Synergistic and additive effects of enriched environment and lithium on the generation of new cells in adult mouse hippocampus

Journal of Neural Transmission

Volumn 121, Issue 7, 2014, Pages 695-706

  Schaeffer, Evelin L ^a   Cerulli, Fabiana G ^a   Souza, Hélio O X ^a   Catanozi, Sergio ^a   Gattaz, Wagner F ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Adult neurogenesis; Enriched environment; Hippocampus; Interaction effect; Lithium

Indexed keywords

BROXURIDINE; LITHIUM CARBONATE; LITHIUM CHLORIDE; TRANQUILIZER;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; DRUG POTENTIATION; ENVIRONMENTAL ENRICHMENT; GRANULE CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PILOT STUDY; PRIORITY JOURNAL; STEREOMETRY; WEIGHT GAIN; ANIMAL; C57BL MOUSE; CELL COUNT; DOSE RESPONSE; DRUG EFFECTS; ENVIRONMENT; HIPPOCAMPUS; METABOLISM; NONPARAMETRIC TEST; PHYSIOLOGY;

ANIMALS; ANTIMANIC AGENTS; BROMODEOXYURIDINE; CELL COUNT; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENT; HIPPOCAMPUS; LITHIUM CHLORIDE; MALE; MICE; MICE, INBRED C57BL; NEUROGENESIS; STATISTICS, NONPARAMETRIC;

EID: 84903307487     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-014-1175-5     Document Type: Article

References (86)

1. Altar CA, Jurata LW, Charles V, Lemire A, Liu P, Bukhman Y, Young TA, Bullard J, Yokoe H, Webster MJ, Knable MB, Brockman JA (2005) Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry 58:85-96 (Pubitemid 41008124)
2. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381 (Pubitemid 20368500)
3. Altshuler LL, Bartzokis G, Grieder T, Curran J, Jimenez T, Leight K, Wilkins J, Gerner R, Mintz J (2000) An MRI study of temporal lobe structures in men with bipolar disorder or schizophrenia. Biol Psychiatry 48:147-162 (Pubitemid 30618804)
4. Arnone D, McIntosh AM, Ebmeier KP, Munafò MR, Anderson IM (2012) Magnetic resonance imaging studies in unipolar depression: systematic review and meta-regression analyses. Eur Neuropsychopharmacol 22:1-16
5. Babu H, Ramirez-Rodriguez G, Fabel K, Bischofberger J, Kempermann G (2009) Synaptic network activity induces neuronal differentiation of adult hippocampal precursor cells through BDNF signaling. Front Neurosci 3:49
6. Bayod S, Menella I, Sanchez-Roige S, Lalanza JF, Escorihuela RM, Camins A, Pallàs M, Canudas AM (2014) Wnt pathway regulation by long-term moderate exercise in rat hippocampus. Brain Res 1543:38-48
7. Bechara RG, Kelly ÀM (2013) Exercise improves object recognition memory and induces BDNF expression and cell proliferation in cognitively enriched rats. Behav Brain Res 245:96-100
8. Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159-168 (Pubitemid 38887743)
9. Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J, Arango V (2009) Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34:2376-2389
10. Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ, Mann JJ, Arango V (2012) Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol Psychiatry 72:562-571
11. Brambilla P, Harenski K, Nicoletti M, Sassi RB, Mallinger AG, Frank E, Kupfer DJ, Keshavan MS, Soares JC (2003) MRI investigation of temporal lobe structures in bipolar patients. J Psychiatr Res 37:287-295 (Pubitemid 36579409)
12. Cavalcanti AN, Marchi GM, Ambrosano GM (2010) Statistical results on restorative dentistry experiments: effect of the interaction between main variables. J Appl Oral Sci 18:255-258
13. Chan JP, Cordeira J, Calderon GA, Iyer LK, RiosM(2008) Depletion of central BDNF in mice impedes terminal differentiation of new granule neurons in the adult hippocampus. Mol Cell Neurosci 39:372-383
14. Chen G, Rajkowska G, Du F, Seraji-Bozorgzad N, Manji HK (2000) Enhancement of hippocampal neurogenesis by lithium. J Neurochem 75:1729-1734
15. Chen BK, Sassi R, Axelson D, Hatch JP, Sanches M, Nicoletti M, Brambilla P, Keshavan MS, Ryan ND, Birmaher B, Soares JC (2004) Cross-sectional study of abnormal amygdala development in adolescents and young adults with bipolar disorder. Biol Psychiatry 56:399-405 (Pubitemid 39195319)
16. Chen Q, Nakajima A, Choi SH, Xiong X, Sisodia SS, Tang YP (2008) Adult neurogenesis is functionally associated with AD-like neurodegeneration. Neurobiol Dis 29:316-326
17. Chow N, Aarsland D, Honarpisheh H, Beyer MK, Somme JH, Elashoff D, Rongve A, Tysnes OB, Thompson PM, Apostolova LG (2012) Comparing hippocampal atrophy in Alzheimer's dementia and dementia with lewy bodies. Dement Geriatr Cogn Disord 34:44-50
18. Delaloye C, de Bilbao F, Moy G, Baudois S, Weber K, Campos L, Canuto A, Giardini U, von Gunten A, Stancu RI, Scheltens P, Lazeyras F, Millet P, Giannakopoulos P, Gold G (2009) Neuroanatomical and neuropsychological features of euthymic patients with bipolar disorder. Am J Geriatr Psychiatry 17:1012-1021
19. Eack SM, Hogarty GE, Cho RY, Prasad KM, Greenwald DP, Hogarty SS, Keshavan MS (2010) Neuroprotective effects of cognitive enhancement therapy against gray matter loss in early schizophrenia: results from a 2-year randomized controlled trial. Arch Gen Psychiatry 67:674-682
20. Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243-250 (Pubitemid 350265488)
21. Epp JR, Beasley CL, Galea LA (2013) Increased hippocampal neurogenesis and p21 expression in depression: dependent on antidepressants, sex, age, and antipsychotic exposure. Neuropsychopharmacology 38:2297-2306
22. Fabel K, Wolf SA, Ehninger D, Babu H, Leal-Galicia P, Kempermann G (2009) Additive effects of physical exercise and environmental enrichment on adult hippocampal neurogenesis in mice. Front Neurosci 3:50
23. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19
24. Fiorentini A, Rosi MC, Grossi C, Luccarini I, Casamenti F (2010) Lithium improves hippocampal neurogenesis, neuropathology and cognitive functions in APP mutant mice. PLoS One 5:e14382
25. Forlenza OV, Diniz BS, Radanovic M, Santos FS, Talib LL, Gattaz WF (2011) Disease-modifying properties of long-term lithium treatment for amnestic mild cognitive impairment: randomised controlled trial. Br J Psychiatry 198:351-356
26. Forlenza OV, de Paula VJ, Machado-Vieira R, Diniz BS, Gattaz WF (2012) Does lithium prevent Alzheimer's disease? Drugs Aging 29:335-342
27. Franklin KBJ, Paxinos G (2007) The mouse brain in stereotaxic coordinates, 3rd edn. Elsevier, Amsterdam
28. Gratzner HG (1982) Monoclonal antibody to 5-bromo- and 5-iododeoxyuridine: a new reagent for detection of DNA replication. Science 218:474-475
29. Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147(Pt 3):229-263
30. Hajek T, Kopecek M, Höschl C, Alda M (2012) Smaller hippocampal volumes in patients with bipolar disorder are masked by exposure to lithium: a meta-analysis. J Psychiatry Neurosci 37:333-343
31. Hammonds MD, Shim SS (2009) 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 105:113-119
32. Hanson ND, Nemeroff CB, Owens MJ (2011) Lithium, but not fluoxetine or the corticotropin-releasing factor receptor 1 receptor antagonist R121919, increases cell proliferation in the adult dentate gyrus. J Pharmacol Exp Ther 337:180-186
33. Haukvik UK, Hartberg CB, Agartz I (2013) Schizophrenia - what does structural MRI show? Tidsskr Nor Laegeforen 133:850-853
34. Herring A, Ambrée O, Tomm M, Habermann H, Sachser N, Paulus W, Keyvani K (2009) Environmental enrichment enhances cellular plasticity in transgenic mice with Alzheimer-like pathology. Exp Neurol 216:184-192
35. Hu YS, Xu P, Pigino G, Brady ST, Larson J, Lazarov O (2010) Complex environment experience rescues impaired neurogenesis, enhances synaptic plasticity, and attenuates neuropathology in familial Alzheimer's disease-linked APPswe/PS1DeltaE9 mice. FASEB J 24:1667-1681
36. Hu YS, Long N, Pigino G, Brady ST, Lazarov O (2013) Molecular mechanisms of environmental enrichment: impairments in Akt/ GSK3b, neurotrophin-3 and CREB signaling. PLoS One 8:e64460
37. Jha S, Dong B, Sakata K (2011) Enriched environment treatment reverses depression-like behavior and restores reduced hippocampal neurogenesis and protein levels of brain-derived neurotrophic factor in mice lacking its expression through promoter IV. Transl Psychiatry 1:e40
38. Jin K, Galvan V, Xie L, Mao XO, Gorostiza OF, Bredesen DE, Greenberg DA (2004a) Enhanced neurogenesis in Alzheimer's disease transgenic (PDGF-APPSw, Ind) mice. Proc Natl Acad Sci USA 101:13363-13367 (Pubitemid 39209671)
39. Jin K, Peel AL, Mao XO, Xie L, Cottrell BA, Henshall DC, Greenberg DA (2004b) Increased hippocampal neurogenesis in Alzheimer's disease. Proc Natl Acad Sci USA 101:343-347 (Pubitemid 38084252)
40. Johnson M, Ekonomou A, Hobbs C, Ballard CG, Perry RH, Perry EK (2011) Neurogenic marker abnormalities in the hippocampus in dementia with Lewy bodies. Hippocampus 21:1126-1136
41. Keilhoff G, Bernstein HG, Becker A, Grecksch G, Wolf G (2004) Increased neurogenesis in a rat ketamine model of schizophrenia. Biol Psychiatry 56:317-322 (Pubitemid 39164516)
42. Kempermann G, Kuhn HG, Gage FH (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386:493-495 (Pubitemid 27164074)
43. Kempermann G, Brandon EP, Gage FH (1998) Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol 8:939-942 (Pubitemid 28371762)
44. Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A, Wolf SA (2010) Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci 4:189
45. Kobilo T, Liu QR, Gandhi K, Mughal M, Shaham Y, van Praag H (2011) Running is the neurogenic and neurotrophic stimulus in environmental enrichment. Learn Mem 18:605-609
46. Koehl M, Abrous DN (2011) A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 33:1101-1114
47. Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033 (Pubitemid 26144015)
48. Kuhn HG, Biebl M, Wilhelm D, Li M, Friedlander RM, Winkler J (2005) Increased generation of granule cells in adult Bcl-2- overexpressing mice: a role for cell death during continued hippocampal neurogenesis. Eur J Neurosci 22:1907-1915 (Pubitemid 41579381)
49. Leyhe T, Eschweiler GW, Stransky E, Gasser T, Annas P, Basun H, Laske C (2009) Increase of BDNF serum concentration in lithium treated patients with early Alzheimer's disease. J Alzheimers Dis 16:649-656
50. Li B, Yamamori H, Tatebayashi Y, Shafit-Zagardo B, Tanimukai H, Chen S, Iqbal K, Grundke-Iqbal I (2008) Failure of neuronal maturation in Alzheimer disease dentate gyrus. J Neuropathol Exp Neurol 67:78-84
51. Lucassen PJ, Stumpel MW, Wang Q, Aronica E (2010) Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 58:940-949
52. Mahar I, Bambico FR, Mechawar N, Nobrega JN (2014) Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neurosci Biobehav Rev 38:173-192
53. Moretti DV, Frisoni GB, Binetti G, Zanetti O (2011) Anatomical substrate and scalp EEG markers are correlated in subjects with cognitive impairment and Alzheimer's disease. Front Psychiatry 1:152
54. Moser MB, Moser EI (1998) Functional differentiation in the hippocampus. Hippocampus 8:608-619
55. Mustroph ML, Chen S, Desai SC, Cay EB, DeYoung EK, Rhodes JS (2012) Aerobic exercise is the critical variable in an enriched environment that increases hippocampal neurogenesis and water maze learning in male C57BL/6J mice. Neuroscience 219:62-71
56. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, Duman RS (2002) Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 22:9868-9876 (Pubitemid 35332871)
57. Nunes PV, Forlenza OV, Gattaz WF (2007) Lithium and risk for Alzheimer's disease in elderly patients with bipolar disorder. Br J Psychiatry 190:359-360 (Pubitemid 46580688)
58. Nunes MA, Viel TA, Buck HS (2013) Microdose lithium treatment stabilized cognitive impairment in patients with Alzheimer's disease. Curr Alzheimer Res 10:104-107
59. O'Leary OF, O'Connor RM, Cryan JF (2012) Lithium-induced effects on adult hippocampal neurogenesis are topographically segregated along the dorso-ventral axis of stressed mice. Neuropharmacology 62:247-255
60. Païzanis E, Renoir T, Lelievre V, Saurini F, Melfort M, Gabriel C, Barden N, Mocaër E, Hamon M, Lanfumey L (2010) Behavioural and neuroplastic effects of the new-generation antidepressant agomelatine compared to fluoxetine in glucocorticoid receptorimpaired mice. Int J Neuropsychopharmacol 13:759-774
61. Pajonk FG, Wobrock T, Gruber O, Scherk H, Berner D, Kaizl I, Kierer A, Müller S, Oest M, Meyer T, Backens M, Schneider- Axmann T, Thornton AE, Honer WG, Falkai P (2010) Hippocampal plasticity in response to exercise in schizophrenia. Arch Gen Psychiatry 67:133-143
62. Pencea V, Bingaman KD, Freedman LJ, Luskin MB (2001) Neurogenesis in the subventricular zone and rostral migratory stream of the neonatal and adult primate forebrain. Exp Neurol 172:1-16 (Pubitemid 33141150)
63. Perry EK, Johnson M, Ekonomou A, Perry RH, Ballard C, Attems J (2012) Neurogenic abnormalities in Alzheimer's disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol Dis 47:155-162
64. Piatti VC, Davies-Sala MG, Espósito MS, Mongiat LA, Trinchero MF, Schinder AF (2011) The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 31:7715-7728
65. Reif A, Schmitt A, Fritzen S, Chourbaji S, Bartsch C, Urani A, Wycislo M, Mössner R, Sommer C, Gass P, Lesch KP (2004) Differential effect of endothelial nitric oxide synthase (NOS-III) on the regulation of adult neurogenesis and behaviour. Eur J Neurosci 20:885-895 (Pubitemid 39141296)
66. Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP (2006) Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11:514-522
67. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, Babbini F, Fabbri ME, Tessarollo L, Maffei L, Berardi N, Caleo M (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24:1850-1856 (Pubitemid 44583469)
68. Sachdev PS, Lipnicki DM, Crawford J, Reppermund S, Kochan NA, Trollor JN, Wen W, Draper B, Slavin MJ, Kang K, Lux O, Mather KA, Brodaty H, Sydney Memory, Ageing Study Team (2013) Factors predicting reversion from mild cognitive impairment to normal cognitive functioning: a population-based study. PLoS One 8:e59649
69. Sasaki T, Kitagawa K, Yagita Y, Sugiura S, Omura-Matsuoka E, Tanaka S, Matsushita K, Okano H, Tsujimoto Y, Hori M (2006) Bcl2 enhances survival of newborn neurons in the normal and ischemic hippocampus. J Neurosci Res 84:1187-1196 (Pubitemid 44654442)
70. Schaeffer EL, Kühn F, Schmitt A, Gattaz WF, Gruber O, Schneider- Axmann T, Falkai P, Schmitt A (2013) Increased cell proliferation in the rat anterior cingulate cortex following neonatal hypoxia: relevance to schizophrenia. J Neural Transm 120:187-195
71. Shapiro EM, Gonzalez-Perez O, Manuel García-Verdugo J, Alvarez- Buylla A, Koretsky AP (2006) Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain. Neuroimage 32:1150-1157 (Pubitemid 44278680)
72. Silva R, Mesquita AR, Bessa J, Sousa JC, Sotiropoulos I, Leão P, Almeida OF, Sousa N (2008) Lithium blocks stress-induced changes in depressive-like behavior and hippocampal cell fate: the role of glycogen-synthase-kinase-3beta. Neuroscience 152:656-669
73. Son H, Yu IT, Hwang SJ, Kim JS, Lee SH, Lee YS, Kaang BK (2003) Lithium enhances long-term potentiation independently of hippocampal neurogenesis in the rat dentate gyrus. J Neurochem 85:872-881 (Pubitemid 36578619)
74. Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA (2006) Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br J Psychiatry 188:510-518 (Pubitemid 43844097)
75. Strakowski SM, DelBello MP, Sax KW, Zimmerman ME, Shear PK, Hawkins JM, Larson ER (1999) Brain magnetic resonance imaging of structural abnormalities in bipolar disorder. Arch Gen Psychiatry 56:254-260 (Pubitemid 29125134)
76. Tanti A, Rainer Q, Minier F, Surget A, Belzung C (2012) Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology 63:374-384
77. Walton NM, Zhou Y, Kogan JH, Shin R, Webster M, Gross AK, Heusner CL, Chen Q, Miyake S, Tajinda K, Tamura K, Miyakawa T, Matsumoto M (2012) Detection of an immature dentate gyrus feature in human schizophrenia/bipolar patients. Transl Psychiatry 2:e135
78. Waterhouse EG, An JJ, Orefice LL, Baydyuk M, Liao GY, Zheng K, Lu B, Xu B (2012) BDNF promotes differentiation and maturation of adult-born neurons through GABAergic transmission. J Neurosci 32:14318-14330
79. West MJ (2012) Basic stereology for biologists and neuroscientists. Cold Spring Harbor, New York
80. West MJ, Slomianka L, Gundersen HJ (1991) Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497
81. Wijeratne C, Draper B (2011) Reformulation of current recommendations for target serum lithium concentration according to clinical indication, age and physical comorbidity. Aust N Z J Psychiatry 45:1026-1032
82. Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90-110
83. Winner B, Regensburger M, Schreglmann S, Boyer L, Prots I, Rockenstein E, Mante M, Zhao C, Winkler J, Masliah E, Gage FH (2012) Role of a-synuclein in adult neurogenesis and neuronal maturation in the dentate gyrus. J Neurosci 32:16906-16916
84. Yamasaki N, Maekawa M, Kobayashi K, Kajii Y, Maeda J, Soma M, Takao K, Tanda K, Ohira K, Toyama K, Kanzaki K, Fukunaga K, Sudo Y, Ichinose H, Ikeda M, Iwata N, Ozaki N, Suzuki H, Higuchi M, Suhara T, Yuasa S, Miyakawa T (2008) Alpha- CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Mol Brain 1:6
85. Yucel K, McKinnon MC, Taylor VH, Macdonald K, Alda M, Young LT, MacQueen GM (2007) Bilateral hippocampal volume increases after long-term lithium treatment in patients with bipolar disorder: a longitudinal MRI study. Psychopharmacology 195:357-367 (Pubitemid 350160270)
86. Zhu XJ, Hua Y, Jiang J, Zhou QG, Luo CX, Han X, Lu YM, Zhu DY (2006) Neuronal nitric oxide synthase-derived nitric oxide inhibits neurogenesis in the adult dentate gyrus by downregulating cyclic AMP response element binding protein phosphorylation. Neuroscience 141:827-836 (Pubitemid 44102701)