Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression

Neuroscience

Volumn 251, Issue , 2013, Pages 33-50

  Licznerski, P ^a   Duman, R S ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Antidepressant; Glutamate; Hippocampus; Neurotrophic factor; Prefrontal cortex; Stress

Indexed keywords

AMITRIPTYLINE; ANTIDEPRESSANT AGENT; BRAIN DERIVED NEUROTROPHIC FACTOR; ESTROGEN; FLUOXETINE; FLUVOXAMINE; IMIPRAMINE; KETAMINE; LITHIUM; MOCLOBEMIDE; PROGESTERONE; ROLIPRAM; SEROTONIN NORADRENALIN REUPTAKE INHIBITOR; SEROTONIN UPTAKE INHIBITOR; TESTOSTERONE;

AMYGDALOID NUCLEUS; ANTIDEPRESSANT ACTIVITY; AUTOPSY; BRAIN CORTEX; BRAIN DYSFUNCTION; CELL COMMUNICATION; CELL DENSITY; CELL STRUCTURE; CONVALESCENCE; DENDRITIC SPINE; DEPRESSION; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG RESEARCH; ELECTROCONVULSIVE THERAPY; HIPPOCAMPUS; HUMAN; LIMBIC CORTEX; MEDICAL RESEARCH; MENTAL STRESS; MOLECULAR MECHANICS; NERVE CELL; NERVE CELL PLASTICITY; NEUROIMAGING; NONHUMAN; PATHOPHYSIOLOGY; PATIENT CARE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; TREATMENT OUTCOME;

ACD; ANTIDEPRESSANT; BD; BDNF; BIPOLAR DISORDER; BRAIN-DERIVED NEUROTROPHIC FACTOR; CAMP RESPONSE ELEMENT-BINDING PROTEIN; CHRONIC RESTRAINT STRESS; CHRONIC UNPREDICTABLE STRESS; CREB; CRS; CUS; DORSAL ANTERIOR CINGULATE; ECS; ELECTROCONVULSIVE SEIZURE; ERK; EXTRACELLULAR-SIGNAL-REGULATED KINASE; FMRI; FORCED SWIM TEST; FST; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLUTAMATE; HIPPOCAMPUS; HPA; HYPOTHALAMIC-PITUITARY-ADRENAL; IES; IL; INESCAPABLE STRESS; INFRALIMBIC; LEARNED HELPLESSNESS; LH; LONG-TERM DEPRESSION; LONG-TERM POTENTIATION; LTD; LTP; MAGNETIC RESONANCE IMAGING; MAJOR DEPRESSIVE DISORDER; MAMMALIAN TARGET OF RAPAMYCIN; MAOI; MAPK-PHOSPHATASE 1; MATERNAL SEPARATION; MDD; MEDIAL PREFRONTAL CORTEX; MKP-1; MONOAMINE OXIDASE INHIBITOR; MPFC; MRI; MS; MTOR; N-METHYL-D-ASPARTATE GLUTAMATE RECEPTOR; NEUROTROPHIC FACTOR; NMDA; OFC; ORBITOFRONTAL CORTEX; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRENATAL STRESS; PS; PTSD; SELECTIVE SEROTONIN RE-UPTAKE INHIBITOR; SSRI; STRESS;

ANIMALS; BRAIN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEPRESSION; HUMANS; NEURONAL PLASTICITY; NEURONS; STRESS, PHYSIOLOGICAL; SYNAPSES;

EID: 84884285513     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.09.057     Document Type: Review

References (252)

1. Ackermann M., Matus A. Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Neurosci 2003, 6:1194-1200.
2. Alcantara-Gonzalez F., Juarez I., Solis O., Martinez-Tellez I., Camacho-Abrego I., Masliah E., Mena R., Flores G. Enhanced dendritic spine number of neurons of the prefrontal cortex, hippocampus, and nucleus accumbens in old rats after chronic donepezil administration. Synapse 2010, 64:786-793.
3. Allain H., Lieury A., Brunet-Bourgin F., Mirabaud C., Trebon P., Le Coz F., Gandon J.M. Antidepressants and cognition: comparative effects of moclobemide, viloxazine and maprotiline. Psychopharmacology (Berl) 1992, 106(Suppl.):S56-S61.
4. Almeida O.P., Lautenschlager N., Vasikaram S., Leedman P., Flicker L. Association between physiological serum concentration of estrogen and the mental health of community-dwelling postmenopausal women age 70years and over. Am J Geriatr Psychiatry 2005, 13:142-149.
5. Alvarez V.A., Sabatini B.L. Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 2007, 30:79-97.
6. Amin Z., Canli T., Epperson C.N. Effect of estrogen-serotonin interactions on mood and cognition. Behav Cogn Neurosci Rev 2005, 4:43-58.
7. Ansorge M.S., Zhou M., Lira A., Hen R., Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 2004, 306:879-881.
8. Autry A.E., Adachi M., Nosyreva E., Na E.S., Los M.F., Cheng P.F., Kavalali E.T., Monteggia L.M. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 2011, 475:91-95.
9. Balschun D., Moechars D., Callaerts-Vegh Z., Vermaercke B., Van Acker N., Andries L., D'Hooge R. Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 2010, 20:684-693.
10. Barbon A., Popoli M., La Via L., Moraschi S., Vallini I., Tardito D., Tiraboschi E., Musazzi L., Giambelli R., Gennarelli M., Racagni G., Barlati S. Regulation of editing and expression of glutamate alpha-amino-propionic-acid (AMPA)/kainate receptors by antidepressant drugs. Biol Psychiatry 2006, 59:713-720.
11. Beneyto M., Kristiansen L.V., Oni-Orisan A., McCullumsmith R.E., Meador-Woodruff J.H. Abnormal glutamate receptor expression in the medial temporal lobe in schizophrenia and mood disorders. Neuropsychopharmacology 2007, 32:1888-1902.
12. Bennur S., Shankaranarayana Rao B.S., Pawlak R., Strickland S., McEwen B.S., Chattarji S. Stress-induced spine loss in the medial amygdala is mediated by tissue-plasminogen activator. Neuroscience 2007, 144:8-16.
13. 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.
14. Bertram C.E., Hanson M.A. Prenatal programming of postnatal endocrine responses by glucocorticoids. Reproduction 2002, 124:459-467.
15. Bessa J.M., Ferreira D., Melo I., Marques F., Cerqueira J.J., Palha J.A., Almeida O.F., Sousa N. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 2009, 14:764-773. 739.
16. Bianchi M., Shah A.J., Fone K.C., Atkins A.R., Dawson L.A., Heidbreder C.A., Hows M.E., Hagan J.J., Marsden C.A. Fluoxetine administration modulates the cytoskeletal microtubular system in the rat hippocampus. Synapse 2009, 63:359-364.
17. 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.
18. Bock J., Gruss M., Becker S., Braun K. Experience-induced changes of dendritic spine densities in the prefrontal and sensory cortex: correlation with developmental time windows. Cereb Cortex 2005, 15:802-808.
19. Bock J., Murmu M.S., Biala Y., Weinstock M., Braun K. Prenatal stress and neonatal handling induce sex-specific changes in dendritic complexity and dendritic spine density in hippocampal subregions of prepubertal rats. Neuroscience 2011, 193:34-43.
20. Boda B., Alberi S., Nikonenko I., Node-Langlois R., Jourdain P., Moosmayer M., Parisi-Jourdain L., Muller D. The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J Neurosci 2004, 24:10816-10825.
21. Bowley M.P., Drevets W.C., Ongur D., Price J.L. Low glial numbers in the amygdala in major depressive disorder. Biol Psychiatry 2002, 52:404-412.
22. Bremner J.D., Vythilingam M., Vermetten E., Nazeer A., Adil J., Khan S., Staib L.H., Charney D.S. Reduced volume of orbitofrontal cortex in major depression. Biol Psychiatry 2002, 51:273-279.
23. Bueller J.A., Aftab M., Sen S., Gomez-Hassan D., Burmeister M., Zubieta J.K. BDNF Val66Met allele is associated with reduced hippocampal volume in healthy subjects. Biol Psychiatry 2006, 59:812-815.
24. Caetano S.C., Hatch J.P., Brambilla P., Sassi R.B., Nicoletti M., Mallinger A.G., Frank E., Kupfer D.J., Keshavan M.S., Soares J.C. Anatomical MRI study of hippocampus and amygdala in patients with current and remitted major depression. Psychiatry Res 2004, 132:141-147.
25. Calhoun M.E., Fletcher B.R., Yi S., Zentko D.C., Gallagher M., Rapp P.R. Age-related spatial learning impairment is unrelated to spinophilin immunoreactive spine number and protein levels in rat hippocampus. Neurobiol Aging 2008, 29:1256-1264.
26. Cavus I., Duman R.S. Influence of estradiol, stress, and 5-HT2A agonist treatment on brain-derived neurotrophic factor expression in female rats. Biol Psychiatry 2003, 54:59-69.
27. Chen G., Manji H.K. The extracellular signal-regulated kinase pathway: an emerging promising target for mood stabilizers. Curr Opin Psychiatry 2006, 19:313-323.
28. Chen Z.Y., Jing D., Bath K.G., Ieraci A., Khan T., Siao C.J., Herrera D.G., Toth M., Yang C., McEwen B.S., Hempstead B.L., Lee F.S. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 2006, 314:140-143.
29. Chen F., Madsen T.M., Wegener G., Nyengaard J.R. Changes in rat hippocampal CA1 synapses following imipramine treatment. Hippocampus 2008, 18:631-639.
30. Chen Y., Dube C.M., Rice C.J., Baram T.Z. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J Neurosci 2008, 28:2903-2911.
31. Chen F., Madsen T.M., Wegener G., Nyengaard J.R. Repeated electroconvulsive seizures increase the total number of synapses in adult male rat hippocampus. Eur Neuropsychopharmacol 2009, 19:329-338.
32. Chen F., Madsen T.M., Wegener G., Nyengaard J.R. Imipramine treatment increases the number of hippocampal synapses and neurons in a genetic animal model of depression. Hippocampus 2010, 20:1376-1384.
33. Chen J.L., Lin W.C., Cha J.W., So P.T., Kubota Y., Nedivi E. Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci 2011, 14:587-594.
34. Chepenik L.G., Fredericks C., Papademetris X., Spencer L., Lacadie C., Wang F., Pittman B., Duncan J.S., Staib L.H., Duman R.S., Gelernter J., Blumberg H.P. Effects of the brain-derived neurotrophic growth factor val66met variation on hippocampus morphology in bipolar disorder. Neuropsychopharmacology 2009, 34:944-951.
35. Chowdhury G.M., Behar K.L., Cho W., Thomas M.A., Rothman D.L., Sanacora G. (1)H-[(1)(3)C]-nuclear magnetic resonance spectroscopy measures of ketamine's effect on amino acid neurotransmitter metabolism. Biol Psychiatry 2012, 71:1022-1025.
36. Citri A., Malenka R.C. Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 2008, 33:18-41.
37. Coe C.L., Kramer M., Czeh B., Gould E., Reeves A.J., Kirschbaum C., Fuchs E. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 2003, 54:1025-1034.
38. Conrad C.D., McLaughlin K.J., Huynh T.N., El-Ashmawy M., Sparks M. Chronic stress and a cyclic regimen of estradiol administration separately facilitate spatial memory: relationship with hippocampal CA1 spine density and dendritic complexity. Behav Neurosci 2012, 126:142-156.
39. Cooke B.M., Woolley C.S. Gonadal hormone modulation of dendrites in the mammalian CNS. J Neurobiol 2005, 64:34-46.
40. Cotter D., Mackay D., Landau S., Kerwin R., Everall I. Reduced glial cell density and neuronal size in the anterior cingulate cortex in major depressive disorder. Arch Gen Psychiatry 2001, 58:545-553.
41. Cotter D., Mackay D., Chana G., Beasley C., Landau S., Everall I.P. Reduced neuronal size and glial cell density in area 9 of the dorsolateral prefrontal cortex in subjects with major depressive disorder. Cereb Cortex 2002, 12:386-394.
42. Dalgleish T., Williams J.M., Golden A.M., Perkins N., Barrett L.F., Barnard P.J., Yeung C.A., Murphy V., Elward R., Tchanturia K., Watkins E. Reduced specificity of autobiographical memory and depression: the role of executive control. J Exp Psychol Gen 2007, 136:23-42.
43. Dalla C., Edgecomb C., Whetstone A.S., Shors T.J. Females do not express learned helplessness like males do. Neuropsychopharmacology 2008, 33:1559-1569.
44. 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.
45. Diazgranados N., Ibrahim L., Brutsche N.E., Newberg A., Kronstein P., Khalife S., Kammerer W.A., Quezado Z., Luckenbaugh D.A., Salvadore G., Machado-Vieira R., Manji H.K., Zarate C.A. A randomized add-on trial of an N-methyl-d-aspartate antagonist in treatment-resistant bipolar depression. Arch Gen Psychiatry 2010, 67:793-802.
46. DiazGranados N., Ibrahim L.A., Brutsche N.E., Ameli R., Henter I.D., Luckenbaugh D.A., Machado-Vieira R., Zarate C.A. Rapid resolution of suicidal ideation after a single infusion of an N-methyl-d-aspartate antagonist in patients with treatment-resistant major depressive disorder. J Clin Psychiatry 2010, 71:1605-1611.
47. Donohue H.S., Gabbott P.L., Davies H.A., Rodriguez J.J., Cordero M.I., Sandi C., Medvedev N.I., Popov V.I., Colyer F.M., Peddie C.J., Stewart M.G. Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 2006, 140:597-606.
48. Drevets W.C. Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders. Curr Opin Neurobiol 2001, 11:240-249.
49. Drevets W.C. Neuroimaging abnormalities in the amygdala in mood disorders. Ann N Y Acad Sci 2003, 985:420-444.
50. Drevets W.C., Bogers W., Raichle M.E. Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur Neuropsychopharmacol 2002, 12:527-544.
51. Drevets W.C., Price J.L., Furey M.L. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 2008, 213:93-118.
52. Du J., Gray N.A., Falke C.A., Chen W., Yuan P., Szabo S.T., Einat H., Manji H.K. Modulation of synaptic plasticity by antimanic agents: the role of AMPA glutamate receptor subunit 1 synaptic expression. J Neurosci 2004, 24:6578-6589.
53. Duman R.S., Monteggia L.M. A neurotrophic model for stress-related mood disorders. Biol Psychiatry 2006, 59:1116-1127.
54. Duman R.S., Malberg J., Thome J. Neural plasticity to stress and antidepressant treatment. Biol Psychiatry 1999, 46:1181-1191.
55. Duman C.H., Schlesinger L., Kodama M., Russell D.S., Duman R.S. A role for MAP kinase signaling in behavioral models of depression and antidepressant treatment. Biol Psychiatry 2007, 61:661-670.
56. 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.
57. Dunkel Schetter C., Tanner L. Anxiety, depression and stress in pregnancy: implications for mothers, children, research, and practice. Curr Opin Psychiatry 2012, 25:141-148.
58. Duric V., Banasr M., Licznerski P., Schmidt H.D., Stockmeier C.A., Simen A.A., Newton S.S., Duman R.S. A negative regulator of MAP kinase causes depressive behavior. Nat Med 2010, 16:1328-1332.
59. Duvarci S., Pare D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 2007, 27:4482-4491.
60. Dwivedi Y., Rizavi H.S., Conley R.R., Roberts R.C., Tamminga C.A., Pandey G.N. Altered gene expression of brain-derived neurotrophic factor and receptor tyrosine kinase B in postmortem brain of suicide subjects. Arch Gen Psychiatry 2003, 60:804-815.
61. Dwivedi Y., Mondal A.C., Rizavi H.S., Faludi G., Palkovits M., Sarosi A., Conley R.R., Pandey G.N. Differential and brain region-specific regulation of Rap-1 and Epac in depressed suicide victims. Arch Gen Psychiatry 2006, 63:639-648.
62. Dwivedi Y., Rizavi H.S., Teppen T., Sasaki N., Chen H., Zhang H., Roberts R.C., Conley R.R., Pandey G.N. Aberrant extracellular signal-regulated kinase (ERK) 5 signaling in hippocampus of suicide subjects. Neuropsychopharmacology 2007, 32:2338-2350.
63. Dwyer J.M., Lepack A.E., Duman R.S. MTOR activation is required for the antidepressant effects of mGluR(2)/(3) blockade. Int J Neuropsychopharmacol 2012, 15:429-434.
64. Dwyer J.M., Lepack A.E., Duman R.S. mTOR activation is required for the antidepressant effects of mGluR2/3 blockade. Int J Neuropsychopharmacol 2011, 1-6.
65. Eriksson E., Sundblad C., Lisjo P., Modigh K., Andersch B. Serum levels of androgens are higher in women with premenstrual irritability and dysphoria than in controls. Psychoneuroendocrinology 1992, 17:195-204.
66. Freeman E.W., Sammel M.D., Lin H., Nelson D.B. Associations of hormones and menopausal status with depressed mood in women with no history of depression. Arch Gen Psychiatry 2006, 63:375-382.
67. Fremeau R.T., Kam K., Qureshi T., Johnson J., Copenhagen D.R., Storm-Mathisen J., Chaudhry F.A., Nicoll R.A., Edwards R.H. Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 2004, 304:1815-1819.
68. Frodl T., Meisenzahl E., Zetzsche T., Bottlender R., Born C., Groll C., Jager M., Leinsinger G., Hahn K., Moller H.J. Enlargement of the amygdala in patients with a first episode of major depression. Biol Psychiatry 2002, 51:708-714.
69. Frye C.A., Paris J.J., Osborne D.M., Campbell J.C., Kippin T.E. Prenatal stress alters progestogens to mediate susceptibility to sex-typical, stress-sensitive disorders, such as drug abuse: a review. Front Psychiatry 2011, 2:52.
70. Fu Z., Lee S.H., Simonetta A., Hansen J., Sheng M., Pak D.T. Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J Neurochem 2007, 100:118-131.
71. Fukazawa Y., Saitoh Y., Ozawa F., Ohta Y., Mizuno K., Inokuchi K. Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 2003, 38:447-460.
72. Fumagalli F., Bedogni F., Perez J., Racagni G., Riva M.A. Corticostriatal brain-derived neurotrophic factor dysregulation in adult rats following prenatal stress. Eur J Neurosci 2004, 20:1348-1354.
73. Gallassi R., Di Sarro R., Morreale A., Amore M. Memory impairment in patients with late-onset major depression: the effect of antidepressant therapy. J Affect Disord 2006, 91:243-250.
74. Garey L.J., Ong W.Y., Patel T.S., Kanani M., Davis A., Mortimer A.M., Barnes T.R., Hirsch S.R. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia. J Neurol Neurosurg Psychiatry 1998, 65:446-453.
75. Gatt J., Nemeroff C.B., Dobson-Stone C., Pauyl R.H., Bryant R.A., Schofield P.R., Gordon E., Kemp A.H., Williams L.M. Interactions between BDNF Val66Met polymorphism and early life stress predict brain and arousal pathways to syndromal depression and anxiety. Mol Psychiatry 2009, 14:681-695.
76. Gibbons A.S., Brooks L., Scarr E., Dean B. AMPA receptor expression is increased post-mortem samples of the anterior cingulate from subjects with major depressive disorder. J Affect Disord 2012, 136:1232-1237.
77. Gilabert-Juan J., Castillo-Gomez E., Perez-Rando M., Molto M.D., Nacher J. Chronic stress induces changes in the structure of interneurons and in the expression of molecules related to neuronal structural plasticity and inhibitory neurotransmission in the amygdala of adult mice. Exp Neurol 2011, 232:33-40.
78. Glantz L.A., Lewis D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch Gen Psychiatry 2000, 57:65-73.
79. Glantz L.A., Lewis D.A. Dendritic spine density in schizophrenia and depression. Arch Gen Psychiatry 2001, 58:203.
80. Gos T., Bock J., Poeggel G., Braun K. Stress-induced synaptic changes in the rat anterior cingulate cortex are dependent on endocrine developmental time windows. Synapse 2008, 62:229-232.
81. 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.
82. Grigoriadis S., Robinson G.E. Gender issues in depression. Ann Clin Psychiatry 2007, 19:247-255.
83. Groc L., Choquet D., Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci 2008, 11:868-870.
84. Grossman A.W., Aldridge G.M., Weiler I.J., Greenough W.T. Local protein synthesis and spine morphogenesis: fragile X syndrome and beyond. J Neurosci 2006, 26:7151-7155.
85. Gruss M., Appenroth D., Flubacher A., Enzensperger C., Bock J., Fleck C., Gille G., Braun K. 9-Methyl-beta-carboline-induced cognitive enhancement is associated with elevated hippocampal dopamine levels and dendritic and synaptic proliferation. J Neurochem 2012, 121:924-931.
86. Gue M., Bravard A., Meunier J., Veyrier R., Gaillet S., Recasens M., Maurice T. Sex differences in learning deficits induced by prenatal stress in juvenile rats. Behav Brain Res 2004, 150:149-157.
87. Hageman I., Nielsen M., Wortwein G., Diemer N.H., Jorgensen M.B. Electroconvulsive stimulations prevent stress-induced morphological changes in the hippocampus. Stress 2008, 11:282-289.
88. Hajek T., Kopecek M., Hoschl C. Reduced hippocampal volumes in healthy carriers of brain-derived neurotrophic factor Val66Met polymorphism: meta-analysis. World J Biol Psychiatry 2012, 13:178-187.
89. Hajszan T., MacLusky N.J., Leranth C. Short-term treatment with the antidepressant fluoxetine triggers pyramidal dendritic spine synapse formation in rat hippocampus. Eur J Neurosci 2005, 21:1299-1303.
90. Hajszan T., Dow A., Warner-Schmidt J.L., Szigeti-Buck K., Sallam N.L., Parducz A., Leranth C., Duman R.S. Remodeling of hippocampal spine synapses in the rat learned helplessness model of depression. Biol Psychiatry 2009, 65:392-400.
91. Hao J., Janssen W.G., Tang Y., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen increases the number of spinophilin-immunoreactive spines in the hippocampus of young and aged female rhesus monkeys. J Comp Neurol 2003, 465:540-550.
92. Hara Y., Rapp P.R., Morrison J.H. Neuronal and morphological bases of cognitive decline in aged rhesus monkeys. Age (Dordr) 2012, 34:1051-1073.
93. Harvey C.D., Svoboda K. Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 2007, 450:1195-1200.
94. Hashimoto R., Numakawa T., Ohnishi T., Kumamaru E., Yagasaki Y., Ishimoto T., Mori T., Nemoto K., Adachi N., Izumi A., Chiba S., Noguchi H., Suzuki T., Iwata N., Ozaki N., Taguchi T., Kamiya A., Kosuga A., Tatsumi M., Kamijima K., Weinberger D.R., Sawa A., Kunugi H. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling. Hum Mol Genet 2006, 15:3024-3033.
95. Hashimoto K., Sawa A., Iyo M. Increased levels of glutamate in brains from patients with mood disorders. Biol Psychiatry 2007, 62:1310-1316.
96. Hasler G., van der Veen J.W., Tumonis T., Meyers N., Shen J., Drevets W.C. Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch Gen Psychiatry 2007, 64:193-200.
97. Hastings R.S., Parsey R.V., Oquendo M.A., Arango V., Mann J.J. Volumetric analysis of the prefrontal cortex, amygdala, and hippocampus in major depression. Neuropsychopharmacology 2004, 29:952-959.
98. Hercher C., Turecki G., Mechawar N. Through the looking glass: examining neuroanatomical evidence for cellular alterations in major depression. J Psychiatr Res 2009, 43:947-961.
99. Hickie I., Naismith S., Ward P.B., Turner K., Scott E., Mitchell P., Wilhelm K., Parker G. Reduced hippocampal volumes and memory loss in patients with early- and late-onset depression. Br J Psychiatry 2005, 186:197-202.
100. Hoeffer C.A., Klann E. mTOR signaling: at the crossroads of plasticity, memory and disease. Trends Neurosci 2010, 33:67-75.
101. Holtmaat A., Svoboda K. Experience-dependent structural synaptic plasticity in the mammalian brain. Nat Rev Neurosci 2009, 10:647-658.
102. Holtmaat A.J., Trachtenberg J.T., Wilbrecht L., Shepherd G.M., Zhang X., Knott G.W., Svoboda K. Transient and persistent dendritic spines in the neocortex in vivo. Neuron 2005, 45:279-291.
103. Huizink A.C., Mulder E.J., Buitelaar J.K. Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol Bull 2004, 130:115-142.
104. Hutsler J.J., Zhang H. Increased dendritic spine densities on cortical projection neurons in autism spectrum disorders. Brain Res 2010, 1309:83-94.
105. Ishiwata H., Shiga T., Okado N. Selective serotonin reuptake inhibitor treatment of early postnatal mice reverses their prenatal stress-induced brain dysfunction. Neuroscience 2005, 133:893-901.
106. 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.
107. Johnson S.A., Wang J.F., Sun X., McEwen B.S., Chattarji S., Young L.T. Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala. Neuroscience 2009, 163:34-39.
108. Kao P.F., Davis D.A., Banigan M.G., Vanderburg C.R., Seshadri S., Delalle I. Modulators of cytoskeletal reorganization in CA1 hippocampal neurons show increased expression in patients at mid-stage Alzheimer's disease. PLoS One 2010, 5:e13337.
109. Kang HJ, Voleti B, Hajszan T, Rajkowska G, Stockmeier CA, Licznerski P, Lepack A, Majik MS, Jeong LS, Banasr M, Son H, Duman RS (2012) Decreased expression of synapse-related genes and loss of synapses in major depressive disorder. Nat Med.
110. Kasper S., McEwen B.S. Neurobiological and clinical effects of the antidepressant tianeptine. CNS Drugs 2008, 22:15-26.
111. Kaufmann W.E., Moser H.W. Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex 2000, 10:981-991.
112. Kerstjens J.M., de Winter A.F., Bocca-Tjeertes I.F., ten Vergert E.M., Reijneveld S.A., Bos A.F. Developmental delay in moderately preterm-born children at school entry. J Pediatr 2011, 159:92-98.
113. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
114. Kessler R.C., McGonagle K.A., Swartz M., Blazer D.G., Nelson C.B. Sex and depression in the national comorbidity survey. I: lifetime prevalence, chronicity and recurrence. J Affect Disord 1993, 29:85-96.
115. King C.R. A novel embryological theory of autism causation involving endogenous biochemicals capable of initiating cellular gene transcription: a possible link between twelve autism risk factors and the autism 'epidemic'. Med Hypotheses 2011, 76:653-660.
116. Koehl M., Lemaire V., Le Moal M., Abrous D.N. Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats. Eur J Neurosci 2009, 29:635-640.
117. Koike H., Iijima M., Chaki S. Involvement of the mammalian target of rapamycin signaling in the antidepressant-like effect of group II metabotropic glutamate receptor antagonists. Neuropharmacology 2011, 61:1419-1423.
118. Kravitz H.M., Janssen I., Lotrich F.E., Kado D.M., Bromberger J.T. Sex steroid hormone gene polymorphisms and depressive symptoms in women at midlife. Am J Med 2006, 119:S87-S93.
119. Krucker T., Siggins G.R., Halpain S. Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci U S A 2000, 97:6856-6861.
120. LaBar K.S., Cabeza R. Cognitive neuroscience of emotional memory. Nat Rev Neurosci 2006, 7:54-64.
121. Lange C., Irle E. Enlarged amygdala volume and reduced hippocampal volume in young women with major depression. Psychol Med 2004, 34:1059-1064.
122. Lechin F., Van der Dijs B., Benaim M. Stress versus depression. Prog Neuropsychopharmacol Biol Psychiatry 1996, 20:899-950.
123. Lee L.J. Neonatal fluoxetine exposure affects the neuronal structure in the somatosensory cortex and somatosensory-related behaviors in adolescent rats. Neurotox Res 2009, 15:212-223.
124. Lee L.J., Lo F.S., Erzurumlu R.S. NMDA receptor-dependent regulation of axonal and dendritic branching. J Neurosci 2005, 25:2304-2311.
125. Lemaire V., Koehl M., Le Moal M., Abrous D.N. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 2000, 97:11032-11037.
126. 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.
127. 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.
128. Liao C.C., Lee L.J. Neonatal fluoxetine exposure affects the action potential properties and dendritic development in cortical subplate neurons of rats. Toxicol Lett 2011, 207:314-321.
129. Liberzon I., Phan K.L. Brain-imaging studies of posttraumatic stress disorder. CNS Spectr 2003, 8:641-650.
130. Lin Y.C., Koleske A.J. Mechanisms of synapse and dendrite maintenance and their disruption in psychiatric and neurodegenerative disorders. Annu Rev Neurosci 2010, 33:349-378.
131. Liston C., Gan W.B. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci U S A 2011, 108:16074-16079.
132. 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.
133. Liu Z.H., Chuang D.M., Smith C.B. Lithium ameliorates phenotypic deficits in a mouse model of fragile X syndrome. Int J Neuropsychopharmacol 2011, 14:618-630.
134. Liu R.J., Lee F.S., Li X.Y., Bambico F., Duman R.S., Aghajanian G.K. Brain-derived neurotrophic factor Val66Met allele impairs basal and ketamine-stimulated synaptogenesis in prefrontal cortex. Biol Psychiatry 2012, 71:996-1005.
135. Lodygensky G.A., Vasung L., Sizonenko S.V., Huppi P.S. Neuroimaging of cortical development and brain connectivity in human newborns and animal models. J Anat 2010, 217:418-428.
136. Luine V.N., Wallace M.E., Frankfurt M. Age-related deficits in spatial memory and hippocampal spines in virgin, female Fischer 344 rats. Curr Gerontol Geriatr Res 2011, 2011:316-386.
137. Maciag D., Hughes J., O'Dwyer G., Pride Y., Stockmeier C.A., Sanacora G., Rajkowska G. Reduced density of calbindin immunoreactive GABAergic neurons in the occipital cortex in major depression: relevance to neuroimaging studies. Biol Psychiatry 2010, 67:465-470.
138. MacQueen G., Frodl T. The hippocampus in major depression: evidence for the convergence of the bench and bedside in psychiatric research?. Mol Psychiatry 2011, 16:252-264.
139. 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.
140. Magarinos A.M., Verdugo J.M., McEwen B.S. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci U S A 1997, 94:14002-14008.
141. Magarinos A.M., Li C.J., Gal Toth J., Bath K.G., Jing D., Lee F.S., McEwen B.S. Effect of brain-derived neurotrophic factor haploinsufficiency on stress-induced remodeling of hippocampal neurons. Hippocampus 2011, 21:253-264.
142. Maller J.J., Daskalakis Z.J., Fitzgerald P.B. Hippocampal volumetrics in depression: the importance of the posterior tail. Hippocampus 2007, 17:1023-1027.
143. Malykhin N.V., Carter R., Seres P., Coupland N.J. Structural changes in the hippocampus in major depressive disorder: contributions of disease and treatment. J Psychiatry Neurosci 2010, 35:337-343.
144. Marchetti C., Tafi E., Middei S., Rubinacci M.A., Restivo L., Ammassari-Teule M., Marie H. Synaptic adaptations of CA1 pyramidal neurons induced by a highly effective combinational antidepressant therapy. Biol Psychiatry 2010, 67:146-154.
145. Markham J.A., McKian K.P., Stroup T.S., Juraska J.M. Sexually dimorphic aging of dendritic morphology in CA1 of hippocampus. Hippocampus 2005, 15:97-103.
146. Martin K.P., Wellman C.L. NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb Cortex 2011, 21:2366-2373.
147. Martinez-Tellez R.I., Hernandez-Torres E., Gamboa C., Flores G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 2009, 63:794-804.
148. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 2001, 4:1086-1092.
149. Matsuzaki M., Honkura N., Ellis-Davies G.C., Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature 2004, 429:761-766.
150. Mayberg H.S., Liotti M., Brannan S.K., McGinnis S., Mahurin R.K., Jerabek P.A., Silva J.A., Tekell J.L., Martin C.C., Lancaster J.L., Fox P.T. Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 1999, 156:675-682.
151. McEwen B.S. Central effects of stress hormones in health and disease: understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 2008, 583:174-185.
152. McEwen B.S., Gianaros P.J. Stress- and allostasis-induced brain plasticity. Annu Rev Med 2011, 62:431-445.
153. McEwen B.S., Chattarji S., Diamond D.M., Jay T.M., Reagan L.P., Svenningsson P., Fuchs E. The neurobiological properties of tianeptine (Stablon): from monoamine hypothesis to glutamatergic modulation. Mol Psychiatry 2010, 15:237-249.
154. McKinnon M.C., Yucel K., Nazarov A., MacQueen G.M. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci 2009, 34:41-54.
155. McLaughlin K.J., Baran S.E., Conrad C.D. Chronic stress- and sex-specific neuromorphological and functional changes in limbic structures. Mol Neurobiol 2009, 40:166-182.
156. McLaughlin K.J., Wilson J.O., Harman J., Wright R.L., Wieczorek L., Gomez J., Korol D.L., Conrad C.D. Chronic 17beta-estradiol or cholesterol prevents stress-induced hippocampal CA3 dendritic retraction in ovariectomized female rats: possible correspondence between CA1 spine properties and spatial acquisition. Hippocampus 2010, 20:768-786.
157. Michelsen K.A., van den Hove D.L., Schmitz C., Segers O., Prickaerts J., Steinbusch H.W. Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex. BMC Neurosci 2007, 8:107.
158. Miguel-Hidalgo J.J., Waltzer R., Whittom A.A., Austin M.C., Rajkowska G., Stockmeier C.A. Glial and glutamatergic markers in depression, alcoholism, and their comorbidity. J Affect Disord 2010, 127:230-240.
159. Mill J., Kiss E., Baji I., Kapornai K., Daroczy G., Vetro A., Kennedy J., Kovacs M., Barr C. Association study of the estrogen receptor alpha gene (ESR1) and childhood-onset mood disorders. Am J Med Genet B Neuropsychiatr Genet 2008, 147B:1323-1326.
160. Minshew N.J., Williams D.L. The new neurobiology of autism: cortex, connectivity, and neuronal organization. Arch Neurol 2007, 64:945-950.
161. Moghaddam B., Adams B., Verma A., Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 1997, 17:2921-2927.
162. Morozov A., Muzzio I.A., Bourtchouladze R., Van-Strien N., Lapidus K., Yin D., Winder D.G., Adams J.P., Sweatt J.D., Kandel E.R. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 2003, 39:309-325.
163. Muhammad A., Kolb B. Maternal separation altered behavior and neuronal spine density without influencing amphetamine sensitization. Behav Brain Res 2011, 223:7-16.
164. Muhammad A., Kolb B. Mild prenatal stress-modulated behavior and neuronal spine density without affecting amphetamine sensitization. Dev Neurosci 2011, 33:85-98.
165. Murmu M.S., Salomon S., Biala Y., Weinstock M., Braun K., Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 2006, 24:1477-1487.
166. Murphy D.D., Segal M. Regulation of dendritic spine density in cultured rat hippocampal neurons by steroid hormones. J Neurosci 1996, 16:4059-4068.
167. Mychasiuk R., Gibb R., Kolb B. Prenatal bystander stress induces neuroanatomical changes in the prefrontal cortex and hippocampus of developing rat offspring. Brain Res 2011, 1412:55-62.
168. 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.
169. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13:1161-1169.
170. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., Monteggia L.M. Neurobiology of depression. Neuron 2002, 34:13-25.
171. Norrholm S.D., Ouimet C.C. Chronic fluoxetine administration to juvenile rats prevents age-associated dendritic spine proliferation in hippocampus. Brain Res 2000, 883:205-215.
172. Norrholm S.D., Ouimet C.C. Altered dendritic spine density in animal models of depression and in response to antidepressant treatment. Synapse 2001, 42:151-163.
173. Odagiri K., Abe H., Kawagoe C., Takeda R., Ikeda T., Matsuo H., Nonaka H., Ebihara K., Nishimori T., Ishizuka Y., Hashiguchi H., Ishida Y. Psychological prenatal stress reduced the number of BrdU immunopositive cells in the dorsal hippocampus without affecting the open field behavior of male and female rats at one month of age. Neurosci Lett 2008, 446:25-29.
174. Ongur D., Drevets W.C., Price J.L. Glial reduction in the subgenual prefrontal cortex in mood disorders. Proc Natl Acad Sci U S A 1998, 95:13290-13295.
175. Pascual R., Zamora-Leon S.P. Chronic. (-)-deprenyl administration attenuates dendritic developmental impairment induced by early social isolation in the rat. Dev Neurosci 2007, 29:261-267.
176. Patterson M., Yasuda R. Signalling pathways underlying structural plasticity of dendritic spines. Br J Pharmacol 2011, 163:1626-1638.
177. Patterson S.L., Abel T., Deuel T.A., Martin K.C., Rose J.C., Kandel E.R. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996, 16:1137-1145.
178. Pawlak R., Magarinos A.M., Melchor J., McEwen B., Strickland S. Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior. Nat Neurosci 2003, 6:168-174.
179. Phillips M.L., Ladouceur C.D., Drevets W.C. A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 2008, 13(829):833-857.
180. Pittenger C., Duman R.S. Stress, depression, and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology 2008, 33:88-109.
181. Pizzagalli D.A. Frontocingulate dysfunction in depression: toward biomarkers of treatment response. Neuropsychopharmacology 2011, 36:183-206.
182. Poeggel G., Helmeke C., Abraham A., Schwabe T., Friedrich P., Braun K. Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci U S A 2003, 100:16137-16142.
183. Popoli M., Yan Z., McEwen B.S., Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2011, 13:22-37.
184. 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.
185. Price J.L., Drevets W.C. Neural circuits underlying the pathophysiology of mood disorders. Trends Cogn Sci 2012, 16:61-71.
186. Qi H., Mailliet F., Spedding M., Rocher C., Zhang X., Delagrange P., McEwen B., Jay T.M., Svenningsson P. Antidepressants reverse the attenuation of the neurotrophic MEK/MAPK cascade in frontal cortex by elevated platform stress; reversal of effects on LTP is associated with GluA1 phosphorylation. Neuropharmacology 2009, 56:37-46.
187. Radley J.J., Rocher A.B., Miller M., Janssen W.G., Liston C., Hof P.R., McEwen B.S., Morrison J.H. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 2006, 16:313-320.
188. 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.
189. Rajkowska G., Miguel-Hidalgo J.J., Wei J., Dilley G., Pittman S.D., Meltzer H.Y., Overholser J.C., Roth B.L., Stockmeier C.A. Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression. Biol Psychiatry 1999, 45:1085-1098.
190. Rajkowska G., Miguel-Hidalgo J.J., Dubey P., Stockmeier C.A., Krishnan K.R. Prominent reduction in pyramidal neurons density in the orbitofrontal cortex of elderly depressed patients. Biol Psychiatry 2005, 58:297-306.
191. Rajkowska G., O'Dwyer G., Teleki Z., Stockmeier C.A., Miguel-Hidalgo J.J. GABAergic neurons immunoreactive for calcium binding proteins are reduced in the prefrontal cortex in major depression. Neuropsychopharmacology 2007, 32:471-482.
192. Rasgon N.L., Carter M.S., Elman S., Bauer M., Love M., Korenman S.G. Common treatment of polycystic ovarian syndrome and major depressive disorder: case report and review. Curr Drug Targets Immune Endocr Metabol Disord 2002, 2:97-102.
193. Rex C.S., Lin C.Y., Kramar E.A., Chen L.Y., Gall C.M., Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 2007, 27:3017-3029.
194. Rigucci S., Serafini G., Pompili M., Kotzalidis G.D., Tatarelli R. Anatomical and functional correlates in major depressive disorder: the contribution of neuroimaging studies. World J Biol Psychiatry 2010, 11:165-180.
195. Roberts R.C., Conley R., Kung L., Peretti F.J., Chute D.J. Reduced striatal spine size in schizophrenia: a postmortem ultrastructural study. Neuroreport 1996, 7:1214-1218.
196. Rosoklija G., Toomayan G., Ellis S.P., Keilp J., Mann J.J., Latov N., Hays A.P., Dwork A.J. Structural abnormalities of subicular dendrites in subjects with schizophrenia and mood disorders: preliminary findings. Arch Gen Psychiatry 2000, 57:349-356.
197. Ryan M.A., Jacobson I.G., Sevick C.J., Smith T.C., Gumbs G.R., Conlin A.M. Health outcomes among infants born to women deployed to United States military operations during pregnancy. Birth Defects Res A Clin Mol Teratol 2011, 91:117-124.
198. Salm A.K., Pavelko M., Krouse E.M., Webster W., Kraszpulski M., Birkle D.L. Lateral amygdaloid nucleus expansion in adult rats is associated with exposure to prenatal stress. Brain Res Dev Brain Res 2004, 148:159-167.
199. Salvadore G., Nugent A.C., Lemaitre H., Luckenbaugh D.A., Tinsley R., Cannon D.M., Neumeister A., Zarate C.A., Drevets W.C. Prefrontal cortical abnormalities in currently depressed versus currently remitted patients with major depressive disorder. Neuroimage 2011, 54:2643-2651.
200. Sanacora G., Gueorguieva R., Epperson C.N., Wu Y.T., Appel M., Rothman D.L., Krystal J.H., Mason G.F. Subtype-specific alterations of gamma-aminobutyric acid and glutamate in patients with major depression. Arch Gen Psychiatry 2004, 61:705-713.
201. Sapolsky R.M. Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. Arch Gen Psychiatry 2000, 57:925-935.
202. Savitz J., Nugent A.C., Bogers W., Liu A., Sills R., Luckenbaugh D.A., Bain E.E., Price J.L., Zarate C., Manji H.K., Cannon D.M., Marrett S., Charney D.S., Drevets W.C. Amygdala volume in depressed patients with bipolar disorder assessed using high resolution 3T MRI: the impact of medication. Neuroimage 2010, 49:2966-2976.
203. Scharfman H.E., MacLusky N.J. The influence of gonadal hormones on neuronal excitability, seizures, and epilepsy in the female. Epilepsia 2006, 47:1423-1440.
204. Schmitz C., Rhodes M.E., Bludau M., Kaplan S., Ong P., Ueffing I., Vehoff J., Korr H., Frye C.A. Depression: reduced number of granule cells in the hippocampus of female, but not male, rats due to prenatal restraint stress. Mol Psychiatry 2002, 7:810-813.
205. Segal M. Dendritic spines and long-term plasticity. Nat Rev Neurosci 2005, 6:277-284.
206. Segal M., Murphy D. Estradiol induces formation of dendritic spines in hippocampal neurons: functional correlates. Horm Behav 2001, 40:156-159.
207. Segal M., Kreher U., Greenberger V., Braun K. Is fragile X mental retardation protein involved in activity-induced plasticity of dendritic spines?. Brain Res 2003, 972:9-15.
208. Sen S., Duman R., Sanacora G. Serum brain-derived neurotrophic factor, depression, and antidepressant medications: meta-analyses and implications. Biol Psychiatry 2008, 64:527-532.
209. 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.
210. 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.
211. Sheline Y.I., Barch D.M., Donnelly J.M., Ollinger J.M., Snyder A.Z., Mintun M.A. Increased amygdala response to masked emotional faces in depressed subjects resolves with antidepressant treatment: an fMRI study. Biol Psychiatry 2001, 50:651-658.
212. Sheline Y.I., Gado M.H., Kraemer H.C. Untreated depression and hippocampal volume loss. Am J Psychiatry 2003, 160:1516-1518.
213. Siegle G.J., Steinhauer S.R., Thase M.E., Stenger V.A., Carter C.S. Can't shake that feeling: event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 2002, 51:693-707.
214. Silva-Gomez A.B., Rojas D., Juarez I., Flores G. Decreased dendritic spine density on prefrontal cortical and hippocampal pyramidal neurons in postweaning social isolation rats. Brain Res 2003, 983:128-136.
215. Sisk C.L., Zehr J.L. Pubertal hormones organize the adolescent brain and behavior. Front Neuroendocrinol 2005, 26:163-174.
216. Smit-Rigter L.A., Noorlander C.W., von Oerthel L., Chameau P., Smidt M.P., van Hooft J.A. Prenatal fluoxetine exposure induces life-long serotonin 5-HT(3) receptor-dependent cortical abnormalities and anxiety-like behaviour. Neuropharmacology 2012, 62:865-870.
217. Soetanto A., Wilson R.S., Talbot K., Un A., Schneider J.A., Sobiesk M., Kelly J., Leurgans S., Bennett D.A., Arnold S.E. Association of anxiety and depression with microtubule-associated protein 2- and synaptopodin-immunolabeled dendrite and spine densities in hippocampal CA3 of older humans. Arch Gen Psychiatry 2010, 67:448-457.
218. Stewart M.G., Davies H.A., Sandi C., Kraev I.V., Rogachevsky V.V., Peddie C.J., Rodriguez J.J., Cordero M.I., Donohue H.S., Gabbott P.L., Popov V.I. Stress suppresses and learning induces plasticity in CA3 of rat hippocampus: a three-dimensional ultrastructural study of thorny excrescences and their postsynaptic densities. Neuroscience 2005, 131:43-54.
219. Stockmeier C.A., Mahajan G.J., Konick L.C., Overholser J.C., Jurjus G.J., Meltzer H.Y., Uylings H.B., Friedman L., Rajkowska G. Cellular changes in the postmortem hippocampus in major depression. Biol Psychiatry 2004, 56:640-650.
220. Sunanda Rao.M.S., Raju T.R. Effect of chronic restraint stress on dendritic spines and excrescences of hippocampal CA3 pyramidal neurons-a quantitative study. Brain Res 1995, 694:312-317.
221. Talge N.M., Holzman C., Wang J., Lucia V., Gardiner J., Breslau N. Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age. Pediatrics 2010, 126:1124-1131.
222. Tanaka J., Horiike Y., Matsuzaki M., Miyazaki T., Ellis-Davies G.C., Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 2008, 319:1683-1687.
223. Tanapat P., Hastings N.B., Reeves A.J., Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 1999, 19:5792-5801.
224. Tang Y., Janssen W.G., Hao J., Roberts J.A., McKay H., Lasley B., Allen P.B., Greengard P., Rapp P.R., Kordower J.H., Hof P.R., Morrison J.H. Estrogen replacement increases spinophilin-immunoreactive spine number in the prefrontal cortex of female rhesus monkeys. Cereb Cortex 2004, 14:215-223.
225. Tham M.W., Woon P.S., Sum M.Y., Lee T.S., Sim K. White matter abnormalities in major depression: evidence from post-mortem, neuroimaging and genetic studies. J Affect Disord 2011, 132:26-36.
226. Thome J., Pesold B., Baader M., Hu M., Gewirtz J.C., Duman R.S., Henn F.A. Stress differentially regulates synaptophysin and synaptotagmin expression in hippocampus. Biol Psychiatry 2001, 50:809-812.
227. Tordera R.M., Totterdell S., Wojcik S.M., Brose N., Elizalde N., Lasheras B., Del Rio J. Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur J Neurosci 2007, 25:281-290.
228. Tsai S.-J., Hong C.-J., Liou Y.-J. Effects of BDNF polymorphisms on antidepressant action. Psychiatry Investig 2010, 7:236-242.
229. Turner R.J., Lloyd D.A. Stress burden and the lifetime incidence of psychiatric disorder in young adults: racial and ethnic contrasts. Arch Gen Psychiatry 2004, 61:481-488.
230. Vaidya V.A., Siuciak J.A., Du F., Duman R.S. Hippocampal mossy fiber sprouting induced by chronic electroconvulsive seizures. Neuroscience 1999, 89:157-166.
231. Vermetten E., Vythilingam M., Southwick S.M., Charney D.S., Bremner J.D. Long-term treatment with paroxetine increases verbal declarative memory and hippocampal volume in posttraumatic stress disorder. Biol Psychiatry 2003, 54:693-702.
232. Videbech P., Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry 2004, 161:1957-1966.
233. von Bohlen und Halbach O., Krause S., Medina D., Sciarretta C., Minichiello L., Minichiello L., Unsicker K. Regional- and age-dependent reduction in trkB receptor expression in the hippocampus is associated with altered spine morphologies. Biol Psychiatry 2006, 59:793-800.
234. von Bohlen und Halbach O., Zacher C., Gass P., Unsicker K. Age-related alterations in hippocampal spines and deficiencies in spatial memory in mice. J Neurosci Res 2006, 83:525-531.
235. 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.
236. Vyas A., Bernal S., Chattarji S. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 2003, 965:290-294.
237. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
238. Vyas A., Jadhav S., Chattarji S. Prolonged behavioral stress enhances synaptic connectivity in the basolateral amygdala. Neuroscience 2006, 143:387-393.
239. Vythilingam M., Vermetten E., Anderson G.M., Luckenbaugh D., Anderson E.R., Snow J., Staib L.H., Charney D.S., Bremner J.D. Hippocampal volume, memory, and cortisol status in major depressive disorder: effects of treatment. Biol Psychiatry 2004, 56:101-112.
240. Wang M., Yang Y., Dong Z., Cao J., Xu L. NR2B-containing N-methyl-d-aspartate subtype glutamate receptors regulate the acute stress effect on hippocampal long-term potentiation/long-term depression in vivo. Neuroreport 2006, 17:1343-1346.
241. Wang J.W., David D.J., Monckton J.E., Battaglia F., Hen R. Chronic fluoxetine stimulates maturation and synaptic plasticity of adult-born hippocampal granule cells. J Neurosci 2008, 28:1374-1384.
242. Warner-Schmidt J.L., Duman R.S. Hippocampal neurogenesis: opposing effects of stress and antidepressant treatment. Hippocampus 2006, 16:239-249.
243. Willner P. Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 2005, 52:90-110.
244. Woolley C.S., Gould E., McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990, 531:225-231.
245. Xie Z., Srivastava D.P., Photowala H., Kai L., Cahill M.E., Woolfrey K.M., Shum C.Y., Surmeier D.J., Penzes P. Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 2007, 56:640-656.
246. Xu F., Luk C., Richard M.P., Zaidi W., Farkas S., Getz A., Lee A., van Minnen J., Syed N.I. Antidepressant fluoxetine suppresses neuronal growth from both vertebrate and invertebrate neurons and perturbs synapse formation between Lymnaea neurons. Eur J Neurosci 2010, 31:994-1005.
247. Yuan P., Zhou R., Wang Y., Li X., Li J., Chen G., Guitart X., Manji H.K. Altered levels of extracellular signal-regulated kinase signaling proteins in postmortem frontal cortex of individuals with mood disorders and schizophrenia. J Affect Disord 2010, 124:164-169.
248. 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.
249. 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.
250. Zehle S., Bock J., Jezierski G., Gruss M., Braun K. Methylphenidate treatment recovers stress-induced elevated dendritic spine densities in the rodent dorsal anterior cingulate cortex. Dev Neurobiol 2007, 67:1891-1900.
251. Zhao C., Warner-Schmidt J., Duman R.S., Gage F.H. Electroconvulsive seizure promotes spine maturation in newborn dentate granule cells in adult rat. Dev Neurobiol 2012, 72:937-942.
252. Zheng J., Xu D.F., Li K., Wang H.T., Shen P.C., Lin M., Cao X.H., Wang R. Neonatal exposure to fluoxetine and fluvoxamine alteres spine density in mouse hippocampal CA1 pyramidal neurons. Int J Clin Exp Pathol 2011, 4:162-168.