BMP signaling mediates effects of exercise on hippocampal neurogenesis and cognition in mice

PLoS ONE

Volumn 4, Issue 10, 2009, Pages

  Gobeske, Kevin T ^a   Das, Sunit ^a   Bonaguidi, Michael A ^a   Weiss, Craig ^a   Radulovic, Jelena ^a   Disterhoft, John F ^a   Kessler, John A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; NEURON SPECIFIC ENOLASE; NOGGIN; BMP4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; EXERCISE; FEMALE; GENE EXPRESSION REGULATION; GENE LOCATION; GENE OVEREXPRESSION; HIPPOCAMPUS; LEARNING; MALE; MAZE TEST; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CELL PROLIFERATION; METABOLISM; NERVE CELL; TRANSGENE;

MUS; MUS MUSCULUS;

ANIMALS; BEHAVIOR, ANIMAL; BONE MORPHOGENETIC PROTEIN 4; CELL PROLIFERATION; COGNITION; FEMALE; HIPPOCAMPUS; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; NEURONS; PHYSICAL CONDITIONING, ANIMAL; SIGNAL TRANSDUCTION; TRANSGENES;

EID: 70449441220     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007506     Document Type: Article

References (134)

1. 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: 2027-33.
2. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17: 5046-61.
3. Seri B, García-Verdugo JM, Collado-Morente L, McEwen BS, Alvarez-Buylla A (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478: 359-78.
4. Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130: 391-9.
5. Kronenberg G, Reuter K, Steiner B, Brandt MD, Jessberger S, et al. (2003) Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J Comp Neurol 467: 455-63.
6. Steiner B, Klempin F, Wang L, Kott M, Kettenmann H, et al. (2006) Type-2 cells as link between glial and neuronal lineage in adult hippocampal neurogenesis. Glia 54: 805-14.
7. van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96: 13427-31.
8. van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, et al. (2002) Functional neurogenesis in the adult hippocampus. Nature 415: 1030-4.
9. Kempermann G, Kunh HG, Gage FH (1997) More hippocampus neurons in adult mice living in an enriched environment. Nature 386: 493-5.
10. Kempermann G, Kuhn HG, Gage FH (1998) Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18: 3206-12.
11. Nilsson M, Perfilieva E, Johansson U, Orwar O, Eriksson PS (1999) Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. J Neurobiol 39: 569-78.
12. Shors TJ, Miesegaes G, Beylin A, Zhao M, Rydel T, et al. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410: 372-6.
13. Snyder JS, Kee N, Wojtowicz JM (2001) Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J Neurophysiol 85: 2423-31.
14. Madsen TM, Kristjansen PE, Bolwig TG, Wörtwein G (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119: 635-42.
15. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, et al. (2004) Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc Natl Acad Sci USA 100: 14385-90.
16. Deisseroth K, Singla S, Toda H, Monje M, Palmer TD, et al. (2004) Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42: 535-52.
17. Becker S (2005) A computational principle for hippocampal learning and neurogenesis. Hippocampus 15: 722-38.
18. Wiskott L, Rasch MJ, Kempermann G (2006) A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16: 329-43.
19. Chambers RA, Conroy SK (2007) Network modeling of adult neurogenesis: shifting rates of neuronal turnover optimally gears network learning according to novelty gradient. J Cogn Neurosci 19: 1-12.
20. Bakker A, Kirwan CB, Miller M, Stark CE (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 319: 1640-2.
21. Aimone JB, Wiles J, Gage FH (2009) Computational influence of adult neurogenesis on memory encoding. Neuron 61: 187-202.
22. Scharfman H (2007) The dentate gyrus: a comprehensive guide to structure, function and clinical implications. Elsevier.
23. Schmidt-Hieber C, Jonas P, Bischofberger J (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429: 184-7.
24. Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, et al. (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25: 10074-86.
25. Meltzer LA, Yabaluri R, Deisseroth K (2005) A role for circuit homeostasis in adult neurogenesis. Trends Neurosci 28: 653-60.
26. Becker S, Wojtowicz JM (2005) A model of hippocampal neurogenesis in memory and mood disorders. Trends Cogn Sci 11: 70-6.
27. Laplagne DA, Espósito MS, Piatti VC, Morgenstern NA, Zhao C, et al. (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4: e409.
28. Laplagne DA, Kamienkowski JE, Espósito MS, Piatti VC, Zhao C, et al. (2007) Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25: 2973-81.
29. Shors TJ, Townsend DA, Zhao M, Kozorovitskiy Y, Gould E (2002) Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12: 578-84.
30. Crandall J, Sakai Y, Zhang J, Koul O, Mineur Y, et al. (2004) 13-cis-retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice. Proc Natl Acad Sci USA 2004 101: 5111-6.
31. Raber J, Rola R, LeFevour A, Morhardt D, Curley J, et al. (2004) Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162: 39-47.
32. Kempermann G, Gage FH (2002) Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16: 129-36.
33. Meshi D, Drew MR, Saxe M, Ansorge MS, David D, et al. (2006) Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat Neurosci 9: 729-31.
34. Saxe MD, Malleret G, Vronskaya S, Mendez I, Garcia AD, et al. (2007) Paradoxical influence of hippocampal neurogenesis on working memory. Proc Natl Acad Sci USA 104: 4642-6.
35. Holick KA, Lee DC, Hen R, Dulawa SC (2008) Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33: 406-17.
36. Gerlai R (2001) Behavioral tests of hippocampal function: simple paradigms complex problems. Behav Brain Res 125: 269-77.
37. Niewoehner B, Single FN, Hvalby Ø, Jensen V, Meyer zum Alten Borgloh S, et al. (2007) Impaired spatial working memory but spared spatial reference memory following functional loss of NMDA receptors in the dentate gyrus. Eur J Neurosci 25: 837-46.
38. McHugh TJ, Jones MW, Quinn JJ, Balthasar N, Coppari R, et al. (2007) Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 317: 94-9.
39. Nakashiba T, Young JZ, McHugh TJ, Buhl DL, Tonegawa S (2008) Transgenic inhibition of synaptic transmission reveals role of CA3 output in hippocampal learning. Science 2008 Feb 29;319(5867): 1260-4.
40. Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54: 559-66.
41. Farioli-Vecchioli S, Saraulli D, Costanzi M, Pacioni S, Cinà I, et al. (2008) The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol 6: e246.
42. Ide Y, Fujiyama F, Okamoto-Furuta K, Tamamaki N, Kaneko T, et al. (2008) Rapid integration of young newborn dentate gyrus granule cells in the adult hippocampal circuitry. Eur J Neurosci 28: 2381-92.
43. Trouche S, Bontempi B, Roullet P, Rampon C (2009) Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc Natl Acad Sci USA 106: 5919-24.
44. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, et al. (2005) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619-23.
45. Lee I, Kesner RP (2004) Encoding versus retrieval of spatial memory: double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14: 66-76.
46. Lee I, Hunsaker MR, Kesner RP (2005) The role of hippocampal subregions in detecting spatial novelty. Behav Neurosci 119: 145-53.
47. Goodrich-Hunsaker NJ, Hunsaker MR, Kesner RP (2008) The interactions and dissociations of the dorsal hippocampus subregions: how the dentate gyrus, CA3, and CA1 process spatial information. Behav Neurosci 122: 16-26.
48. Hunsaker MR, Rosenberg JS, Kesner RP (2008) The role of the dentate gyrus, CA3a,b, and CA3c for detecting spatial and environmental novelty. Hippocampus 18: 1064-73.
49. Tsien JZ, Huerta PT, Tonegawa S (1996) The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996 Dec 27;87(7): 1327-38.
50. Seidenbecher T, Laxmi TR, Stork O, Pape HC (2003) Amygdalar and hippocampal theta rhythm synchronization during fear memory retrieval. Science 301: 846-50.
51. Saxe MD, Battaglia F, Wang JW, Malleret G, David DJ, et al. (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 103: 17501-6.
52. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM (2005) A role for adult neurogenesis in spatial long-term memory. Neuroscience 130: 843-52.
53. Fan Y, Liu Z, Weinstein PR, Fike JR, Liu J (2007) Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur J Neurosci 25: 38-46.
54. Clark PJ, Brzezinska WJ, Thomas MW, Ryzhenko NA, Toshkov SA, et al. (2008) Intact neurogenesis is required for benefits of exercise on spatial memory but not motor performance or contextual fear conditioning in C57BL/6J mice. Neuroscience 155: 1048-58.
55. Hernández-Rabaza V, Llorens-Martín M, Velázquez-Sánchez C, Ferragud A, Arcusa A, et al. (2009) Inhibition of adult hippocampal neurogenesis disrupts contextual learning but spares spatial working memory, long-term conditional rule retention and spatial reversal. Neuroscience 159: 59-68.
56. Bruel-Jungerman E, Laroche S, Rampon C (2005) New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 21: 513-21.
57. Garcia AD, Doan NB, Imura T, Bush TG, Sofroniew MV (2004) GFA-Pexpressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 7: 1233-41.
58. Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, et al. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci 11: 1153-61.
59. Singer BH, Jutkiewicz EM, Fuller CL, Lichtenwalner RJ, Zhang H, et al. (2009) Conditional ablation and recovery of forebrain neurogenesis in the mouse. J Comp Neurol 514: 567-582.
60. Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, et al. (2008) TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59: 399-412.
61. Bergami M, Rimondini R, Santi S, Blum R, Götz M, et al. (2008) Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc Natl Acad Sci USA 105: 15570-5.
62. Dupret D, Revest JM, Koehl M, Ichas F, De Giorgi F, et al. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3: e1959.
63. Zhang CL, Zou Y, He W, Gage FH, Evans RM (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451: 1004-7.
64. Jessberger S, Clark RE, Broadbent NJ, Clemenson GD Jr, Consiglio A, et al. (2009) Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn Mem 16: 147-54.
65. Gorski JA, Balogh SA, Wehner JM, Jones KR (2003) Learning deficits in forebrain-restricted brain-derived neurotrophic factor mutant mice. Neuroscience 121: 341-54.
66. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12: 656-70.
67. Trejo JL, Llorens-Martín MV, Torres-Alemán I (2008) The effects of exercise on spatial learning and anxiety-like behavior are mediated by an IGF-I-dependent mechanism related to hippocampal neurogenesis. Mol Cell Neurosci 37: 402-11.
68. Minichiello L, Korte M, Wolfer D, Kühn R, Unsicker K, et al. (1999) Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24: 401-14.
69. Bartkowska K, Paquin A, Gauthier AS, Kaplan DR, Miller FD (2007) Trk signaling regulates neural precursor cell proliferation and differentiation during cortical development. Development 134: 4369-80.
70. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, et al. (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827-35.
71. Vaynman S, Ying Z, Gomez-Pinilla F (2004) Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition. Eur J Neurosci 20: 2580-90.
72. Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, et al. (2003) VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 18: 2803-12.
73. Trejo JL, Carro E, Torres-Aleman I (2001) Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci 21: 1628-34.
74. Gross RE, Mehler MF, Mabie PC, Zang Z, Santschi L, et al. (1996) Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17: 595-606.
75. Mehler MF, Mabie PC, Zhu G, Gokhan S, Kessler JA (2000) Developmental changes in progenitor cell responsiveness to bone morphogenetic proteins differentially modulate progressive CNS lineage fate. Dev Neurosci 22: 74-85.
76. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, Garcia-Verdugo JM, et al. (2000) Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28: 713-26.
77. Fan X, Xu H, Huang Y, Cai W (2004) A combined in situ hybridization and RT-PCR method to detect spatial and temporal patterns of Noggin gene expression in embryonic and postnatal rat hippocampus. Brain Res Brain Res Protoc 13: 99-105.
78. Bonaguidi MA, McGuire T, Hu M, Kan L, Samanta J, et al. (2005) LIF and BMP signaling generate separate and discrete types of GFAP-expressing cells. Development 132: 5503-14.
79. Bonaguidi MA, Peng CY, McGuire T, Falciglia G, Gobeske KT, et al. (2008) Noggin expands neural stem cells in the adult hippocampus. J Neurosci 28: 9194-204.
80. Nohno T, Ishikawa T, Saito T, Hosokawa K, Noji S, et al. (1995) Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with BMP type I receptors. J Biol Chem 270: 22522-22526.
81. Nohe A, Hassel S, Ehrlich M, Neubauer F, Sebald W, et al. (2002) The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 277: 5330-8.
82. Derynck R, Zhang YE (2003) Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425: 577-84.
83. Samanta J, Kessler JA (2004) Interactions between ID and OLIG proteins mediate the inhibitory effects of BMP4 on oligodendroglial differentiation. Development 131: 4131-42.
84. Massagué J, Chen YG (2000) Controlling TGF-beta signaling. Genes Dev 14: 627-44.
85. Sim FJ, Lang JK, Waldau B, Roy NS, Schwartz TE, et al. (2006) Complementary patterns of gene expression by human oligodendrocyte progenitors and their environment predict determinants of progenitor maintenance and differentiation. Ann Neurol 2006 May;59(5): 763-79.
86. Fan X, Xu H, Huang Y, Cai W (2003) A combined in situ hybridization and RT-PCR method to detect spatial and temporal patterns of Noggin gene expression in embryonic and postnatal rat hippocampus. Brain Res Brain Res Protoc 13: 99-105.
87. Peretto P, Dati C, De Marchis S, Kim HH, Ukhanova M, et al. (2004) Expression of the secreted factors noggin and bone morphogenetic proteins in the subependymal layer and olfactory bulb of the adult mouse brain. Neuroscience 128: 685-96.
88. Colak D, Mori T, Brill MS, Pfeifer A, Falk S, et al. (2008) Adult neurogenesis requires Smad4-mediated bone morphogenic protein signaling in stem cells. J Neurosci 28: 434-46.
89. Gomes WA, Mehler MF, Kessler JA (2003) Transgenic overexpression of BMP4 increases astroglial and decreases oligodendroglial lineage commitment. Dev Biol 255: 164-77.
90. Guha U, Mecklenburg L, Cowin P, Kan L, O'Guin WM, et al. (2004) Bone morphogenetic protein signaling regulates postnatal hair follicle differentiation and cycling. Am J Pathol 165: 729-40.
91. Forss-Petter S, Danielson PE, Catsicas S, Battenberg E, Price J, et al. (1990) Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron 5: 187-97.
92. Thuret S, Toni N, Aigner S, Yeo GW, Gage FH (2009) Hippocampus-dependent learning is associated with adult neurogenesis in MRL/MpJ mice. Hippocampus published online Jan 12.
93. Suh H, Consiglio A, Ray J, Sawai T, D'Amour KA, et al. (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1: 515-28.
94. Van der Borght K, Havekes R, Bos T, Eggen BJ, Van der Zee EA (2007) Exercise improves memory acquisition and retrieval in the Y-maze task: relationship with hippocampal neurogenesis. Behav Neurosci 121: 324-34.
95. O'Callaghan RM, Ohle R, Kelly AM (2007) The effects of forced exercise on hippocampal plasticity in the rat: A comparison of LTP, spatial- and non-spatial learning. Behav Brain Res 176: 362-6.
96. Baruch DE, Swain RA, Helmstetter FJ (2004) Effects of exercise on Pavlovian fear conditioning. Behav Neurosci 118: 1123-7.
97. Burghardt PR, Pasumarthi RK, Wilson MA, Fadel J (2006) Alterations in fear conditioning and amygdalar activation following chronic wheel running in rats. Pharmacol Biochem Behav 84: 306-12.
98. Jackson WJ, Strong PN Jr (1969) Differential effects of hippocampal lesions upon sequential tasks and maze learning by the rat. J Comp Physiol Psychol 68: 442-50.
99. Ehninger D, Kempermann G (2006) Paradoxical effects of learning the Morris water maze on adult hippocampal neurogenesis in mice may be explained by a combination of stress and physical activity. Genes Brain Behav 5: 29-39.
100. Van Dam D, Lenders G, De Deyn PP (2006) Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem 85: 164-72.
101. Branchi I, Ricceri L (2004) Refining learning and memory assessment in laboratory rodents: an ethological perspective. Ann Ist Super Sanita 40: 231-6.
102. Leutgeb JK, Leutgeb S, Moser MB, Moser EI (2007) Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315: 961-6.
103. Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132: 645-60.
104. Baines RA (2004) Synaptic strengthening mediated my bone morphogenetic protein-dependent retrograde signaling in the drosophila CNS. J Neurosci 24: 6904-6911.
105. Sun M, Thomas MJ, Herder R, Bofenkamp ML, Selleck SB, et al. (2007) Presynaptic contributions of chordin to hippocampal plasticity and spatial learning. J Neurosci 27: 7740-50.
106. Fabel K, Kempermann G (2008) Physical activity and the regulation of neurogenesis in the adult and aging brain. Neuromolecular Med 10: 59-66.
107. Chmielnicki E, Benraiss A, Economides AN, Goldman SA (2004) Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci 24: 2133-42.
108. Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, et al. (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17: 2042-6.
109. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, et al. (2006) GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439: 589-93.
110. Hastings NB, Gould E (1999) Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol 413: 146-54.
111. Jones SP, Rahimi O, O'Boyle MP, Diaz DL, Claiborne BJ (2003) Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3. Hippocampus 13: 413-27.
112. Gutiérrez R, Romo-Parra H, Maqueda J, Vivar C, Ramírez M, et al. (2003) Plasticity of the GABAergic phenotype of the "glutamatergic" granule cells of the rat dentate gyrus. J Neurosci 23: 5594-8.
113. Wang LP, Kempermann G, Kettenmann H (2005) A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci 29: 181-9.
114. Overstreet Wadiche L, Bromberg DA, Bensen AL, Westbrook GL (2005) GABAergic signaling to newborn neurons in dentate gyrus. J Neurophysiol 94: 4528-32.
115. Shaw KN, Commins S, O'Mara SM (2003) Deficits in spatial learning and synaptic plasticity induced by the rapid and competitive broad-spectrum cyclooxygenase inhibitor ibuprofen are reversed by increasing endogenous brain-derived neurotrophic factor. Eur J Neurosci 17: 2438-46.
116. Ding Q, Vaynman S, Akhavan M, Ying Z, Gomez-Pinilla F (2006) Insulin-like growth factor I interfaces with brain-derived neurotrophic factor-mediated synaptic plasticity to modulate aspects of exercise-induced cognitive function. Neuroscience 140: 823-33.
117. Vaynman S, Ying Z, Gomez-Pinilla F (2003) Interplay between brain-derived neurotrophic factor and signal transduction modulators in the regulation of the effects of exercise on synaptic-plasticity. Neuroscience 122: 647-57.
118. Adlard PA, Perreau VM, Cotman CW (2005) The exercise-induced expression of BDNF within the hippocampus varies across life-span. Neurobiol Aging 26: 511-20.
119. Carro E, Nuñez A, Busiguina S, Torres-Aleman I (2000) Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci 20: 2926-33.
120. Walker TL, White A, Black DM, Wallace RH, Sah P, et al. (2008) Latent stem and progenitor cells in the hippocampus are activated by neural excitation. J Neurosci 28: 5240-7.
121. Aberg MA, Aberg ND, Palmer TD, Alborn AM, Carlsson-Skwirut C, et al. (2003) IGF-I has a direct proliferative effect in adult hippocampal progenitor cells. Mol Cell Neurosci 24: 23-40.
122. Hsieh J, Aimone JB, Kaspar BK, Kuwabara T, Nakashima K, et al. (2004) IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 164: 111-22.
123. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, et al. (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA 99: 11946-50.
124. Lichtenwalner RJ, Forbes ME, Bennett SA, Lynch CD, Sonntag WE, et al. (2001) Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107: 603-13.
125. Zigova T, Pencea V, Wiegand SJ, Luskin MB (1998) Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 11: 234-45.
126. Rossi C, Angelucci A, Costantin L, Braschi C, Mazzantini M, et al. (2006) Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur J Neurosci 24: 1850-6.
127. Messaoudi E, Ying SW, Kanhema T, Croll SD, Bramham CR (2002) Brain-derived neurotrophic factor triggers transcription-dependent, late phase longterm potentiation in vivo. J Neurosci 22: 7453-61.
128. Kovalchuk Y, Hanse E, Kafitz KW, Konnerth A (2002) Postsynaptic Induction of BDNF-Mediated Long-Term Potentiation. Science 295: 1729-34.
129. McCloskey DP, Croll SD, Scharfman HE (2005) Depression of synaptic transmission by vascular endothelial growth factor in adult rat hippocampus and evidence for increased efficacy after chronic seizures. J Neurosci 25: 8889-97.
130. Kim BW, Choi M, Kim YS, Park H, Lee HR, et al. (2008) Vascular endothelial growth factor (VEGF) signaling regulates hippocampal neurons by elevation of intracellular calcium and activation of calcium/ calmodulin protein kinase II and mammalian target of rapamycin. Cell Signal 20: 714-25.
131. Galvão RP, Garcia-Verdugo JM, Alvarez-Buylla A (2008) Brain-derived neurotrophic factor signaling does not stimulate subventricular zone neurogenesis in adult mice and rats. J Neurosci 28: 13368-83.
132. Suzuki S, Kiyosue K, Hazama S, Ogura A, Kashihara M, et al. (2007) Brain-derived neurotrophic factor regulates cholesterol metabolism for synapse development. J Neurosci 27: 6417-27.
133. Vega CJ, Peterson DA (2005) Stem cell proliferative history in tissue revealed by temporal halogenated thymidine analog discrimination. Nat Methods 2: 167-9.
134. Bauer S, Patterson PH (2006) Leukemia inhibitory factor promotes neural stem cell self-renewal in the adult brain. J Neurosci 26: 12089-99.