Lithium's role in neural plasticity and its implications for mood disorders

Acta Psychiatrica Scandinavica

Volumn 128, Issue 5, 2013, Pages 347-361

  Gray, J D ^a   Mcewen, B S ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Amygdala; Bipolar disorder; Glutamate; Hippocampus; Lithium; Plasticity; Stress

Indexed keywords

GLUCOCORTICOID RECEPTOR; GLUTAMIC ACID; GLYCOGEN SYNTHASE KINASE 3; HYDROCORTISONE; LITHIUM; MINERALOCORTICOID RECEPTOR; N ACETYLASPARTIC ACID;

AMYGDALOID NUCLEUS; ARTICLE; BIPOLAR DISORDER; CELL PROLIFERATION; CHRONIC STRESS; DENTATE GYRUS; HIPPOCAMPUS; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IN VITRO STUDY; MOOD DISORDER; NERVE CELL PLASTICITY; NEUROIMAGING; NONHUMAN; PRIORITY JOURNAL;

AMYGDALA; BIPOLAR DISORDER; GLUTAMATE; HIPPOCAMPUS; LITHIUM; PLASTICITY; STRESS;

ANTIMANIC AGENTS; BRAIN; HUMANS; LITHIUM; MOOD DISORDERS; NEURONAL PLASTICITY; STRESS, PSYCHOLOGICAL;

EID: 84885335908     PISSN: 0001690X     EISSN: 16000447     Source Type: Journal    
DOI: 10.1111/acps.12139     Document Type: Article

References (168)

1. McEwen BS, Gianaros PJ. Stress- and allostasis-induced brain plasticity. Annu Rev Med 2011;62:431-445.
2. McEwen BS. 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.
3. McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999;22:105-122.
4. Karatsoreos IN, McEwen BS. Psychobiological allostasis: resistance, resilience and vulnerability. Trends Cogn Sci 2011;15:576-584.
5. Kessler RC. The effects of stressful life events on depression. Annu Rev Psychol 1997;48:191-214.
6. Miklowitz DJ. Functional impairment, stress, and psychosocial intervention in bipolar disorder. Curr Psychiatry Rep 2011;13:504-512.
7. Strakowski SM, Delbello MP, Adler CM. The functional neuroanatomy of bipolar disorder: a review of neuroimaging findings. Mol Psychiatry 2005;10:105-116.
8. Savitz J, Drevets WC. Bipolar and major depressive disorder: neuroimaging the developmental-degenerative divide. Neurosci Biobehav Rev 2009;33:699-771.
9. Wood GE, Young LT, Reagan LP, Chen B, McEwen BS. Stress-induced structural remodeling in hippocampus: prevention by lithium treatment. Proc Natl Acad Sci U S A 2004;101:3973-3978.
10. Johnson SA, Wang JF, Sun X, McEwen BS, Chattarji S, Young LT. Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala. Neuroscience 2009;163:34-39.
11. Funder JW. Glucocorticoid and mineralocorticoid receptors: biology and clinical relevance. Annu Rev Med 1997;48:231-240.
12. McEwen BS, Weiss JM, Schwartz LS. Selective retention of corticosterone by limbic structures in rat brain. Nature 1968;220:911-912.
13. Daban C, Vieta E, Mackin P, Young AH. Hypothalamic-pituitary-adrenal axis and bipolar disorder. Psychiatr Clin North Am 2005;28:469-480.
14. Pariante CM, Lightman SL. The HPA axis in major depression: classical theories and new developments. Trends Neurosci 2008;31:464-468.
15. Schmider J, Lammers CH, Gotthardt U, Dettling M, Holsboer F, Heuser IJ. Combined dexamethasone/corticotropin-releasing hormone test in acute and remitted manic patients, in acute depression, and in normal controls: I. Biol Psychiatry 1995;38:797-802.
16. Watson S, Gallagher P, Ritchie JC, Ferrier IN, Young AH. Hypothalamic-pituitary-adrenal axis function in patients with bipolar disorder. Br J Psychiatry 2004;184:496-502.
17. Sapolsky RM, Krey LC, McEwen BS. Prolonged glucocorticoid exposure reduces hippocampal neuron number: implications for aging. J Neurosci 1985;5:1222-1227.
18. Gould E, Cameron HA, Daniels DC, Woolley CS, McEwen BS. Adrenal hormones suppress cell division in the adult rat dentate gyrus. J Neurosci 1992;12:3642-3650.
19. Kim JB, Ju JY, Kim JH et al. Dexamethasone inhibits proliferation of adult hippocampal neurogenesis in vivo and in vitro. Brain Res 2004;1027:1-10.
20. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK. Enhancement of hippocampal neurogenesis by lithium. J Neurochem 2000;75:1729-1734.
21. Son H, Yu IT, Hwang SJ et al. Lithium enhances long-term potentiation independently of hippocampal neurogenesis in the rat dentate gyrus. J Neurochem 2003;85:872-881.
22. Kim JS, Chang MY, Yu IT et al. Lithium selectively increases neuronal differentiation of hippocampal neural progenitor cells both in vitro and in vivo. J Neurochem 2004;89:324-336.
23. Boku S, Nakagawa S, Masuda T et al. Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway. Neuropsychopharmacology 2009;34:805-815.
24. Burstein DE, Seeley PJ, Greene LA. Lithium ion inhibits nerve growth factor-induced neurite outgrowth and phosphorylation of nerve growth factor-modulated microtubule-associated proteins. J Cell Biol 1985;101:862-870.
25. Lucas FR, Goold RG, Gordon-Weeks PR, Salinas PC. Inhibition of GSK-3beta leading to the loss of phosphorylated MAP-1B is an early event in axonal remodelling induced by WNT-7a or lithium. J Cell Sci 1998;111:1351-1361.
26. Williams RS, Cheng L, Mudge AW, Harwood AJ. A common mechanism of action for three mood-stabilizing drugs. Nature 2002;417:292-295.
27. Cadotte DW, Xu B, Racine RJ et al. Chronic lithium treatment inhibits pilocarpine-induced mossy fiber sprouting in rat hippocampus. Neuropsychopharmacology 2003;28:1448-1453.
28. Mello LE, Cavalheiro EA, Tan AM et al. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 1993;34:985-995.
29. Dowlatshahi D, Macqueen G, Wang JF, Chen B, Young LT. Increased hippocampal supragranular Timm staining in subjects with bipolar disorder. NeuroReport 2000;11:3775-3778.
30. Magarinos AM, Verdugo JM, McEwen BS. Chronic stress alters synaptic terminal structure in hippocampus. Proc Natl Acad Sci U S A 1997;94:14002-14008.
31. Watase K, Gatchel JR, Sun Y et al. Lithium therapy improves neurological function and hippocampal dendritic arborization in a spinocerebellar ataxia type 1 mouse model. PLoS Med 2007;4:e182.
32. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002;22:6810-6818.
33. Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci U S A 2005;102:9371-9376.
34. Liu ZH, Chuang DM, Smith CB. Lithium ameliorates phenotypic deficits in a mouse model of fragile × syndrome. Int J Neuropsychopharmacol 2011;14:618-630.
35. Yazlovitskaya EM, Edwards E, Thotala D et al. Lithium treatment prevents neurocognitive deficit resulting from cranial irradiation. Cancer Res 2006;66:11179-11186.
36. Nocjar C, Hammonds MD, Shim SS. Chronic lithium treatment magnifies learning in rats. Neuroscience 2007;150:774-788.
37. Birch NJ. Letter: Lithium and magnesium-dependent enzymes. Lancet 1974;2:965-966.
38. Klein PS, Melton DA. A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci U S A 1996;93:8455-8459.
39. Stambolic V, Ruel L, Woodgett JR. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 1996;6:1664-1668.
40. Ryves WJ, Harwood AJ. Lithium inhibits glycogen synthase kinase-3 by competition for magnesium. Biochem Biophys Res Commun 2001;280:720-725.
41. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995;378:785-789.
42. Zhang F, Phiel CJ, Spece L, Gurvich N, Klein PS. Inhibitory phosphorylation of glycogen synthase kinase-3 (GSK-3) in response to lithium. Evidence for autoregulation of GSK-3. J Biol Chem 2003;278:33067-33077.
43. Chalecka-Franaszek E, Chuang DM. Lithium activates the serine/threonine kinase Akt-1 and suppresses glutamate-induced inhibition of Akt-1 activity in neurons. Proc Natl Acad Sci U S A 1999;96:8745-8750.
44. Jope RS, Johnson GV. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem Sci 2004;29:95-102.
45. Logan CY, Nusse R. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 2004;20:781-810.
46. Lie DC, Colamarino SA, Song HJ et al. Wnt signalling regulates adult hippocampal neurogenesis. Nature 2005;437:1370-1375.
47. Wexler EM, Geschwind DH, Palmer TD. Lithium regulates adult hippocampal progenitor development through canonical Wnt pathway activation. Mol Psychiatry 2008;13:285-292.
48. de Ferrari GV, Chacon MA, Barria MI et al. Activation of Wnt signaling rescues neurodegeneration and behavioral impairments induced by beta-amyloid fibrils. Mol Psychiatry 2003;8:195-208.
49. Boer U, Cierny I, Krause D et al. Chronic lithium salt treatment reduces CRE/CREB-directed gene transcription and reverses its upregulation by chronic psychosocial stress in transgenic reporter gene mice. Neuropsychopharmacology 2008;33:2407-2415.
50. Gould TD, Chen G, Manji HK. In vivo evidence in the brain for lithium inhibition of glycogen synthase kinase-3. Neuropsychopharmacology 2004;29:32-38.
51. Gould TD, Einat H, O'donnell KC, Picchini AM, Schloesser RJ, Manji HK. Beta-catenin overexpression in the mouse brain phenocopies lithium-sensitive behaviors. Neuropsychopharmacology 2007;32:2173-2183.
52. Beaulieu JM, Sotnikova TD, Yao WD et al. Lithium antagonizes dopamine-dependent behaviors mediated by an AKT/glycogen synthase kinase 3 signaling cascade. Proc Natl Acad Sci U S A 2004;101:5099-5104.
53. O'brien WT, Harper AD, Jove F et al. Glycogen synthase kinase-3beta haploinsufficiency mimics the behavioral and molecular effects of lithium. J Neurosci 2004;24:6791-6798.
54. Prickaerts J, Moechars D, Cryns K et al. Transgenic mice overexpressing glycogen synthase kinase 3beta: a putative model of hyperactivity and mania. J Neurosci 2006;26:9022-9029.
55. Benedetti F, Serretti A, Colombo C, Lorenzi C, Tubazio V, Smeraldi E. A glycogen synthase kinase 3-beta promoter gene single nucleotide polymorphism is associated with age at onset and response to total sleep deprivation in bipolar depression. Neurosci Lett 2004;368:123-126.
56. Benedetti F, Serretti A, Pontiggia A et al. Long-term response to lithium salts in bipolar illness is influenced by the glycogen synthase kinase 3-beta -50 T/C SNP. Neurosci Lett 2005;376:51-55.
57. Szczepankiewicz A, Rybakowski JK, Suwalska A et al. Association study of the glycogen synthase kinase-3beta gene polymorphism with prophylactic lithium response in bipolar patients. World J Biol Psychiatry 2006;7:158-161.
58. de Sarno P, Li X, Jope RS. Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 2002;43:1158-1164.
59. Downward J. PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 2004;15:177-182.
60. Chen G, Zeng WZ, Yuan PX et al. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 1999;72:879-882.
61. Chen RW, Chuang DM. Long term lithium treatment suppresses p53 and Bax expression but increases Bcl-2 expression. A prominent role in neuroprotection against excitotoxicity. J Biol Chem 1999;274:6039-6042.
62. Beaulieu JM, Marion S, Rodriguiz RM et al. A beta-arrestin 2 signaling complex mediates lithium action on behavior. Cell 2008;132:125-136.
63. Pan JQ, Lewis MC, Ketterman JK et al. AKT kinase activity is required for lithium to modulate mood-related behaviors in mice. Neuropsychopharmacology 2011;36:1397-1411.
64. Gould TD, O'Donnell KC, Picchini AM, Manji HK. Strain differences in lithium attenuation of d-amphetamine-induced hyperlocomotion: a mouse model for the genetics of clinical response to lithium. Neuropsychopharmacology 2007;32:1321-1333.
65. Hashimoto R, Takei N, Shimazu K, Christ L, Lu B, Chuang DM. Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: an essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology 2002;43:1173-1179.
66. Fukumoto T, Morinobu S, Okamoto Y, Kagaya A, Yamawaki S. Chronic lithium treatment increases the expression of brain-derived neurotrophic factor in the rat brain. Psychopharmacology 2001;158:100-106.
67. Einat H, Yuan P, Gould TD et al. The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J Neurosci 2003;23:7311-7316.
68. Rantamaki T, Knuuttila JE, Hokkanen ME, Castren E. The effects of acute and long-term lithium treatments on trkB neurotrophin receptor activation in the mouse hippocampus and anterior cingulate cortex. Neuropharmacology 2006;50:421-427.
69. Hammonds MD, Shim SS, Feng P, Calabrese JR. Effects of subchronic lithium treatment on levels of BDNF, Bcl-2 and phospho-CREB in the rat hippocampus. Basic Clin Pharmacol Toxicol 2007;100:356-359.
70. Hammonds MD, Shim SS. Effects of 4-week treatment with lithium and olanzapine on levels of brain-derived neurotrophic factor, B-cell CLL/lymphoma 2 and phosphorylated cyclic adenosine monophosphate response element-binding protein in the sub-regions of the hippocampus. Basic Clin Pharmacol Toxicol 2009;105:113-119.
71. Sklar P, Gabriel SB, McInnis MG et al. Family-based association study of 76 candidate genes in bipolar disorder: BDNF is a potential risk locus. Brain-derived neutrophic factor. Mol Psychiatry 2002;7:579-593.
72. Neves-Pereira M, Mundo E, Muglia P, King N, Macciardi F, Kennedy JL. The brain-derived neurotrophic factor gene confers susceptibility to bipolar disorder: evidence from a family-based association study. Am J Hum Genet 2002;71:651-655.
73. Brunoni AR, Lopes M, Fregni F. A systematic review and meta-analysis of clinical studies on major depression and BDNF levels: implications for the role of neuroplasticity in depression. Int J Neuropsychopharmacol 2008;11:1169-1180.
74. Dwivedi Y. Brain-derived neurotrophic factor: role in depression and suicide. Neuropsychiatr Dis Treat 2009;5:433-449.
75. Xiu MH, Hui L, Dang YF et al. Decreased serum BDNF levels in chronic institutionalized schizophrenia on long-term treatment with typical and atypical antipsychotics. Prog Neuropsychopharmacol Biol Psychiatry 2009;33:1508-1512.
76. Maina G, Rosso G, Zanardini R, Bogetto F, Gennarelli M, Bocchio-Chiavetto L. Serum levels of brain-derived neurotrophic factor in drug-naive obsessive-compulsive patients: a case-control study. J Affect Disord 2010;122:174-178.
77. de Sousa RT, van de Bilt MT, Diniz BS et al. Lithium increases plasma brain-derived neurotrophic factor in acute bipolar mania: a preliminary 4-week study. Neurosci Lett 2011;494:54-56.
78. Huang TL, Hung YY, Lee CT, Chen RF. Serum protein levels of brain-derived neurotrophic factor and tropomyosin-related kinase B in bipolar disorder: effects of mood stabilizers. Neuropsychobiology 2012;65:65-69.
79. Rybakowski JK, Suwalska A. Excellent lithium responders have normal cognitive functions and plasma BDNF levels. Int J Neuropsychopharmacol 2010;13:617-622.
80. Rybakowski JK. BDNF gene: functional Val66Met polymorphism in mood disorders and schizophrenia. Pharmacogenomics 2008;9:1589-1593.
81. Rybakowski JK, Suwalska A, Skibinska M et al. Prophylactic lithium response and polymorphism of the brain-derived neurotrophic factor gene. Pharmacopsychiatry 2005;38:166-170.
82. Dmitrzak-Weglarz M, Rybakowski JK, Suwalska A et al. Association studies of the BDNF and the NTRK2 gene polymorphisms with prophylactic lithium response in bipolar patients. Pharmacogenomics 2008;9:1595-1603.
83. Gray JD, Milner TA, McEwen BS. Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 2013;239:214-227.
84. Lu B, Pang PT, Woo NH. The yin and yang of neurotrophin action. Nat Rev Neurosci 2005;6:603-614.
85. Kabakov AY, Karkanias NB, Lenox RH, Papke RL. Synapse-specific accumulation of lithium in intracellular microdomains: a model for uncoupling coincidence detection in the brain. Synapse 1998;28:271-279.
86. Nonaka S, Hough CJ, Chuang DM. Chronic lithium treatment robustly protects neurons in the central nervous system against excitotoxicity by inhibiting N-methyl-D-aspartate receptor-mediated calcium influx. Proc Natl Acad Sci U S A 1998;95:2642-2647.
87. Riedel G, Platt B, Micheau J. Glutamate receptor function in learning and memory. Behav Brain Res 2003;140:1-47.
88. Sattler R, Tymianski M. Molecular mechanisms of glutamate receptor-mediated excitotoxic neuronal cell death. Mol Neurobiol 2001;24:107-129.
89. Sanacora G, Treccani G, Popoli M. Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders. Neuropharmacology 2012;62:63-77.
90. Zarate C Jr, Machado-Vieira R, Henter I, Ibrahim L, Diazgranados N, Salvadore G. Glutamatergic modulators: the future of treating mood disorders? Harv Rev Psychiatry 2010;18:293-303.
91. Dixon JF, Los GV, Hokin LE. Lithium stimulates glutamate "release" and inositol 1, 4, 5-trisphosphate accumulation via activation of the N-methyl-D-aspartate receptor in monkey and mouse cerebral cortex slices. Proc Natl Acad Sci U S A 1994;91:8358-8362.
92. Dixon JF, Hokin LE. The antibipolar drug valproate mimics lithium in stimulating glutamate release and inositol 1, 4, 5-trisphosphate accumulation in brain cortex slices but not accumulation of inositol monophosphates and bisphosphates. Proc Natl Acad Sci U S A 1997;94:4757-4760.
93. Dixon JF, Hokin LE. Lithium acutely inhibits and chronically up-regulates and stabilizes glutamate uptake by presynaptic nerve endings in mouse cerebral cortex. Proc Natl Acad Sci U S A 1998;95:8363-8368.
94. Albensi BC. The NMDA receptor/ion channel complex: a drug target for modulating synaptic plasticity and excitotoxicity. Curr Pharm Des 2007;13:3185-3194.
95. Hashimoto R, Hough C, Nakazawa T, Yamamoto T, Chuang DM. Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J Neurochem 2002;80:589-597.
96. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME. Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science 2002;295:491-495.
97. Hashimoto R, Fujimaki K, Jeong MR, Christ L, Chuang DM. Lithium-induced inhibition of Src tyrosine kinase in rat cerebral cortical neurons: a role in neuroprotection against N-methyl-D-aspartate receptor-mediated excitotoxicity. FEBS Lett 2003;538:145-148.
98. Christopherson KS, Hillier BJ, Lim WA, Bredt DS. PSD-95 assembles a ternary complex with the N-methyl-D-aspartic acid receptor and a bivalent neuronal NO synthase PDZ domain. J Biol Chem 1999;274:27467-27473.
99. Sattler R, Xiong Z, Lu WY, Hafner M, MacDonald JF, Tymianski M. Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 1999;284:1845-1848.
100. Ghasemi M, Sadeghipour H, Mosleh A, Sadeghipour HR, Mani AR, Dehpour AR. Nitric oxide involvement in the antidepressant-like effects of acute lithium administration in the mouse forced swimming test. Eur Neuropsychopharmacol 2008;18:323-332.
101. Ghasemi M, Raza M, Dehpour AR. NMDA receptor antagonists augment antidepressant-like effects of lithium in the mouse forced swimming test. J Psychopharmacol 2010;24:585-594.
102. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002;25:103-126.
103. Du J, Gray NA, Falke C, Yuan P, Szabo S, Manji HK. Structurally dissimilar antimanic agents modulate synaptic plasticity by regulating AMPA glutamate receptor subunit GluR1 synaptic expression. Ann N Y Acad Sci 2003;1003:378-380.
104. Du J, Creson TK, Wu LJ et al. The role of hippocampal GluR1 and GluR2 receptors in manic-like behavior. J Neurosci 2008;28:68-79.
105. Gould TD, O'Donnell KC, Dow ER, Du J, Chen G, Manji HK. Involvement of AMPA receptors in the antidepressant-like effects of lithium in the mouse tail suspension test and forced swim test. Neuropharmacology 2008;54:577-587.
106. Beneyto M, Meador-Woodruff JH. Lamina-specific abnormalities of NMDA receptor-associated postsynaptic protein transcripts in the prefrontal cortex in schizophrenia and bipolar disorder. Neuropsychopharmacology 2008;33:2175-2186.
107. Iwamoto K, Kakiuchi C, Bundo M, Ikeda K, Kato T. Molecular characterization of bipolar disorder by comparing gene expression profiles of postmortem brains of major mental disorders. Mol Psychiatry 2004;9:406-416.
108. Mozhui K, Karlsson RM, Kash TL et al. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 2010;30:5357-5367.
109. Belzung C, Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 2001;125:141-149.
110. Millstein RA, Ralph RJ, Yang RJ, Holmes A. Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes Brain Behav 2006;5:346-354.
111. Pothion S, Bizot JC, Trovero F, Belzung C. Strain differences in sucrose preference and in the consequences of unpredictable chronic mild stress. Behav Brain Res 2004;155:135-146.
112. Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 2012;13:22-37.
113. Joels M, de Kloet ER. Control of neuronal excitability by corticosteroid hormones. Trends Neurosci 1992;15:25-30.
114. de Kloet ER, Oitzl MS, Joels M. Stress and cognition: are corticosteroids good or bad guys? Trends Neurosci 1999;22:422-426.
115. 2+ elevation in cultured rat hippocampal neurons. J Neurochem 2002;83:1441-1451.
116. 2+ elevation in mouse hippocampal slices. Biochem Biophys Res Commun 2004;321:510-513.
117. Prager EM, Johnson LR. Stress at the synapse: signal transduction mechanisms of adrenal steroids at neuronal membranes. Sci Signal 2009;2:re5.
118. Liu L, Wang C, Ni X, Sun J. A rapid inhibition of NMDA receptor current by corticosterone in cultured hippocampal neurons. Neurosci Lett 2007;420:245-250.
119. Karst H, Joels M. Corticosterone slowly enhances miniature excitatory postsynaptic current amplitude in mice CA1 hippocampal cells. J Neurophysiol 2005;94:3479-3486.
120. Olijslagers JE, de Kloet ER, Elgersma Y, van Woerden GM, Joels M, Karst H. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur J Neurosci 2008;27:2542-2550.
121. Karst H, Nair S, Velzing E et al. Glucocorticoids alter calcium conductances and calcium channel subunit expression in basolateral amygdala neurons. Eur J Neurosci 2002;16:1083-1089.
122. Duvarci S, Pare D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J Neurosci 2007;27:4482-4491.
123. Kavushansky A, Richter-Levin G. Effects of stress and corticosterone on activity and plasticity in the amygdala. J Neurosci Res 2006;84:1580-1587.
124. Goold RG, Owen R, Gordon-Weeks PR. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J Cell Sci 1999;112(Pt 19):3373-3384.
125. Berridge MJ, Irvine RF. Inositol phosphates and cell signalling. Nature 1989;341:197-205.
126. Berridge MJ. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta 2009;1793:933-940.
127. Shimshoni JA, Dalton EC, Watson P, Boris Y, Bialer M, Harwood AJ. Evaluation of the effects of propylisopropylacetic acid (PIA) on neuronal growth cone morphology. Neuropharmacology 2009;56:831-837.
128. Liston C, Gan WB. Glucocorticoids are critical regulators of dendritic spine development and plasticity in vivo. Proc Natl Acad Sci U S A 2011;108:16074-16079.
129. Harrell JM, Murphy PJ, Morishima Y et al. Evidence for glucocorticoid receptor transport on microtubules by dynein. J Biol Chem 2004;279:54647-54654.
130. Morsink MC, Steenbergen PJ, Vos JB et al. Acute activation of hippocampal glucocorticoid receptors results in different waves of gene expression throughout time. J Neuroendocrinol 2006;18:239-252.
131. Sklar P, Smoller JW, Fan J et al. Whole-genome association study of bipolar disorder. Mol Psychiatry 2008;13:558-569.
132. Ferreira MA, O'Donovan MC, Meng YA et al. Collaborative genome-wide association analysis supports a role for ANK3 and CACNA1C in bipolar disorder. Nat Genet 2008;40:1056-1058.
133. Takata A, Kim SH, Ozaki N et al. Association of ANK3 with bipolar disorder confirmed in East Asia. Am J Med Genet B Neuropsychiatr Genet 2011;156B:312-315.
134. Rudolf R, Bittins CM, Gerdes HH. The role of myosin V in exocytosis and synaptic plasticity. J Neurochem 2011;116:177-191.
135. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V. AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 1998;143:1295-1304.
136. Brachet A, Leterrier C, Irondelle M et al. Ankyrin G restricts ion channel diffusion at the axonal initial segment before the establishment of the diffusion barrier. J Cell Biol 2010;191:383-395.
137. Sobotzik JM, Sie JM, Politi C et al. AnkyrinG is required to maintain axo-dendritic polarity in vivo. Proc Natl Acad Sci U S A 2009;106:17564-17569.
138. Hedstrom KL, Ogawa Y, Rasband MN. AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 2008;183:635-640.
139. Ruberto G, Vassos E, Lewis CM et al. The cognitive impact of the ANK3 risk variant for bipolar disorder: initial evidence of selectivity to signal detection during sustained attention. PLoS ONE 2011;6:e16671.
140. McQuillin A, Rizig M, Gurling HM. A microarray gene expression study of the molecular pharmacology of lithium carbonate on mouse brain mRNA to understand the neurobiology of mood stabilization and treatment of bipolar affective disorder. Pharmacogenet Genomics 2007;17:605-617.
141. Leussis MP, Berry-Scott EM, Saito M et al. The ANK3 bipolar disorder gene regulates psychiatric-related behaviors that are modulated by lithium and stress. Biol Psychiatry 2013;73:683-690.
142. Moore GJ, Bebchuk JM, Wilds IB, Chen G, Manji HK. Lithium-induced increase in human brain grey matter. Lancet 2000;356:1241-1242.
143. Moore GJ, Bebchuk JM, Hasanat K et al. Lithium increases N-acetyl-aspartate in the human brain: in vivo evidence in support of bcl-2's neurotrophic effects? Biol Psychiatry 2000;48:1-8.
144. Brambilla P, Stanley JA, Sassi RB et al. 1H MRS study of dorsolateral prefrontal cortex in healthy individuals before and after lithium administration. Neuropsychopharmacology 2004;29:1918-1924.
145. Friedman SD, Dager SR, Parow A et al. Lithium and valproic acid treatment effects on brain chemistry in bipolar disorder. Biol Psychiatry 2004;56:340-348.
146. Hajek T, Bauer M, Pfennig A et al. Large positive effect of lithium on prefrontal cortex N-acetylaspartate in patients with bipolar disorder: 2-centre study. J Psychiatry Neurosci 2012;37:185-192.
147. Bowley MP, Drevets WC, Ongur D, Price JL. Low glial numbers in the amygdala in major depressive disorder. Biol Psychiatry 2002;52:404-412.
148. Young LT, Bezchlibnyk YB, Chen B, Wang JF, MacQueen GM. Amygdala cyclic adenosine monophosphate response element binding protein phosphorylation in patients with mood disorders: effects of diagnosis, suicide, and drug treatment. Biol Psychiatry 2004;55:570-577.
149. Bearden CE, Thompson PM, Dalwani M et al. Greater cortical gray matter density in lithium-treated patients with bipolar disorder. Biol Psychiatry 2007;62:7-16.
150. Yucel K, McKinnon MC, Taylor VH et al. Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology 2007;195:357-367.
151. Yucel K, Taylor VH, McKinnon MC et al. Bilateral hippocampal volume increase in patients with bipolar disorder and short-term lithium treatment. Neuropsychopharmacology 2008;33:361-367.
152. Lyoo IK, Dager SR, Kim JE et al. Lithium-induced gray matter volume increase as a neural correlate of treatment response in bipolar disorder: a longitudinal brain imaging study. Neuropsychopharmacology 2010;35:1743-1750.
153. Germana C, Kempton MJ, Sarnicola A et al. The effects of lithium and anticonvulsants on brain structure in bipolar disorder. Acta Psychiatr Scand 2010;122:481-487.
154. Hajek T, Kopecek M, Hoschl C, Alda M. Smaller hippocampal volumes in patients with bipolar disorder are masked by exposure to lithium: a meta-analysis. J Psychiatry Neurosci 2012;37:110143.
155. Altshuler LL, Bartzokis G, Grieder T, Curran J, Mintz J. Amygdala enlargement in bipolar disorder and hippocampal reduction in schizophrenia: an MRI study demonstrating neuroanatomic specificity. Arch Gen Psychiatry 1998;55:663-664.
156. Strakowski SM, DelBello MP, Sax KW et al. Brain magnetic resonance imaging of structural abnormalities in bipolar disorder. Arch Gen Psychiatry 1999;56:254-260.
157. Rosso IM, Killgore WD, Cintron CM, Gruber SA, Tohen M, Yurgelun-Todd DA. Reduced amygdala volumes in first-episode bipolar disorder and correlation with cerebral white matter. Biol Psychiatry 2007;61:743-749.
158. Blumberg HP, Kaufman J, Martin A et al. Amygdala and hippocampal volumes in adolescents and adults with bipolar disorder. Arch Gen Psychiatry 2003;60:1201-1208.
159. Hallahan B, Newell J, Soares JC et al. Structural magnetic resonance imaging in bipolar disorder: an international collaborative mega-analysis of individual adult patient data. Biol Psychiatry 2011;69:326-335.
160. Adler CM, Holland SK, Schmithorst V et al. Abnormal frontal white matter tracts in bipolar disorder: a diffusion tensor imaging study. Bipolar Disord 2004;6:197-203.
161. Wang F, Kalmar JH, Edmiston E et al. Abnormal corpus callosum integrity in bipolar disorder: a diffusion tensor imaging study. Biol Psychiatry 2008;64:730-733.
162. Wang F, Jackowski M, Kalmar JH et al. Abnormal anterior cingulum integrity in bipolar disorder determined through diffusion tensor imaging. Br J Psychiatry 2008;193:126-129.
163. Chaddock CA, Barker GJ, Marshall N et al. White matter microstructural impairments and genetic liability to familial bipolar I disorder. Br J Psychiatry 2009;194:527-534.
164. Benedetti F, Absinta M, Rocca MA et al. Tract-specific white matter structural disruption in patients with bipolar disorder. Bipolar Disord 2011;13:414-424.
165. Monkul ES, Matsuo K, Nicoletti MA et al. Prefrontal gray matter increases in healthy individuals after lithium treatment: a voxel-based morphometry study. Neurosci Lett 2007;429:7-11.
166. Bavelier D, Levi DM, Li RW, Dan Y, Hensch TK. Removing brakes on adult brain plasticity: from molecular to behavioral interventions. J Neurosci 2010;30:14964-14971.
167. Castren E, Rantamaki T. The role of BDNF and its receptors in depression and antidepressant drug action: reactivation of developmental plasticity. Dev Neurobiol 2010;70:289-297.
168. Bauer M, Adli M, Bschor T et al. Lithium's emerging role in the treatment of refractory major depressive episodes: augmentation of antidepressants. Neuropsychobiology 2010;62:36-42.