The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course

Neuron

Volumn 79, Issue 1, 2013, Pages 16-29

  McEwen, BruceS ^a   Morrison, JohnH ^b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ESTROGEN; TRANSCRIPTION FACTOR CLOCK;

ACUTE STRESS; AGING; AMYGDALOID NUCLEUS; AUTOREGULATION; BRAIN DEVELOPMENT; CHRONIC STRESS; CIRCADIAN RHYTHM; COGNITION; EMOTION; HIPPOCAMPUS; HUMAN; IMMOBILIZATION STRESS; LONG TERM POTENTIATION; MENTAL STRESS; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SEX DIFFERENCE; SPATIAL MEMORY; WORKING MEMORY;

COGNITION; HUMANS; LIFE CHANGE EVENTS; MEMORY, SHORT-TERM; NEURONAL PLASTICITY; PREFRONTAL CORTEX; STRESS, PSYCHOLOGICAL;

EID: 84880008715     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.06.028     Document Type: Review

References (160)

1. Ahima R.S., Harlan R.E. Charting of type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system. Neuroscience 1990, 39:579-604.
2. Ahima R., Krozowski Z., Harlan R. Type I corticosteroid receptor-like immunoreactivity in the rat CNS: distribution and regulation by corticosteroids. J.Comp. Neurol. 1991, 313:522-538.
3. Akers K.G., Yang Z., DelVecchio D.P., Reeb B.C., Romeo R.D., McEwen B.S., Tang A.C. Social competitiveness and plasticity of neuroendocrine function in old age: influence of neonatal novelty exposure and maternal care reliability. PLoS ONE 2008, 3:e2840.
4. Akirav I., Richter-Levin G. Biphasic modulation of hippocampal plasticity by behavioral stress and basolateral amygdala stimulation in the rat. J.Neurosci. 1999, 19:10530-10535.
5. Anda R.F., Butchart A., Felitti V.J., Brown D.W. Building a framework for global surveillance of the public health implications of adverse childhood experiences. Am. J. Prev. Med. 2010, 39:93-98.
6. Ansell E.B., Rando K., Tuit K., Guarnaccia J., Sinha R. Cumulative adversity and smaller gray matter volume in medial prefrontal, anterior cingulate, and insula regions. Biol. Psychiatry 2012, 72:57-64.
7. Arnsten A.F. Ameliorating prefrontal cortical dysfunction in mental illness: inhibition of phosphotidyl inositol-protein kinase C signaling. Psychopharmacology (Berl.) 2009, 202:445-455.
8. Arnsten A.F. Stress signalling pathways that impair prefrontal cortex structure and function. Nat. Rev. Neurosci. 2009, 10:410-422.
9. Arnsten A.F., Paspalas C.D., Gamo N.J., Yang Y., Wang M. Dynamic Network Connectivity: A new form of neuroplasticity. Trends Cogn. Sci. 2010, 14:365-375.
10. Arnsten A.F., Wang M.J., Paspalas C.D. Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron 2012, 76:223-239.
11. Atsak P., Hauer D., Campolongo P., Schelling G., McGaugh J.L., Roozendaal B. Glucocorticoids interact with the hippocampal endocannabinoid system in impairing retrieval of contextual fear memory. Proc. Natl. Acad. Sci. USA 2012, 109:3504-3509.
12. Barbas H., Saha S., Rempel-Clower N., Ghashghaei T. Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neurosci. 2003, 4:25.
13. Barense M.D., Fox M.T., Baxter M.G. Aged rats are impaired on an attentional set-shifting task sensitive to medial frontal cortex damage in young rats. Learn. Mem. 2002, 9:191-201.
14. Barsegyan A., Mackenzie S.M., Kurose B.D., McGaugh J.L., Roozendaal B. Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism. Proc. Natl. Acad. Sci. USA 2010, 107:16655-16660.
15. 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. 2010, 30:14964-14971.
16. Bennett E.L., Diamond M.C., Krech D., Rosenzweig M.R. Chemical and anatomical plasticity of brain. Science 1964, 146:610-619.
17. Berntson G.G., Cacioppo J.T. Integrative physiology: homeostasis, allostasis and the orchestration of systemic physiology. Handbook of Psychophysiology 2007, 433-452. Cambridge University Press, Cambridge. J.T. Cacioppo, L.G. Tassinary, G.G. Berntson (Eds.).
18. Bezzola L., Mérillat S., Gaser C., Jäncke L. Training-induced neural plasticity in golf novices. J.Neurosci. 2011, 31:12444-12448.
19. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J.Neurosci. 2000, 20:4320-4324.
20. Blake D.T., Heiser M.A., Caywood M., Merzenich M.M. Experience-dependent adult cortical plasticity requires cognitive association between sensation and reward. Neuron 2006, 52:371-381.
21. Bloss E.B., Janssen W.G., McEwen B.S., Morrison J.H. Interactive effects of stress and aging on structural plasticity in the prefrontal cortex. J.Neurosci. 2010, 30:6726-6731.
22. Bloss E.B., Janssen W.G., Ohm D.T., Yuk F.J., Wadsworth S., Saardi K.M., McEwen B.S., Morrison J.H. Evidence for reduced experience-dependent dendritic spine plasticity in the aging prefrontal cortex. J.Neurosci. 2011, 31:7831-7839.
23. Cahill L. Why sex matters for neuroscience. Nat. Rev. Neurosci. 2006, 7:477-484.
24. Campolongo P., Roozendaal B., Trezza V., Hauer D., Schelling G., McGaugh J.L., Cuomo V. Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc. Natl. Acad. Sci. USA 2009, 106:4888-4893.
25. Casey B.J., Giedd J.N., Thomas K.M. Structural and functional brain development and its relation to cognitive development. Biol. Psychol. 2000, 54:241-257.
26. Casey B.J., Somerville L.H., Gotlib I.H., Ayduk O., Franklin N.T., Askren M.K., Jonides J., Berman M.G., Wilson N.L., Teslovich T., et al. Behavioral and neural correlates of delay of gratification 40 years later. Proc. Natl. Acad. Sci. USA 2011, 108:14998-15003.
27. Cerqueira J.J., Pêgo J.M., Taipa R., Bessa J.M., Almeida O.F.X., Sousa N. Morphological correlates of corticosteroid-induced changes in prefrontal cortex-dependent behaviors. J.Neurosci. 2005, 25:7792-7800.
28. Cerqueira J.J., Mailliet F., Almeida O.F.X., Jay T.M., Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J.Neurosci. 2007, 27:2781-2787.
29. Cho K. Chronic 'jet lag' produces temporal lobe atrophy and spatial cognitive deficits. Nat. Neurosci. 2001, 4:567-568.
30. Colcombe S.J., Kramer A.F., Erickson K.I., Scalf P., McAuley E., Cohen N.J., Webb A., Jerome G.J., Marquez D.X., Elavsky S. Cardiovascular fitness, cortical plasticity, and aging. Proc. Natl. Acad. Sci. USA 2004, 101:3316-3321.
31. Cook S.C., Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J.Neurobiol. 2004, 60:236-248.
32. Crombag H.S., Gorny G., Li Y., Kolb B., Robinson T.E. Opposite effects of amphetamine self-administration experience on dendritic spines in the medial and orbital prefrontal cortex. Cereb. Cortex 2005, 15:341-348.
33. Danese A., McEwen B.S. Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiol. Behav. 2012, 106:29-39.
34. de Lange F.P., Koers A., Kalkman J.S., Bleijenberg G., Hagoort P., van der Meer J.W.M., Toni I. Increase in prefrontal cortical volume following cognitive behavioural therapy in patients with chronic fatigue syndrome. Brain 2008, 131:2172-2180.
35. Diorio D., Viau V., Meaney M.J. The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J.Neurosci. 1993, 13:3839-3847.
36. Draganski B., Gaser C., Kempermann G., Kuhn H.G., Winkler J., Büchel C., May A. Temporal and spatial dynamics of brain structure changes during extensive learning. J.Neurosci. 2006, 26:6314-6317.
37. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386:824-827.
38. Drevets W.C., Price J.L., Simpson J.R., Todd R.D., Reich T., Vannier M., Raichle M.E. Subgenual prefrontal cortex abnormalities in mood disorders. Nature 1997, 386:824-827.
39. Duckworth A.L., Kim B., Tsukayama E. Life stress impairs self-control in early adolescence. Front Psychol 2012, 3:608.
40. Dumitriu D., Hao J., Hara Y., Kaufmann J., Janssen W.G., Lou W., Rapp P.R., Morrison J.H. Selective changes in thin spine density and morphology in monkey prefrontal cortex correlate with aging-related cognitive impairment. J.Neurosci. 2010, 30:7507-7515.
41. Dumitriu D., Rapp P.R., McEwen B.S., Morrison J.H. Estrogen and the aging brain: an elixir for the weary cortical network. Ann. N Y Acad. Sci. 2010, 1204:104-112.
42. Edmiston E.E., Wang F., Mazure C.M., Guiney J., Sinha R., Mayes L.C., Blumberg H.P. Corticostriatal-limbic gray matter morphology in adolescents with self-reported exposure to childhood maltreatment. Arch. Pediatr. Adolesc. Med. 2011, 165:1069-1077.
43. Eiland L., McEwen B.S. Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus 2012, 22:82-91.
44. Eiland L., Ramroop J., Hill M.N., Manley J., McEwen B.S. Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 2012, 37:39-47.
45. Evans G.W., Wachs T.D. Chaos and Its Influence on Children's Development: An Ecological Perspective 2010, American Psychological Association, Washington, DC. First Edition.
46. Evans G.W., Gonnella C., Marcynyszyn L.A., Gentile L., Salpekar N. The role of chaos in poverty and children's socioemotional adjustment. Psychol. Sci. 2005, 16:560-565.
47. Felitti V.J., Anda R.F., Nordenberg D., Williamson D.F., Spitz A.M., Edwards V., Koss M.P., Marks J.S. 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. 1998, 14:245-258.
48. Funahashi S., Bruce C.J., Goldman-Rakic P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J.Neurophysiol. 1989, 61:331-349.
49. Fuster J.M. The Prefrontal Cortex 2008, Academic Press, London. Fourth Edition.
50. Galea L.A.M., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997, 81:689-697.
51. Gallagher M., Rapp P.R. The use of animal models to study the effects of aging on cognition. Annu. Rev. Psychol. 1997, 48:339-370.
52. Gamo N.J., Arnsten A.F. Molecular modulation of prefrontal cortex: rational development of treatments for psychiatric disorders. Behav. Neurosci. 2011, 125:282-296.
53. García-Tardón N., González-González I.M., Martínez-Villarreal J., Fernández-Sánchez E., Giménez C., Zafra F. Protein kinase C (PKC)-promoted endocytosis of glutamate transporter GLT-1 requires ubiquitin ligase Nedd4-2-dependent ubiquitination but not phosphorylation. J.Biol. Chem. 2012, 287:19177-19187.
54. Garrett J.E., Wellman C.L. Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 2009, 162:195-207.
55. Gazzaley A., Nobre A.C. Top-down modulation: bridging selective attention and working memory. Trends Cogn. Sci. 2012, 16:129-135.
56. Gee D.G., Humphreys K.L., Flannery J., Goff B., Telzer E.H., Shapiro M., Hare T.A., Bookheimer S.Y., Tottenham N. A developmental shift from positive to negative connectivity in human amygdala-prefrontal circuitry. J.Neurosci. 2013, 33:4584-4593.
57. Ghashghaei H.T., Barbas H. Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the rhesus monkey. Neuroscience 2002, 115:1261-1279.
58. Gianaros P.J., Jennings J.R., Sheu L.K., Derbyshire S.W.G., Matthews K.A. Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity. Hypertension 2007, 49:134-140.
59. Gianaros P.J., Hariri A.R., Sheu L.K., Muldoon M.F., Sutton-Tyrrell K., Manuck S.B. Preclinical atherosclerosis covaries with individual differences in reactivity and functional connectivity of the amygdala. Biol. Psychiatry 2009, 65:943-950.
60. Goldman-Rakic P.S. Topography of cognition: parallel distributed networks in primate association cortex. Annu. Rev. Neurosci. 1988, 11:137-156.
61. Goldman-Rakic P.S. Cellular basis of working memory. Neuron 1995, 14:477-485.
62. Goldwater D.S., Pavlides C., Hunter R.G., Bloss E.B., Hof P.R., McEwen B.S., Morrison J.H. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 2009, 164:798-808.
63. 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.
64. 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. USA 2009, 106:17957-17962.
65. Hao J., Rapp P.R., Leffler A.E., Leffler S.R., Janssen W.G., Lou W., McKay H., Roberts J.A., Wearne S.L., Hof P.R., Morrison J.H. Estrogen alters spine number and morphology in prefrontal cortex of aged female rhesus monkeys. J.Neurosci. 2006, 26:2571-2578.
66. Hao J., Rapp P.R., Janssen W.G., Lou W., Lasley B.L., Hof P.R., Morrison J.H. Interactive effects of age and estrogen on cognition and pyramidal neurons in monkey prefrontal cortex. Proc. Natl. Acad. Sci. USA 2007, 104:11465-11470.
67. Hill M.N., McEwen B.S. Endocannabinoids: The silent partner of glucocorticoids in the synapse. Proc. Natl. Acad. Sci. USA 2009, 106:4579-4580.
68. Hof P.R., Morrison J.H. The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci. 2004, 27:607-613.
69. Holmes A., Wellman C.L. Stress-induced prefrontal reorganization and executive dysfunction in rodents. Neurosci. Biobehav. Rev. 2009, 33:773-783.
70. Hölzel B.K., Carmody J., Evans K.C., Hoge E.A., Dusek J.A., Morgan L., Pitman R.K., Lazar S.W. Stress reduction correlates with structural changes in the amygdala. Soc. Cogn. Affect. Neurosci. 2010, 5:11-17.
71. Ikegaya Y., Saito H., Abe K. Dentate gyrus field potentials evoked by stimulation of the basolateral amygdaloid nucleus in anesthetized rats. Brain Res. 1996, 718:53-60.
72. Jancke L. Music drives brain plasticity. F1000 Biol. Rep. 2009, 1:78.
73. 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 2011, 108:1657-1662.
74. Kesner R.P., Churchwell J.C. An analysis of rat prefrontal cortex in mediating executive function. Neurobiol. Learn. Mem. 2011, 96:417-431.
75. 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, 25:1532-1539.
76. Kramer A.F., Hahn S., Cohen N.J., Banich M.T., McAuley E., Harrison C.R., Chason J., Vakil E., Bardell L., Boileau R.A., Colcombe A. Ageing, fitness and neurocognitive function. Nature 1999, 400:418-419.
77. Krantz D.S., Manuck S.B. Acute psychophysiologic reactivity and risk of cardiovascular disease: a review and methodologic critique. Psychol. Bull. 1984, 96:435-464.
78. Lenroot R.K., Schmitt J.E., Ordaz S.J., Wallace G.L., Neale M.C., Lerch J.P., Kendler K.S., Evans A.C., Giedd J.N. Differences in genetic and environmental influences on the human cerebral cortex associated with development during childhood and adolescence. Hum. Brain Mapp. 2009, 30:163-174.
79. 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.
80. Liston C., McEwen B.S., Casey B.J. Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc. Natl. Acad. Sci. USA 2009, 106:912-917.
81. Liu R.-J., Aghajanian G.K. Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc. Natl. Acad. Sci. USA 2008, 105:359-364.
82. 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 2006, 103:18775-18780.
83. Markham J.A., Mullins S.E., Koenig J.I. Peri-adolescent maturation of the prefrontal cortex is sex-specific and disrupted by prenatal stress. J.Comp. Neurol. 2012, 521:1828-1843.
84. Martin K.P., Wellman C.L. NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb. Cortex 2011, 21:2366-2373.
85. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castrén E., Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008, 320:385-388.
86. McCarthy M.M. Estradiol and the developing brain. Physiol. Rev. 2008, 88:91-124.
87. McDonald A.J. Organization of amygdaloid projections to the mediodorsal thalamus and prefrontal cortex: a fluorescence retrograde transport study in the rat. J.Comp. Neurol. 1987, 262:46-58.
88. Mcdonald A.J., Mascagni F., Guo L. Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat. Neuroscience 1996, 71:55-75.
89. McEwen B.S. Sleep deprivation as a neurobiologic and physiologic stressor: Allostasis and allostatic load. Metabolism 2006, 55(10, Suppl 2):S20-S23.
90. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2011, 62:431-445.
91. McEwen B.S., Milner T.A. Hippocampal formation: shedding light on the influence of sex and stress on the brain. Brain Res. Brain Res. Rev. 2007, 55:343-355.
92. 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. 2005, 7:103-123.
93. Meijer O.C., de Lange E.C.M., Breimer D.D., de Boer A.G., Workel J.O., de Kloet E.R. Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1A P-glycoprotein knockout mice. Endocrinology 1998, 139:1789-1793.
94. Milad M.R., Quirk G.J. Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 2002, 420:70-74.
95. Miller E.K. The prefrontal cortex and cognitive control. Nat. Rev. Neurosci. 2000, 1:59-65.
96. Miller M.M., Morrison J.H., McEwen B.S. Basal anxiety-like behavior predicts differences in dendritic morphology in the medial prefrontal cortex in two strains of rats. Behav. Brain Res. 2012, 229:280-288.
97. 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.
98. Mischel W., Ebbesen E.B., Zeiss A.R. Cognitive and attentional mechanisms in delay of gratification. J.Pers. Soc. Psychol. 1972, 21:204-218.
99. Mischel W., Ayduk O., Berman M.G., Casey B.J., Gotlib I.H., Jonides J., Kross E., Teslovich T., Wilson N.L., Zayas V., Shoda Y. 'Willpower' over the life span: decomposing self-regulation. Soc. Cogn. Affect. Neurosci. 2011, 6:252-256.
100. Morgan M.A., LeDoux J.E. Differential contribution of dorsal and ventral medial prefrontal cortex to the acquisition and extinction of conditioned fear in rats. Behav. Neurosci. 1995, 109:681-688.
101. Moriceau S., Sullivan R.M. Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 2006, 9:1004-1006.
102. Morrison J.H., Baxter M.G. The ageing cortical synapse: hallmarks and implications for cognitive decline. Nat. Rev. Neurosci. 2012, 13:240-250.
103. Morrison J.H., Hof P.R. Life and death of neurons in the aging brain. Science 1997, 278:412-419.
104. Muhammad A., Carroll C., Kolb B. Stress during development alters dendritic morphology in the nucleus accumbens and prefrontal cortex. Neuroscience 2012, 216:103-109.
105. Mychasiuk R., Gibb R., Kolb B. Prenatal stress alters dendritic morphology and synaptic connectivity in the prefrontal cortex and hippocampus of developing offspring. Synapse 2012, 66:308-314.
106. Nelson E.E., Guyer A.E. The development of the ventral prefrontal cortex and social flexibility. Dev Cogn Neurosci 2011, 1:233-245.
107. Nelson A.J., Iwamoto G.A. Reversibility of exercise-induced dendritic attenuation in brain cardiorespiratory and locomotor areas following exercise detraining. J.Appl. Physiol. 2006, 101:1243-1251.
108. Nelson A.J., Juraska J.M., Musch T.I., Iwamoto G.A. Neuroplastic adaptations to exercise: neuronal remodeling in cardiorespiratory and locomotor areas. J.Appl. Physiol. 2005, 99:2312-2322.
109. Niedhammer I., Lert F., Marne M.J. Prevalence of overweight and weight gain in relation to night work in a nurses' cohort. Int. J. Obes. Relat. Metab. Disord. 1996, 20:625-633.
110. Parker K.J., Buckmaster C.L., Sundlass K., Schatzberg A.F., Lyons D.M. Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc. Natl. Acad. Sci. USA 2006, 103:3000-3005.
111. Pattwell S.S., Duhoux S., Hartley C.A., Johnson D.C., Jing D., Elliott M.D., Ruberry E.J., Powers A., Mehta N., Yang R.R., et al. Altered fear learning across development in both mouse and human. Proc. Natl. Acad. Sci. USA 2012, 109:16318-16323.
112. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res. Brain Res. Rev. 2001, 38:247-289.
113. Pfeifer J.H., Kahn L.E., Merchant J.S., Peake S.J., Veroude K., Masten C.L., Lieberman M.D., Mazziotta J.C., Dapretto M. Longitudinal change in the neural bases of adolescent social self-evaluations: effects of age and pubertal development. J.Neurosci. 2013, 33:7415-7419.
114. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 1992, 106:274-285.
115. Popov V.I., Bocharova L.S. Hibernation-induced structural changes in synaptic contacts between mossy fibres and hippocampal pyramidal neurons. Neuroscience 1992, 48:53-62.
116. Preuss T. Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J.Cogn. Neurosci. 1995, 7:1-24.
117. Qin S., Hermans E.J., van Marle H.J., Luo J., Fernández G. Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol. Psychiatry 2009, 66:25-32.
118. Quirk G.J., Likhtik E., Pelletier J.G., Paré D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J.Neurosci. 2003, 23:8800-8807.
119. Quirk G.J., Garcia R., González-Lima F. Prefrontal mechanisms in extinction of conditioned fear. Biol. Psychiatry 2006, 60:337-343.
120. 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.
121. Radley J.J., Rocher A.B., Janssen W.G.M., Hof P.R., McEwen B.S., Morrison J.H. Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp. Neurol. 2005, 196:199-203.
122. Radley J.J., Arias C.M., Sawchenko P.E. Regional differentiation of the medial prefrontal cortex in regulating adaptive responses to acute emotional stress. J.Neurosci. 2006, 26:12967-12976.
123. Radley J.J., Rocher A.B., Rodriguez A., Ehlenberger D.B., Dammann M., McEwen B.S., Morrison J.H., Wearne S.L., Hof P.R. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J.Comp. Neurol. 2008, 507:1141-1150.
124. Rajkowska G. Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol. Psychiatry 2000, 48:766-777.
125. Rapp P.R., Morrison J.H., Roberts J.A. Cyclic estrogen replacement improves cognitive function in aged ovariectomized rhesus monkeys. J.Neurosci. 2003, 23:5708-5714.
126. Richardson M.P., Strange B.A., Dolan R.J. Encoding of emotional memories depends on amygdala and hippocampus and their interactions. Nat. Neurosci. 2004, 7:278-285.
127. Robinson T.E., Gorny G., Mitton E., Kolb B. Cocaine self-administration alters the morphology of dendrites and dendritic spines in the nucleus accumbens and neocortex. Synapse 2001, 39:257-266.
128. Robinson T.E., Gorny G., Savage V.R., Kolb B. Widespread but regionally specific effects of experimenter- versus self-administered morphine on dendritic spines in the nucleus accumbens, hippocampus, and neocortex of adult rats. Synapse 2002, 46:271-279.
129. Roitman M.F., Na E., Anderson G., Jones T.A., Bernstein I.L. Induction of a salt appetite alters dendritic morphology in nucleus accumbens and sensitizes rats to amphetamine. J.Neurosci. 2002, 22:RC225.
130. Roozendaal B., McReynolds J.R., McGaugh J.L. The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J.Neurosci. 2004, 24:1385-1392.
131. Sallet J., Mars R.B., Noonan M.P., Andersson J.L., O'Reilly J.X., Jbabdi S., Croxson P.L., Jenkinson M., Miller K.L., Rushworth M.F. Social network size affects neural circuits in macaques. Science 2011, 334:697-700.
132. Santini E., Ge H., Ren K., Peña de Ortiz S., Quirk G.J. Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J.Neurosci. 2004, 24:5704-5710.
133. Sesack S.R., Deutch A.Y., Roth R.H., Bunney B.S. Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J.Comp. Neurol. 1989, 290:213-242.
134. Shanmugan S., Epperson C.N. Estrogen and the prefrontal cortex: Towards a new understanding of estrogen's effects on executive functions in the menopause transition. Hum. Brain Mapp. 2012, Published online December 14, 2012. 10.1002/hbm.22218.
135. Shansky R.M., Glavis-Bloom C., Lerman D., McRae P., Benson C., Miller K., Cosand L., Horvath T.L., Arnsten A.F.T. Estrogen mediates sex differences in stress-induced prefrontal cortex dysfunction. Mol. Psychiatry 2004, 9:531-538.
136. Shansky R.M., Rubinow K., Brennan A., Arnsten A.F. The effects of sex and hormonal status on restraint-stress-induced working memory impairment. Behav. Brain Funct. 2006, 2:8.
137. Shansky R.M., Hamo C., Hof P.R., McEwen B.S., Morrison J.H. Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb. Cortex 2009, 19:2479-2484.
138. Shansky R.M., Hamo C., Hof P.R., Lou W., McEwen B.S., Morrison J.H. Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cereb. Cortex 2010, 20:2560-2567.
139. Sisk C.L., Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front. Neuroendocrinol. 2005, 26:163-174.
140. Somerville L.H., Hare T., Casey B.J. Frontostriatal maturation predicts cognitive control failure to appetitive cues in adolescents. J.Cogn. Neurosci. 2011, 23:2123-2134.
141. Spinelli S., Chefer S., Suomi S.J., Higley J.D., Barr C.S., Stein E. Early-life stress induces long-term morphologic changes in primate brain. Arch. Gen. Psychiatry 2009, 66:658-665.
142. Spinelli S., Chefer S., Carson R.E., Jagoda E., Lang L., Heilig M., Barr C.S., Suomi S.J., Higley J.D., Stein E.A. Effects of early-life stress on serotonin(1A) receptors in juvenile Rhesus monkeys measured by positron emission tomography. Biol. Psychiatry 2010, 67:1146-1153.
143. Spolidoro M., Baroncelli L., Putignano E., Maya-Vetencourt J.F., Viegi A., Maffei L. Food restriction enhances visual cortex plasticity in adulthood. Nat Commun 2011, 2:320.
144. Stockmeier C.A., Mahajan G.J., Konick L.C., Overholser J.C., Jurjus G.J., Meltzer H.Y., Uylings H.B.M., Friedman L., Rajkowska G. Cellular changes in the postmortem hippocampus in major depression. Biol. Psychiatry 2004, 56:640-650.
145. Suwazono Y., Dochi M., Sakata K., Okubo Y., Oishi M., Tanaka K., Kobayashi E., Kido T., Nogawa K. A longitudinal study on the effect of shift work on weight gain in male Japanese workers. Obesity (Silver Spring) 2008, 16:1887-1893.
146. Tan H.Y., Callicott J.H., Weinberger D.R. Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cereb. Cortex 2007, 17(Suppl 1):i171-i181.
147. Tang A.C., Yang Z., Reeb-Sutherland B.C., Romeo R.D., McEwen B.S. Maternal modulation of novelty effects on physical development. Proc. Natl. Acad. Sci. USA 2012, 109:2120-2125.
148. Thayer J.F., Brosschot J.F. Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 2005, 30:1050-1058.
149. Thayer J.F., Sternberg E. Beyond heart rate variability: vagal regulation of allostatic systems. Ann. N Y Acad. Sci. 2006, 1088:361-372.
150. Tottenham N., Phuong J., Flannery J., Gabard-Durnam L., Goff B. A negativity bias for ambiguous facial-expression valence during childhood: converging evidence from behavior and facial corrugator muscle responses. Emotion 2013, 13:92-103.
151. Treiber F.A., Kamarck T., Schneiderman N., Sheffield D., Kapuku G., Taylor T. Cardiovascular reactivity and development of preclinical and clinical disease states. Psychosom. Med. 2003, 65:46-62.
152. Turek F.W., Joshu C., Kohsaka A., Lin E., Ivanova G., McDearmon E., Laposky A., Losee-Olson S., Easton A., Jensen D.R., et al. Obesity and metabolic syndrome in circadian Clock mutant mice. Science 2005, 308:1043-1045.
153. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J.Neurosci. 2002, 22:6810-6818.
154. Wang M., Gamo N.J., Yang Y., Jin L.E., Wang X.J., Laubach M., Mazer J.A., Lee D., Arnsten A.F. Neuronal basis of age-related working memory decline. Nature 2011, 476:210-213.
155. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J.Neurobiol. 2001, 49:245-253.
156. Wise S.P. Forward frontal fields: phylogeny and fundamental function. Trends Neurosci. 2008, 31:599-608.
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. USA 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. Yuen G.S., McEwen B.S., Akama K.T. LIM kinase mediates estrogen action on the actin depolymerization factor Cofilin. Brain Res. 2011, 1379:44-52.
160. Yuen E.Y., Wei J., Liu W., Zhong P., Li X., Yan Z. Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 2012, 73:962-977.