harris, R.A. &Fanselow, M.S. Amygdala transcriptome and cellular mechanisms underlying stress-enhanced fear learning in a rat model of posttraumatic stress disorder. Neuropsychopharmacology 35, 1402-1411 (2010)
46. Ponomarev, I., Wang, S., Zhang, L., Harris, R.A. &Mayfield, R.D. Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence. J. Neurosci. 32, 1884-1897 (2012)
47. Lowy, M.T., Gault, L. &Yamamoto, B.K. Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J. Neurochem. 61, 1957-1960 (1993)
48. Karst, H. et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. USA 102, 19204-19207 (2005)
49. Treccani, G. et al. Stress and corticosterone increase the readily releasable pool of glutamate vesicles in synaptic terminals of prefrontal and frontal cortex. Mol. Psychiatry 19, 433-443 (2014)
50. Magariños, 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 69, 89-98 (1995)
51. Watanabe, Y., Gould, E. &McEwen, B.S. Stress induces atrophy of apical dendrites of hippocampus CA3 pyramidal neurons. Brain Res. 588, 341-345 (1992)
52. Martin, K.P. &Wellman, C.L. NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb. Cortex 21, 2366-2373 (2011)
53. Sapolsky, R.M., Krey, L.C. &McEwen, B.S. The neuroendocrinology of stress and aging: the glucocorticoid cascade hypothesis. Endocr. Rev. 7, 284-301 (1986)
54. Lisman, J.E. Relating hippocampal circuitry to function: recall of memory sequences by reciprocal dentate-CA3 interactions. Neuron 22, 233-242 (1999)
55. McEwen, B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105-122 (1999)
56. Magariños, A.M., McEwen, B.S., Saboureau, M. &Pevet, P. Rapid and reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc. Natl. Acad. Sci. USA 103, 18775-18780 (2006)
57. Popov, V.I., Bocharova, L.S. &Bragin, A.G. Repeated changes of dendritic morphology in the hippocampus of ground squirrels in the course of hibernation. Neuroscience 48, 45-51 (1992)
58. McCall, T. et al. Depletion of polysialic acid from neural cell adhesion molecule (PSA-NCAM) increases CA3 dendritic arborization and increases vulnerability to excitotoxicity. Exp. Neurol. 241, 5-12 (2013)
59. Joëls, M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol. Sci. 27, 244-250 (2006)
60. Revollo, J.R. &Cidlowski, J.A. Mechanisms generating diversity in glucocorticoid receptor signaling. Ann. NY Acad. Sci. 1179, 167-178 (2009)
61. Hill, M.N. &McEwen, B.S. Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 791-797 (2010)
62. Du, J. et al. Dynamic regulation of mitochondrial function by glucocorticoids. Proc. Natl. Acad. Sci. USA 106, 3543-3548 (2009)
63. Wei, Q. et al. Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional lability. Proc. Natl. Acad. Sci. USA 101, 11851-11856 (2004)
64. Jacobson, L. Forebrain glucocorticoid receptor gene deletion attenuates behavioral changes and antidepressant responsiveness during chronic stress. Brain Res. 1583, 109-121 (2014)
65. Szyf, M., Weaver, I.C.G., Champagne, F.A., Diorio, J. &Meaney, M.J. Maternal programming of steroid receptor expression and phenotype through DNA methylation in the rat. Front. Neuroendocrinol. 26, 139-162 (2005)
66. McGowan, P.O. et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat. Neurosci. 12, 342-348 (2009)
67. Rao, R.P., Anilkumar, S., McEwen, B.S. &Chattarji, S. Glucocorticoids protect against the delayed behavioral and cellular effects of acute stress on the amygdala. Biol. Psychiatry 72, 466-475 (2012)
68. Zohar, J. et al. High dose hydrocortisone immediately after trauma may alter the trajectory of PTSD: interplay between clinical and animal studies. Eur. Neuropsychopharmacol. 21, 796-809 (2011)
69. Schelling, G., Roozendaal, B. &De Quervain, D.J.-F. Can posttraumatic stress disorder be prevented with glucocorticoids? Ann. NY Acad. Sci. 1032, 158-166 (2004)
70. Mitra, R. &Sapolsky, R.M. Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc. Natl. Acad. Sci. USA 105, 5573-5578 (2008)
71. Nasca, C., Bigio, B., Zelli, D., Nicoletti, F. &McEwen, B.S. Mind the gap: glucocorticoids modulate hippocampal glutamate tone underlying individual differences in stress susceptibility. Mol. Psychiatry 20, 755-763 (2015)
72. Francis, D., Diorio, J., Liu, D. &Meaney, M.J. Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286, 1155-1158 (1999)
73. Pawlak, R. et al. Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc. Natl. Acad. Sci. USA 102, 18201-18206 (2005)
74. Chen, Y., Fenoglio, K.A., Dube, C.M., Grigoriadis, D.E. &Baram, T.Z. Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol. Psychiatry 11, 992-1002 (2006)
75. Bennur, S. et al. Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 144, 8-16 (2007)
76. Matys, T. et al. Tissue plasminogen activator promotes the effects of corticotropin releasing factor on the amygdala and anxiety-like behavior. Proc. Natl. Acad. Sci. USA 101, 16345-16350 (2004)
77. Mucha, M. et al. Lipocalin-2 controls neuronal excitability and anxiety by regulating dendritic spine formation and maturation. Proc. Natl. Acad. Sci. USA 108, 18436-18441 (2011)
78. Skrzypiec, A.E. et al. Stress-induced lipocalin-2 controls dendritic spine formation and neuronal activity in the amygdala. PLoS ONE 8, e61046 (2013)
79. Hill, M.N. et al. Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. J. Neurosci. 31, 10506-10515 (2011)
80. Hill, M.N. et al. Endogenous cannabinoid signaling is essential for stress adaptation. Proc. Natl. Acad. Sci. USA 107, 9406-9411 (2010)
81. Hill, M.N., Hillard, C.J. &McEwen, B.S. Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb. Cortex 21, 2056-2064 (2011)
82. Lee, T.T., Filipski, S.B., Hill, M.N. &McEwen, B.S. Morphological and behavioral evidence for impaired prefrontal cortical function in female CB1 receptor deficient mice. Behav. Brain Res. 271, 106-110 (2014)
83. Hill, M.N. et al. Downregulation of endocannabinoid signaling in the hippocampus following chronic unpredictable stress. Neuropsychopharmacology 30, 508-515 (2005)
84. Bowles, N.P. et al. Chronic, noninvasive glucocorticoid administration suppresses limbic endocannabinoid signaling in mice. Neuroscience 204, 83-89 (2012)
85. Mitra, R., Jadhav, S., McEwen, B.S., Vyas, A. &Chattarji, S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. USA 102, 9371-9376 (2005)
86. Lomazzo, E. et al. Therapeutic potential of inhibitors of endocannabinoid degradation for the treatment of stress-related hyperalgesia in an animal model of chronic pain. Neuropsychopharmacology 40, 488-501 (2015)
87. Bortolato, M. et al. Antidepressant-like activity of the fatty acid amide hydrolase inhibitor URB597 in a rat model of chronic mild stress. Biol. Psychiatry 62, 1103-1110 (2007)
88. Rossi, S. et al. Preservation of striatal cannabinoid CB1 receptor function correlates with the antianxiety effects of fatty acid amide hydrolase inhibition. Mol. Pharmacol. 78, 260-268 (2010)
89. Tsankova, N., Renthal, W., Kumar, A. &Nestler, E.J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 8, 355-367 (2007)
90. Zoppi, S. et al. Regulatory role of cannabinoid receptor 1 in stress-induced excitotoxicity and neuroinflammation. Neuropsychopharmacology 36, 805-818 (2011)
91. Gray, J.M. et al. Corticotropin-releasing hormone drives anandamide hydrolysis in the amygdala to promote anxiety. J. Neurosci. 35, 3879-3892 (2015)
92. Daskalakis, N.P., Cohen, H., Cai, G., Buxbaum, J.D. &Yehuda, R. Expression profiling associates blood and brain glucocorticoid receptor signaling with trauma-related individual differences in both sexes. Proc. Natl. Acad. Sci. USA 111, 13529-13534 (2014)
93. Govindarajan, A. et al. Transgenic brain-derived neurotrophic factor expression causes both anxiogenic and antidepressant effects. Proc. Natl. Acad. Sci. USA 103, 13208-13213 (2006)
94. Lakshminarasimhan, H. &Chattarji, S. Stress leads to contrasting effects on the levels of brain derived neurotrophic factor in the hippocampus and amygdala. PLoS ONE 7, e30481 (2012)
95. Gray, J.D., Milner, T.A. &McEwen, B.S. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 239, 214-227 (2013)
96. Suri, D. et al. Early stress evokes age-dependent biphasic changes in hippocampal neurogenesis, BDNF expression, and cognition. Biol. Psychiatry 73, 658-666 (2013)
97. Seki, T. &Arai, Y. Different polysialic acid-neural cell adhesion molecule expression patterns in distinct types of mossy fiber boutons in the adult hippocampus. J. Comp. Neurol. 410, 115-125 (1999)
98. Rutishauser, U. Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nat. Rev. Neurosci. 9, 26-35 (2008)
99. Theodosis, D.T., Bonhomme, R., Vitiello, S., Rougon, G. &Poulain, D.A. Cell surface expression of polysialic acid on NCAM is a prerequisite for activity-dependent morphological neuronal and glial plasticity. J. Neurosci. 19, 10228-10236 (1999)
100. Pham, K., Nacher, J., Hof, P.R. &McEwen, B.S. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 17, 879-886 (2003)
101. Sandi, C. Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 5, 917-930 (2004)
102. van der Kooij, M.A. et al. Impaired hippocampal neuroligin-2 function by chronic stress or synthetic peptide treatment is linked to social deficits and increased aggression. Neuropsychopharmacology 39, 1148-1158 (2014)
103. Wood, G.E., Young, L.T., Reagan, L.P. &McEwen, B.S. Acute and chronic restraint stress alter the incidence of social conflict in male rats. Horm. Behav. 43, 205-213 (2003)
104. van der Kooij, M.A. et al. Role for MMP-9 in stress-induced downregulation of nectin-3 in hippocampal CA1 and associated behavioural alterations. Nat. Commun. 5, 4995 (2014)
105. Matus, A., Brinkhaus, H. &Wagner, U. Actin dynamics in dendritic spines: a form of regulated plasticity at excitatory synapses. Hippocampus 10, 555-560 (2000)
106. Arendt, T. et al. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 23, 6972-6981 (2003)
107. Morris, M., Maeda, S., Vossel, K. &Mucke, L. The many faces of tau. Neuron 70, 410-426 (2011)
108. Kinoshita, Y. et al. Role for NUP62 depletion and PYK2 redistribution in dendritic retraction resulting from chronic stress. Proc. Natl. Acad. Sci. USA 111, 16130-16135 (2014)
109. Tochigi, M. et al. Gene expression profiling of major depression and suicide in the prefrontal cortex of postmortem brains. Neurosci. Res. 60, 184-191 (2008)
110. Gould, E., McEwen, B.S., Tanapat, P., Galea, L.A.M. &Fuchs, E. Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J. Neurosci. 17, 2492-2498 (1997)
111. Gould, E., Tanapat, P., McEwen, B.S., Flugge, G. &Fuchs, E. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc. Natl. Acad. Sci. USA 95, 3168-3171 (1998)
112. Cameron, H.A. &Gould, E. Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209 (1994)
113. Leuner, B., Glasper, E.R. &Gould, E. Sexual experience promotes adult neurogenesis in the hippocampus despite an initial elevation in stress hormones. PLoS ONE 5, e11597 (2010)
114. Leuner, B., Caponiti, J.M. &Gould, E. Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22, 861-868 (2012)
115. Lightman, S.L. et al. The significance of glucocorticoid pulsatility. Eur. J. Pharmacol. 583, 255-262 (2008)
116. Liston, C. &Gan, W.B. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc. Natl. Acad. Sci. USA 108, 16074-16079 (2011)
117. Liston, C. et al. Circadian glucocorticoid oscillations promote learning-dependent synapse formation and maintenance. Nat. Neurosci. 16, 698-705 (2013)
118. Akana, S.F., Jacobson, L., Cascio, C.S., Shinsako, J. &Dallman, M.F. Constant corticosterone replacement normalizes basal adrenocorticotropin (ACTH) but permits sustained ACTH hypersecretion after stress in adrenalectomized rats. Endocrinology 122, 1337-1342 (1988)
119. Karatsoreos, I.N. &McEwen, B.S. Timing is everything: a collection on how clocks affect resilience in biological systems. F1000 Res. 3, 273 (2014)
120. Seeman, T., Epel, E., Gruenewald, T., Karlamangla, A. &McEwen, B.S. Socio-economic differentials in peripheral biology: cumulative allostatic load. Ann. NY Acad. Sci. 1186, 223-239 (2010)
121. Karatsoreos, I.N. &McEwen, B.S. Psychobiological allostasis: resistance, resilience and vulnerability. Trends Cogn. Sci. 15, 576-584 (2011)
122. Radley, J.J. et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125, 1-6 (2004)
123. Karatsoreos, I.N., Bhagat, S., Bloss, E.B., Morrison, J.H. &McEwen, B.S. Disruption of circadian clocks has ramifications for metabolism, brain, and behavior. Proc. Natl. Acad. Sci. USA 108, 1657-1662 (2011)
124. Phillips, D.J., Savenkova, M.I. &Karatsoreos, I.N. Environmental disruption of the circadian clock leads to altered sleep and immune responses in mouse. Brain Behav. Immun. 47, 14-23 (2015)
125. Lamont, E.W., Robinson, B., Stewart, J. &Amir, S. The central and basolateral nuclei of the amygdala exhibit opposite diurnal rhythms of expression of the clock protein Period2. Proc. Natl. Acad. Sci. USA 102, 4180-4184 (2005)
126. Reddy, A.B. et al. Glucocorticoid signaling synchronizes the liver circadian transcriptome. Hepatology 45, 1478-1488 (2007)
127. McEwen, B.S., Gray, J. &Nasca, C. Recognizing resilience: learning from the effects of stress on the brain. Neurobiol. Stress 1, 1-11 (2015)
128. Russo, S.J., Murrough, J.W., Han, M.H., Charney, D.S. &Nestler, E.J. Neurobiology of resilience. Nat. Neurosci. 15, 1475-1484 (2012)
129. Waddington, C.H. The epigenotype. Endeavour 1, 18-20 (1942)
130. Bavelier, D., Levi, D.M., Li, R.W., Dan, Y. &Hensch, T.K. Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J. Neurosci. 30, 14964-14971 (2010)
131. Castrén, E. &Rantamaki, T. The role of BDNF and its receptors in depression and antidepressant drug action: Reactivation of developmental plasticity. Dev. Neurobiol. 70, 289-297 (2010)
132. McEwen, B.S. &Gianaros, P.J. Stress-and allostasis-induced brain plasticity. Annu. Rev. Med. 62, 431-445 (2011)
133. Yan, X.-X., Toth, Z., Schultz, L., Ribak, C.E. &Baram, T.Z. Corticotropin-releasing hormone (CRH)-containing neurons in the immature rat hippocampal formation: light and electron microscopic features and colocalization with glutamate decarboxylase and parvalbumin. Hippocampus 8, 231-243 (1998)
134. Hill, M.N. &McEwen, B.S. Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 791-797 (2010)
135. Gunduz-Cinar, O., Hill, M.N., McEwen, B.S. &Holmes, A. Amygdala FAAH and anandamide: mediating protection and recovery from stress. Trends Pharmacol. Sci. 34, 637-644 (2013)
136. Hill, M.N. et al. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdalar microstructure. Mol. Psychiatry 18, 1125-1135 (2013)
137. Vyas, A., Mitra, R., Rao, B.S.S. &Chattarji, S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J. Neurosci. 22, 6810-6818 (2002)
138. Liston, C. et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J. Neurosci. 26, 7870-7874 (2006)
139. McEwen, B.S. &Morrison, J.H. The brain on stress: vulnerability and plasticity of the prefrontal cortex over the life course. Neuron 79, 16-29 (2013)
140. Du, J., McEwen, B.S. &Manji, H.K. Glucocorticoid receptors modulate mitochondrial function. Commun. Integr. Biol. 2, 350-352 (2009)
141. Armanini, M.P., Hutchings, C., Stein, B. &Sapolsky, R. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res. 532, 7-12 (1990)