Effects of protein restriction during gestation and lactation on cell proliferation in the hippocampus and subventricular zone: Functional implications. Protein restriction alters hippocampal/SVZ cell proliferation

Brain Research

Volumn 1496, Issue , 2013, Pages 10-27

  Godoy, Mariana Araya De ^a   Souza, Amanda Santos De ^a   Lobo, Mônica Alves ^a   Sampaio, Omar Vidal Kress ^a   Moraes, Louise ^a   Baldanza, Marcelo Ribeiro ^a   Magri, Tatiana Przybylski Ribeiro ^a   Wernerck De Castro, João Pedro Saar ^a   Tavares Do Carmo, Maria Das Graças ^a   Soares Mota, Márcia ^a   Rocha, Monica Santos ^a   Mendez Otero, Rosalia ^a   Santiago, Marcelo Felippe ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Behavior; Cell proliferation; Metabolic programming; Protein restriction; SGZ; SVZ

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; FORCED SWIMMING TEST; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LACTATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN DIET; PROTEIN RESTRICTION; RAT; SMELLING; SUBVENTRICULAR ZONE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; AVOIDANCE LEARNING; BROMODEOXYURIDINE; CELL PROLIFERATION; CEREBRAL VENTRICLES; DIET, PROTEIN-RESTRICTED; EXPLORATORY BEHAVIOR; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HINDLIMB SUSPENSION; HIPPOCAMPUS; HISTONES; KI-67 ANTIGEN; LACTATION; MALE; MAZE LEARNING; NEUROGENESIS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SWIMMING;

RATTUS; RATTUS NORVEGICUS;

EID: 84872875161     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.10.047     Document Type: Article

References (125)

1. D.N. Abrous, M. Koehl, and M. Le Moal Adult neurogenesis: from precursors to network and physiology Physiol. Rev. 85 2005 523 569 (Pubitemid 40404636)
2. R.D. Airan, L.A. Meltzer, M. Roy, Y. Gong, H. Chen, and K. Deisseroth High speed imaging reveals neurophysiological links to behavior in an animal model of depression Science 317 2007 819 823 (Pubitemid 47257922)
3. C. Akman, Q. Zhao, X. Liu, and G.L. Holmes Effect of food deprivation during early development on cognition and neurogenesis in the rat Epilepsy Behav.: E&B 5 2004 446 454 (Pubitemid 39060700)
4. M. Alonso, C. Viollet, M.M. Gabellec, V. Meas-Yedid, J.C. Olivo-Marin, and P.M. Lledo Olfactory discrimination learning increases the survival of adult-born neurons in the olfactory bulb J. Neurosci.: Off. J. Soc. Neurosci. 26 2006 10508 10513 (Pubitemid 44564601)
5. S.S. Almeida, J. Tonkiss, and J.R. Galler Prenatal protein malnutrition affects the social interactions of juvenile rats Physiol. Behav. 60 1996 197 201 (Pubitemid 126335874)
6. J. Altman, and G.D. Das Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats J. Comp. Neurol. 124 1965 319 335
7. A. Alvarez-Buylla, J.M. Garcia-Verdugo, and A.D. Tramontin A unified hypothesis on the lineage of neural stem cells nature reviews Neuroscience 2 2001 287 293 (Pubitemid 33673069)
8. C. Aydemir, E.S. Yalcin, S. Aksaray, C. Kisa, S.G. Yildirim, T. Uzbay, and E. Goka Brain-derived neurotrophic factor (BDNF) changes in the serum of depressed women Prog. Neuropsychopharmacol. Biol.Psychiatry 30 2006 1256 1260 (Pubitemid 44216065)
9. C. Bardy, and M. Pallotto What happens to olfaction without adult neurogenesis? Front. Neurosci. 4 2010 24
10. A. Barnea, and F. Nottebohm Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees PNAS 91 1994 11217 11221
11. S.A. Bayer, and J. Altman Hippocampal development in the rat: cytogenesis and morphogenesis examined with autoradiography and low-level X-irradiation J. Comp. Neurol. 158 1974 55 79
12. S.A. Bayer Changes in the total number of dentate granule cells in juvenile and adult rats: a correlated volumetric and 3H-thymidine autoradiographic study Exp. Brain Res. Experimentelle Hirnforschung. Experimentation cerebrale 46 1982 315 323 (Pubitemid 12040016)
13. J. Bengzon, Z. Kokaia, E. Elmer, A. Nanobashvili, M. Kokaia, and O. Lindvall Apoptosis and proliferation of dentate gyrus neurons after single and intermittent limbic seizures Proc. Natl. Acad. Sci. U S A 94 1997 10432 10437
14. R.A. Bevins, and J. Besheer Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory' Nat. Protoc. 1 2006 1306 1311
15. K. Boekhoorn, M. Joels, and P.J. Lucassen Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus Neurobiol. Dis. 24 2006 1 14 (Pubitemid 44416208)
16. M. Boldrini, M.D. Underwood, R. Hen, G.B. Rosoklija, A.J. Dwork, J. John Mann, and V. Arango Antidepressants increase neural progenitor cells in the human hippocampus Neuropsychopharmacolog.: Off. Publ. Am. Coll. Neuropsychopharmacolog. 34 2009 2376 2389
17. E. Bruel-Jungerman, S. Laroche, and C. Rampon New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment Eur. J. Neurosci. 21 2005 513 521 (Pubitemid 40204254)
18. J.E. Bruni Ependymal development, proliferation, and functions: a review Microsc. Res. Tech. 41 1998 2 13 (Pubitemid 28160601)
19. B. Chen, D. Dowlatshahi, G.M. MacQueen, J.F. Wang, and L.T. Young Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication Biol. Psychiatry 50 2001 260 265 (Pubitemid 32778442)
20. R. Chermat, B. Thierry, J.A. Mico, L. Steru, and P. Simon Adaptation of the tail suspension test to the rat J. Pharmacol-Paris 17 1986 348 350 (Pubitemid 17175387)
21. B.J. Chiasson, V. Tropepe, C.M. Morshead, and D. van der Kooy Adult mammalian forebrain ependymal and subependymal cells demonstrate proliferative potential, but only subependymal cells have neural stem cell characteristics J. Neurosci.: Off. J Soc. Neurosci. 19 1999 4462 4471 (Pubitemid 29241097)
22. J.C. Conover, and R.L. Allen The subventricular zone: new molecular and cellular developments Cell. Mol. Life Sci. 59 2002 2128 2135 (Pubitemid 36140285)
23. R. Coras, F.A. Siebzehnrubl, E. Pauli, H.B. Huttner, M. Njunting, K. Kobow, C. Villmann, E. Hahnen, W. Neuhuber, D. Weigel, M. Buchfelder, H. Stefan, H. Beck, D.A. Steindler, and I. Blumcke Low proliferation and differentiation capacities of adult hippocampal stem cells correlate with memory dysfunction in humans Brain: Int. J. Neurol. 133 2010 3359 3372
24. V. Coskun, H. Wu, B. Blanchi, S. Tsao, K. Kim, J. Zhao, J.C. Biancotti, L. Hutnick, R.C. Krueger Jr., G. Fan, J. de Vellis, and Y.E. Sun CD133+ neural stem cells in the ependyma of mammalian postnatal forebrain PNAS 105 2008 1026 1031 (Pubitemid 351282075)
25. M.R. Costa, F. Ortega, M.S. Brill, R. Beckervordersandforth, C. Petrone, T. Schroeder, M. Gotz, and B. Berninger Continuous live imaging of adult neural stem cell division and lineage progression in vitro Development 138 2011 1057 1068
26. C.G. Craig, V. Tropepe, C.M. Morshead, B.A. Reynolds, S. Weiss, and D. van der Kooy In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain J. Neurosci. Off. J. Soc. Neurosci. 16 1996 2649 2658 (Pubitemid 26122682)
27. J.F. Cryan, A. Markou, and I. Lucki Assessing antidepressant activity in rodents: recent developments and future needs Trends Pharmacol. Sci. 23 2002 238 245 (Pubitemid 34465544)
28. M.A. Curtis, V.F. Low, and R.L. Faull Neurogenesis and progenitor cells in the adult human brain: a comparison between hippocampal and subventricular progenitor proliferation Dev. Neurobiol. 72 2012 990 1005
29. S.C. Danzer Depression, stress, epilepsy and adult neurogenesis Exp. Neurol. 233 2012 22 32
30. D.J. David, J. Wang, B.A. Samuels, Q. Rainer, I. David, A.M. Gardier, and R. Hen Implications of the functional integration of adult-born hippocampal neurons in anxiety-depression disorders Neurosci.: Rev. J. Bringing Neurobiol. Neurol. Psychiatry 16 2010 578 591
31. W.A. Debassio, T.L. Kemper, J. Tonkiss, and J.R. Galler Effect of prenatal protein deprivation on postnatal granule cell generation in the hippocampal dentate gyrus Brain Res. Bull. 41 1996 379 383 (Pubitemid 26427631)
32. W. Deng, J.B. Aimone, and F.H. Gage New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nature reviews Neuroscience 11 2010 339 350
33. N.A. DeCarolis, and A.J. Eisch Hippocampal neurogenesis as a target for the treatment of mental illness: a critical evaluation Neuropharmacology 58 2010 884 893
34. A.S. de Souza, C. Pacheco Lda, S. Castro Pda, J.N. Hokoc, M.S. Rocha, and M.G. do Carmo Brain fatty acid profiles and spatial learning in malnourished rats: effects of nutritional intervention Nutr. Neurosci. 11 2008 119 127
35. G.L. Dike Severe malnutrition due to subtle neurologic deficits and epilepsy: report of three cases East Afr. Med. J. 76 1999 597 598
36. J. Dobbing, J.W. Hopewell, and A. Lynch Vulnerability of developing brain. VII. Permanent deficit of neurons in cerebral and cerebellar cortex following early mild undernutrition Exp. Neurol. 32 1971 439 447
37. F. Doetsch, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain J. Neurosci.: Off. J. Soc. Neurosci. 17 1997 5046 5061 (Pubitemid 27263818)
38. F. Doetsch, I. Caille, D.A. Lim, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Subventricular zone astrocytes are neural stem cells in the adult mammalian brain Cell 97 1999 703 716 (Pubitemid 29278045)
39. F. Doetsch The glial identity of neural stem cells Nat. Neurosci. 6 2003 1127 1134 (Pubitemid 37346029)
40. E. Drapeau, W. Mayo, C. Aurousseau, M. Le Moal, P.V. Piazza, and D.N. Abrous Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis PNAS 100 2003 14385 14390 (Pubitemid 37499246)
41. A.J. Eisch, H.A. Cameron, J.M. Encinas, L.A. Meltzer, G.L. Ming, and L.S. Overstreet-Wadiche Adult neurogenesis, mental health, and mental illness: hope or hype? J. Neurosci.: Off. J. Soc. Neurosci. 28 2008 11785 11791
42. R.G. Ellis-Hutchings, R.M. Zucker, B.E. Grey, J. Norwood Jr., J.H. Richards, C. Lau, and J.M. Rogers Altered health outcomes in adult offspring of Sprague Dawley and Wistar rats undernourished during early or late pregnancy. Birth defects research. Part B Dev. Reprod. Toxicol. 89 2010 396 407
43. A. Ennaceur, and J. Delacour A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data Behav. Brain Res. 31 1988 47 59
44. P.S. Eriksson, E. Perfilieva, T. Bjork-Eriksson, A.M. Alborn, C. Nordborg, D.A. Peterson, and F.H. Gage Neurogenesis in the adult human hippocampus Nat. Med. 4 1998 1313 1317 (Pubitemid 28512114)
45. M.L. Florian, and M.L. Nunes Effects of intra-uterine and early extra-uterine malnutrition on seizure threshold and hippocampal morphometry of pup rats Nutr. Neurosci. 13 2010 265 273
46. A.L. Fowden, D.A. Giussani, and A.J. Forhead Intrauterine programming of physiological systems: causes and consequences Physiology 21 2006 29 37 (Pubitemid 43752515)
47. F.H. Gage Mammalian neural stem cells Science 287 2000 1433 1438 (Pubitemid 30127128)
48. C. Gemma, A.D. Bachstetter, M.J. Cole, M. Fister, C. Hudson, and P.C. Bickford Blockade of caspase-1 increases neurogenesis in the aged hippocampus Eur. J. Neurosci. 26 2007 2795 2803 (Pubitemid 350115504)
49. G. Gheusi, I. Ortega-Perez, K. Murray, and P.M. Lledo A niche for adult neurogenesis in social behavior Behav. Brain Res. 200 2009 315 322
50. E.R. Glasper, T.J. Schoenfeld, and E. Gould Adult neurogenesis: optimizing hippocampal function to suit the environment Behav. Brain Res. 227 2012 380 383
51. N.J. Goodrich-Hunsaker, M.R. Hunsaker, and R.P. Kesner The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information Behav. Neurosci. 122 2008 16 26 (Pubitemid 351389700)
52. E. Gould, and P. Tanapat Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat Neuroscience 80 1997 427 436 (Pubitemid 27334592)
53. C.S. Hall Temperament: a survey of animal studies Psychol. Bull. 38 1941 909 918
54. J. Hsieh, and A.J. Eisch Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: unraveling the genome to understand the mind Neurobiol. Dis. 39 2010 73 84
55. C.B. Johansson, S. Momma, D.L. Clarke, M. Risling, U. Lendahl, and J. Frisen Identification of a neural stem cell in the adult mammalian central nervous system Cell 96 1999 25 34 (Pubitemid 29044150)
56. A.V. Kalueff, M. Wheaton, and D.L. Murphy What's wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression Behav. Brain Res. 179 2007 1 18 (Pubitemid 46441486)
57. N. Kee, S. Sivalingam, R. Boonstra, and J.M. Wojtowicz The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis J. Neurosci. Methods 115 2002 97 105 (Pubitemid 34202283)
58. N. Kee, C.M. Teixeira, A.H. Wang, and P.W. Frankland Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus Nat. Neurosci. 10 2007 355 362
59. G. Kempermann, H.G. Kuhn, and F.H. Gage More hippocampal neurons in adult mice living in an enriched environment Nature 386 1997 493 495 (Pubitemid 27164074)
60. G. Kempermann, H.G. Kuhn, and F.H. Gage Experience-induced neurogenesis in the senescent dentate gyrus J. Neurosci.: Off. J. Soc. Neurosci. 18 1998 3206 3212 (Pubitemid 28186013)
61. W.R. Kim, K. Christian, G.L. Ming, and H. Song Time-dependent involvement of adult-born dentate granule cells in behavior Behav. Brain Res. 227 2012 470 479
62. R.S. King, W.A. DeBassio, T.L. Kemper, D.L. Rosene, J. Tonkiss, J.R. Galler, and G.J. Blatt Effects of prenatal protein malnutrition and acute postnatal stress on granule cell genesis in the fascia dentata of neonatal and juvenile rats Brain Res. Dev. Brain Res. 150 2004 9 15 (Pubitemid 39090078)
63. A. Korosi, E.F. Naninck, C.A. Oomen, M. Schouten, H. Krugers, C. Fitzsimons, and P.J. Lucassen Early-life stress mediated modulation of adult neurogenesis and behavior Behav. Brain Res. 227 2012 400 409
64. H.G. Kuhn, H. Dickinson-Anson, and F.H. Gage Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation J. Neurosci.: Off. J. Soc. Neurosci. 16 1996 2027 2033 (Pubitemid 26144015)
65. C.O. Lacefield, V. Itskov, T. Reardon, R. Hen, and J.A. Gordon Effects of adult-generated granule cells on coordinated network activity in the dentate gyrus Hippocampus 22 2012 106 116
66. H.V. Lad, L. Liu, J.L. Paya-Cano, M.J. Parsons, R. Kember, and C. Fernandes Behavioural battery testing: evaluation and behavioural outcomes in 8 inbred mouse strains Physiol. Behav. 99 2010 301 316
67. S.E. Lazic Using causal models to distinguish between neurogenesis-dependent and -independent effects on behaviour J. R. Soc. Interface R. Soc. 9 2012 907 917
68. J. Lee, W. Duan, J.M. Long, D.K. Ingram, and M.P. Mattson Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats J. Mol. Neurosci.: MN. 15 2000 99 108 (Pubitemid 32108679)
69. J. Lee, K.B. Seroogy, and M.P. Mattson Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice J. Neurochem. 80 2002 539 547 (Pubitemid 36383037)
70. B.H. Lee, H. Kim, S.H. Park, and Y.K. Kim Decreased plasma BDNF level in depressive patients J. Affect. Disord. 101 2007 239 244 (Pubitemid 46879923)
71. S. Lee, J. Jeong, Y. Kwak, and S.K. Park Depression research: where are we now? Mol. Brain 3 2010 8
72. J.B. Lennington, Z. Yang, and J.C. Conover Neural stem cells and the regulation of adult neurogenesis Reprod. Biol. Endocrinol.: RB&E. 1 2003 99
73. P.D. Lewis, A.J. Patel, and R. Balazs Effect of undernutrition on cell generation in the rat hippocampus Brain Res. 168 1979 186 189 (Pubitemid 9164945)
74. J.P. Lister, G.J. Blatt, W.A. DeBassio, T.L. Kemper, J. Tonkiss, J.R. Galler, and D.L. Rosene Effect of prenatal protein malnutrition on numbers of neurons in the principal cell layers of the adult rat hippocampal formation Hippocampus 15 2005 393 403 (Pubitemid 40668358)
75. P.M. Lledo, and A. Saghatelyan Integrating new neurons into the adult olfactory bulb: joining the network, life-death decisions, and the effects of sensory experience Trends Neurosci. 28 2005 248 254 (Pubitemid 41556909)
76. P.M. Lledo, M. Alonso, and M.S. Grubb Adult neurogenesis and functional plasticity in neuronal circuits Nat. Rev. Neurosci. 7 2006 179 193 (Pubitemid 43292464)
77. C. Lois, J.M. Garcia-Verdugo, and A. Alvarez-Buylla Chain migration of neuronal precursors Science 271 1996 978 981 (Pubitemid 26066393)
78. A. Lucas Programming by early nutrition: an experimental approach J. Nutr. 128 1998 401S 406S (Pubitemid 28090391)
79. N.V. Lukoyanov, and J.P. Andrade Behavioral effects of protein deprivation and rehabilitation in adult rats: relevance to morphological alterations in the hippocampal formation Behav. Brain Res. 112 2000 85 97
80. D.K. Ma, M.A. Bonaguidi, G.L. Ming, and H. Song Adult neural stem cells in the mammalian central nervous system Cell Res. 19 2009 672 682
81. K.L. McIlwain, M.Y. Merriweather, L.A. Yuva-Paylor, and R. Paylor The use of behavioral test batteries: effects of training history Physiol. Behav. 73 2001 705 717 (Pubitemid 32885560)
82. T.M. Madsen, P.E. Kristjansen, T.G. Bolwig, and G. Wortwein Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat Neuroscience 119 2003 635 642 (Pubitemid 36694791)
83. S.S. Magavi, B.D. Mitchell, O. Szentirmai, B.S. Carter, and J.D. Macklis Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo J. Neurosci.: Off. J. Soc. Neurosci. 25 2005 10729 10739 (Pubitemid 41681921)
84. C.D. Mandyam, G.C. Harburg, and A.J. Eisch Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zone Neuroscience 146 2007 108 122 (Pubitemid 46654600)
85. R.J. Matos, R. Orozco-Solis, S. Lopes de Souza, R. Manhaes-de-Castro, and F. Bolanos-Jimenez Nutrient restriction during early life reduces cell proliferation in the hippocampus at adulthood but does not impair the neuronal differentiation process of the new generated cells Neuroscience 196 2011 16 24
86. M.P. Mattson Energy intake, meal frequency, and health: a neurobiological perspective Annu. Rev. Nutr. 25 2005 237 260 (Pubitemid 41209002)
87. R.M. Mesquita, P.A. Pereira, and J.P. Andrade Low levels of brain-derived neurotrophic factor and tyrosine kinase receptor B are related to loss of dentate granule cells after prolonged low-protein feeding in the rat Neurosci. Lett. 330 2002 155 158 (Pubitemid 35257888)
88. S. Mizumatsu, M.L. Monje, D.R. Morhardt, R. Rola, T.D. Palmer, and J.R. Fike Extreme sensitivity of adult neurogenesis to low doses of X-irradiation Cancer Res. 63 2003 4021 4027 (Pubitemid 36917922)
89. D.J. Mokler, O.I. Torres, J.R. Galler, and P.J. Morgane Stress-induced changes in extracellular dopamine and serotonin in the medial prefrontal cortex and dorsal hippocampus of prenatally malnourished rats Brain Res. 1148 2007 226 233 (Pubitemid 46602176)
90. L. Moraes, A. Vasconcelos-Dos-Santos, F.C. Santana, M.A. de Godoy, P.H. Rosado-de-Castro, Jasmin, R.L. de Azevedo-Pereira, W.M. Cintra, E.L. Gasparetto, M.F. Santiago, and R Mendez-Otero Neuroprotective effects and magnetic resonance imaging of mesenchymal stem cells labeled with SPION in a rat model of Huntington's disease Stem Cell Res. 9 2012 143 155
91. P.J. Morgane, D.J. Mokler, and J.R. Galler Effects of prenatal protein malnutrition on the hippocampal formation Neurosci. Biobehav. Rev. 26 2002 471 483 (Pubitemid 36158663)
92. P.J. Morgane, R. Austin-LaFrance, J. Bronzino, J. Tonkiss, S. Diaz-Cintra, L. Cintra, T. Kemper, and J.R Galler Prenatal malnutrition and development of the brain Neurosci. Biobehav. Rev. 17 1993 91 128 (Pubitemid 23068946)
93. R. Morris Developments of a water-maze procedure for studying spatial learning in the rat J. Neurosci. Methods 11 1984 47 60 (Pubitemid 14088970)
94. M. Nakafuku, M. Nagao, A. Grande, and A. Cancelliere Revisiting neural stem cell identity PNAS 105 2008 829 830 (Pubitemid 351282042)
95. S. Nakamura, N. Murayama, T. Noshita, H. Annoura, and T. Ohno Progressive brain dysfunction following intracerebroventricular infusion of beta(1-42)-amyloid peptide Brain Res. 912 2001 128 136 (Pubitemid 32800666)
96. C.A. Netto, and I. Izquierdo On how passive is inhibitory avoidance Behav. Neural. Biol. 43 1985 327 330 (Pubitemid 15089205)
97. M. Nilsson, E. Perfilieva, U. Johansson, O. Orwar, and P.S. Eriksson Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory J. Neurobiol. 39 1999 569 578 (Pubitemid 29260777)
98. R.S. Nowakowski, S.B. Lewin, and M.W. Miller Bromodeoxyuridine immunohistochemical determination of the lengths of the cell cycle and the DNA-synthetic phase for an anatomically defined population J. Neurocytol. 18 1989 311 318 (Pubitemid 19147398)
99. F. Ohl, and E. Fuchs Differential effects of chronic stress on memory processes in the tree shrew Brain Res. Cogn. Brain Res. 7 1999 379 387 (Pubitemid 29029979)
100. G. Paxinos, and C. Watson The rat Brain in Stereotaxic Coordinates second ed. 1986 Academic Press San Diego
101. T.D. Perera, A.J. Dwork, K.A. Keegan, L. Thirumangalakudi, C.M. Lipira, N. Joyce, C. Lange, J.D. Higley, G. Rosoklija, R. Hen, H.A. Sackeim, and J.D. Coplan Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates PLoS One 6 2011 e17600
102. R.D. Porsolt, M. Le Pichon, and M. Jalfre Depression: a new animal model sensitive to antidepressant treatments Nature 266 1977 730 732 (Pubitemid 8073804)
103. R.D. Porsolt, A. Bertin, and M. Jalfre Behavioural despair" in rats and mice: strain differences and the effects of imipramine Eur. J. Pharmacol. 51 1978 291 294 (Pubitemid 9208063)
104. R.D. Prediger, L.C. Batista, and R.N. Takahashi Caffeine reverses age-related deficits in olfactory discrimination and social recognition memory in rats. Involvement of adenosine A1 and A2A receptors Neurobiol. Aging 26 2005 957 964 (Pubitemid 40249499)
105. P.G. Reeves, F.H. Nielsen, and G.C. Fahey Jr. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet J. Nutr. 123 1993 1939 1951 (Pubitemid 23342492)
106. O. Resnick, M. Miller, W. Forbes, R. Hall, T. Kemper, J. Bronzino, and P.J. Morgane Developmental protein malnutrition: influences on the central nervous system of the rat Neurosci. Biobehav. Rev. 3 1979 233 246 (Pubitemid 10103185)
107. B.A. Samuels, and R. Hen Neurogenesis and affective disorders Eur. J. Neurosci. 33 2011 1152 1159
108. L. Santarelli, M. Saxe, C. Gross, A. Surget, F. Battaglia, S. Dulawa, N. Weisstaub, J. Lee, R. Duman, O. Arancio, C. Belzung, and R. Hen Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants Science 301 2003 805 809 (Pubitemid 36962615)
109. U. Schmitt, and C. Hiemke Combination of open field and elevated plus-maze: a suitable test battery to assess strain as well as treatment differences in rat behavior Prog. Neuropsychopharmacol. Biol. Psychiatry 22 1998 1197 1215 (Pubitemid 28511595)
110. B. Seri, J.M. Garcia-Verdugo, B.S. McEwen, and A. Alvarez-Buylla Astrocytes give rise to new neurons in the adult mammalian hippocampus J. Neurosci.: Off. J. Soc. Neurosci. 21 2001 7153 7160 (Pubitemid 32846963)
111. T.J. Shors, G. Miesegaes, A. Beylin, M. Zhao, T. Rydel, and E. Gould Neurogenesis in the adult is involved in the formation of trace memories Nature 410 2001 372 376 (Pubitemid 32246054)
112. T.J. Shors, D.A. Townsend, M. Zhao, Y. Kozorovitskiy, and E. Gould Neurogenesis may relate to some but not all types of hippocampal-dependent learning Hippocampus 12 2002 578 584 (Pubitemid 35363952)
113. T. Scholzen, and J. Gerdes The Ki-67 protein: from the known and the unknown J. Cell. Physiol. 182 2000 311 322 (Pubitemid 30054364)
114. J.S. Snyder, A. Soumier, M. Brewer, J. Pickel, and H.A. Cameron Adult hippocampal neurogenesis buffers stress responses and depressive behaviour Nature 476 2011 458 461
115. J.S. Snyder, and H.A. Cameron Could adult hippocampal neurogenesis be relevant for human behavior? Behav. Brain Res. 227 2012 384 390
116. T. Takahashi, R.S. Nowakowski, and V.S. Caviness Jr. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse J. Neurosci.: Off. J. Soc. Neurosci. 13 1993 820 833 (Pubitemid 23045162)
117. A. Tashiro, H. Makino, and F.H. Gage Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage J. Neurosci.: Off. J. Soc. Neurosci. 27 2007 3252 3259 (Pubitemid 46474131)
118. P. Taupin Stroke-induced neurogenesis: physiopathology and mechanisms Curr. Neurovascular Res. 3 2006 67 72
119. P. Taupin BrdU immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation Brain Res. Rev. 53 2007 198 214 (Pubitemid 44854215)
120. J. Tonkiss, G.A. Foster, and J.R. Galler Prenatal protein malnutrition and hippocampal function: partial reinforcement extinction effect Brain Res. Bull. 27 1991 809 813
121. K. Tureyen, R. Vemuganti, K.A. Sailor, K.K. Bowen, and R.J. Dempsey Transient focal cerebral ischemia-induced neurogenesis in the dentate gyrus of the adult mouse J. Neurosurg. 101 2004 799 805 (Pubitemid 39430973)
122. H. van Praag, G. Kempermann, and F.H. Gage Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus Nat. Neurosci. 2 1999 266 270 (Pubitemid 30491298)
123. Y. Yagita, K. Kitagawa, T. Ohtsuki, K. Takasawa, T. Miyata, H. Okano, M. Hori, and M. Matsumoto Neurogenesis by progenitor cells in the ischemic adult rat hippocampus Stroke; A J. Cereb. Circ. 32 2001 1890 1896 (Pubitemid 32772226)
124. S.Y. Yau, B.W. Lau, and K.F. So Adult hippocampal neurogenesis: a possible way how physical exercise counteracts stress Cell Transplant. 20 2011 99 111
125. B. Winner, C.M. Cooper-Kuhn, R. Aigner, J. Winkler, and H.G. Kuhn Long-term survival and cell death of newly generated neurons in the adult rat olfactory bulb Eur. J. Neurosci. 16 2002 1681 1689.T