1. Brain Research Institute, Faculty of Medicine, University of Zurich, 8057 Zurich, Switzerland; 2. Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland
New neurons are generated throughout life in distinct areas of the mammalian brain. This process, called adult neurogenesis, has challenged previously held concepts about adult brain plasticity and opened novel therapeutic avenues to treat certain neuro-psychiatric diseases. Here, we review the current knowledge regarding the fate and potency of neural stem cells (NSCs), as well as the mechanisms underlying neuronal differentiation and subsequent integration. Furthermore, we discuss the functional significance of adult neurogenesis in health and disease, and offer brief insight into the future directions of the adult neurogenesis field.
. Adult neurogenesis in the mammalian brain[J]. Frontiers in Biology, 2013, 8(3): 295-304.
Simon M.G. BRAUN, Sebastian JESSBERGER. Adult neurogenesis in the mammalian brain. Front Biol, 2013, 8(3): 295-304.
Ables J L, Decarolis N A, Johnson M A, Rivera P D, Gao Z, Cooper D C, Radtke F, Hsieh J, Eisch A J (2010). Notch1 is required for maintenance of the reservoir of adult hippocampal stem cells. J Neurosci , 30(31): 10484-10492 doi: 10.1523/JNEUROSCI.4721-09.2010 pmid:20685991
2
Abramson S, Miller R G, Phillips R A (1977). The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med , 145(6): 1567-1579 doi: 10.1084/jem.145.6.1567 pmid:140917
3
Aimone J B, Deng W, Gage F H (2011). Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron , 70(4): 589-596 doi: 10.1016/j.neuron.2011.05.010 pmid:21609818
4
Altman J (1962). Are new neurons formed in the brains of adult mammals? Science , 135(3509): 1127-1128 doi: 10.1126/science.135.3509.1127 pmid:13860748
5
Amaral D G, Scharfman H E, Lavenex P (2007). The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res , 163: 3-22 doi: 10.1016/S0079-6123(07)63001-5 pmid:17765709
6
Arruda-Carvalho M, Sakaguchi M, Akers K G, Josselyn S A, Frankland P W (2011). Posttraining ablation of adult-generated neurons degrades previously acquired memories. J Neurosci , 31(42): 15113-15127 doi: 10.1523/JNEUROSCI.3432-11.2011 pmid:22016545
7
Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002). Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med , 8(9): 963-970 doi: 10.1038/nm747 pmid:12161747
8
Bonaguidi M A, Wheeler M A, Shapiro J S, Stadel R P, Sun G J, Ming G L, Song H (2011). In vivo clonal analysis reveals self-renewing and multipotent adult neural stem cell characteristics. Cell , 145(7): 1142-1155 doi: 10.1016/j.cell.2011.05.024 pmid:21664664
9
Bracko O, Singer T, Aigner S, Knobloch M, Winner B, Ray J, Clemenson G D Jr, Suh H, Couillard-Despres S, Aigner L, Gage F H, Jessberger S (2012). Gene expression profiling of neural stem cells and their neuronal progeny reveals IGF2 as a regulator of adult hippocampal neurogenesis. J Neurosci , 32(10): 3376-3387 doi: 10.1523/JNEUROSCI.4248-11.2012 pmid:22399759
10
Brill M S, Ninkovic J, Winpenny E, Hodge R D, Ozen I, Yang R, Lepier A, Gascón S, Erdelyi F, Szabo G, Parras C, Guillemot F, Frotscher M, Berninger B, Hevner R F, Raineteau O, G?tz M (2009). Adult generation of glutamatergic olfactory bulb interneurons. Nat Neurosci , 12(12): 1524-1533 doi: 10.1038/nn.2416 pmid:19881504
11
Carleton A, Petreanu L T, Lansford R, Alvarez-Buylla A, Lledo P M (2003). Becoming a new neuron in the adult olfactory bulb. Nat Neurosci , 6(5): 507-518 pmid:12704391
12
Chen D Y, Stern S A, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer R D, Alberini C M (2011). A critical role for IGF-II in memory consolidation and enhancement. Nature , 469(7331): 491-497 doi: 10.1038/nature09667 pmid:21270887
13
Clelland C D, Choi M, Romberg C, Clemenson G D Jr, Fragniere A, Tyers P, Jessberger S, Saksida L M, Barker R A, Gage F H, Bussey T J (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science , 325(5937): 210-213 doi: 10.1126/science.1173215 pmid:19590004
14
del Rio J A, Soriano E (1989). Immunocytochemical detection of 5′-bromodeoxyuridine incorporation in the central nervous system of the mouse. Brain Res Dev Brain Res , 49(2): 311-317 doi: 10.1016/0165-3806(89)90033-3 pmid:2805336
15
Deng W, Aimone J B, Gage F H (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci , 11(5): 339-350 doi: 10.1038/nrn2822 pmid:20354534
16
Deng W, Saxe M D, Gallina I S, Gage F H (2009). Adult-born hippocampal dentate granule cells undergoing maturation modulate learning and memory in the brain. J Neurosci , 29(43): 13532-13542 doi: 10.1523/JNEUROSCI.3362-09.2009 pmid:19864566
17
Doetsch F, Caillé I, Lim D A, García-Verdugo J M, Alvarez-Buylla A (1999). Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell , 97(6): 703-716 doi: 10.1016/S0092-8674(00)80783-7 pmid:10380923
18
Duan X, Chang J H, Ge S, Faulkner R L, Kim J Y, Kitabatake Y, Liu X B, Yang C H, Jordan J D, Ma D K, Liu C Y, Ganesan S, Cheng H J, Ming G L, Lu B, Song H (2007). Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell , 130(6): 1146-1158 doi: 10.1016/j.cell.2007.07.010 pmid:17825401
19
Ehm O, G?ritz C, Covic M, Sch?ffner I, Schwarz T J, Karaca E, Kempkes B, Kremmer E, Pfrieger F W, Espinosa L, Bigas A, Giachino C, Taylor V, Frisén J, Lie D C (2010). RBPJkappa-dependent signaling is essential for long-term maintenance of neural stem cells in the adult hippocampus. J Neurosci , 30(41): 13794-13807 doi: 10.1523/JNEUROSCI.1567-10.2010 pmid:20943920
20
Encinas J M, Michurina T V, Peunova N, Park J H, Tordo J, Peterson D A, Fishell G, Koulakov A, Enikolopov G (2011). Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell , 8(5): 566-579 doi: 10.1016/j.stem.2011.03.010 pmid:21549330
21
Erickson K I, Voss M W, Prakash R S, Basak C, Szabo A, Chaddock L, Kim J S, Heo S, Alves H, White S M, Wojcicki T R, Mailey E, Vieira V J, Martin S A, Pence B D, Woods J A, McAuley E, Kramer A F (2011). Exercise training increases size of hippocampus and improves memory. Proc Natl Acad Sci USA , 108(7): 3017-3022 doi: 10.1073/pnas.1015950108 pmid:21282661
22
Eriksson P S, Perfilieva E, Bj?rk-Eriksson T, Alborn A M, Nordborg C, Peterson D A, Gage F H (1998). Neurogenesis in the adult human hippocampus. Nat Med , 4(11): 1313-1317 doi: 10.1038/3305 pmid:9809557
23
Favaro R, Valotta M, Ferri A L M, Latorre E, Mariani J, Giachino C, Lancini C, Tosetti V, Ottolenghi S, Taylor V, Nicolis S K (2009). Hippocampal development and neural stem cell maintenance require Sox2-dependent regulation of Shh. Nat Neurosci , 12(10): 1248-1256 doi: 10.1038/nn.2397 pmid:19734891
24
Fenno L, Yizhar O, Deisseroth K (2011). The development and application of optogenetics. Annu Rev Neurosci , 34(1): 389-412 doi: 10.1146/annurev-neuro-061010-113817 pmid:21692661
Gao Z, Ure K, Ables J L, Lagace D C, Nave K A, Goebbels S, Eisch A J, Hsieh J (2009). Neurod1 is essential for the survival and maturation of adult-born neurons. Nat Neurosci , 12(9): 1090-1092 doi: 10.1038/nn.2385 pmid:19701197
27
Ge S, Yang C H, Hsu K S, Ming G L, Song H (2007). A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron , 54(4): 559-566 doi: 10.1016/j.neuron.2007.05.002 pmid:17521569
28
Gu Y, Arruda-Carvalho M, Wang J, Janoschka S R, Josselyn S A, Frankland P W, Ge S (2012). Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci , 15(12): 1700-1706 doi: 10.1038/nn.3260 pmid:23143513
29
Hall P A, Watt F M (1989). Stem cells: the generation and maintenance of cellular diversity. Development , 106(4): 619-633 pmid:2562658
30
Imayoshi I, Sakamoto M, Ohtsuka T, Takao K, Miyakawa T, Yamaguchi M, Mori K, Ikeda T, Itohara S, Kageyama R (2008). Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat Neurosci , 11(10): 1153-1161 doi: 10.1038/nn.2185 pmid:18758458
31
Jablonska B, Aguirre A, Raymond M, Szabo G, Kitabatake Y, Sailor K A, Ming G L, Song H, Gallo V (2010). Chordin-induced lineage plasticity of adult SVZ neuroblasts after demyelination. Nat Neurosci , 13(5): 541-550 doi: 10.1038/nn.2536 pmid:20418875
32
Jang M H, Bonaguidi M A, Kitabatake Y, Sun J, Song J, Kang E, Jun H, Zhong C, Su Y, Guo J U, Wang M X, Sailor K A, Kim J Y, Gao Y, Christian K M, Ming G L, Song H (2013). Secreted frizzled-related protein 3 regulates activity-dependent adult hippocampal neurogenesis. Cell Stem Cell , 12(2): 215-223 doi: 10.1016/j.stem.2012.11.021 pmid:23395446
33
Jessberger S, Aigner S, Clemenson G D Jr, Toni N, Lie D C, Karalay O, Overall R, Kempermann G, Gage F H (2008). Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol , 6(11): e272 doi: 10.1371/journal.pbio.0060272 pmid:18998770
34
Jessberger S, Nakashima K, Clemenson G D Jr, Mejia E, Mathews E, Ure K, Ogawa S, Sinton C M, Gage F H, Hsieh J (2007a). Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci , 27(22): 5967-5975 doi: 10.1523/JNEUROSCI.0110-07.2007 pmid:17537967
35
Jessberger S, Zhao C, Toni N, Clemenson G D Jr, Li Y, Gage F H (2007b). Seizure-associated, aberrant neurogenesis in adult rats characterized with retrovirus-mediated cell labeling. J Neurosci , 27(35): 9400-9407 doi: 10.1523/JNEUROSCI.2002-07.2007 pmid:17728453
36
Jin K, Zhu Y, Sun Y, Mao X O, Xie L, Greenberg D A (2002). Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci USA , 99(18): 11946-11950 doi: 10.1073/pnas.182296499 pmid:12181492
37
Karalay O, Doberauer K, Vadodaria K C, Knobloch M, Berti L, Miquelajauregui A, Schwark M, Jagasia R, Taketo M M, Tarabykin V, Lie D C, Jessberger S (2011). Prospero-related homeobox 1 gene (Prox1) is regulated by canonical Wnt signaling and has a stage-specific role in adult hippocampal neurogenesis. Proc Natl Acad Sci USA , 108(14): 5807-5812 doi: 10.1073/pnas.1013456108 pmid:21436036
38
Kempermann G, Kuhn H G, Gage F H (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature , 386(6624): 493-495 doi: 10.1038/386493a0 pmid:9087407
39
Knobloch M, Braun S M G, Zurkirchen L, von Schoultz C, Zamboni N, Araúzo-Bravo M J, Kovacs W J, Karalay O, Suter U, Machado R A, Roccio M, Lutolf M P, Semenkovich C F, Jessberger S (2013). Metabolic control of adult neural stem cell activity by Fasn-dependent lipogenesis. Nature , 493(7431): 226-230 doi: 10.1038/nature11689 pmid:23201681
40
Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, Meyer R P, Horvat V, Volk B, Kempermann G (2010). Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS ONE , 5(1): e8809 doi: 10.1371/journal.pone.0008809 pmid:20126454
41
Kuhn H G, Dickinson-Anson H, Gage F H (1996). Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci , 16(6): 2027-2033 pmid:8604047
42
Lavado A, Lagutin O V, Chow L M L, Baker S J, Oliver G (2010). Prox1 is required for granule cell maturation and intermediate progenitor maintenance during brain neurogenesis. PLoS Biol , 8(8): 8 doi: 10.1371/journal.pbio.1000460 pmid:20808958
43
Lazarini F, Lledo P M (2011). Is adult neurogenesis essential for olfaction? Trends Neurosci , 34(1): 20-30 doi: 10.1016/j.tins.2010.09.006 pmid:20980064
44
Lazic S E, Grote H, Armstrong R J E, Blakemore C, Hannan A J, van Dellen A, Barker R A (2004). Decreased hippocampal cell proliferation in R6/1 Huntington’s mice. Neuroreport , 15(5): 811-813 doi: 10.1097/00001756-200404090-00014 pmid:15073520
45
Lie D C, Colamarino S A, Song H J, Désiré L, Mira H, Consiglio A, Lein E S, Jessberger S, Lansford H, Dearie A R, Gage F H (2005). Wnt signalling regulates adult hippocampal neurogenesis. Nature , 437(7063): 1370-1375 doi: 10.1038/nature04108 pmid:16251967
46
Lois C, Alvarez-Buylla A (1994). Long-distance neuronal migration in the adult mammalian brain. Science , 264(5162): 1145-1148 doi: 8178174" target="_blank">10.1126/science. pmid:8178174 pmid:8178174
47
Lois C, García-Verdugo J M, Alvarez-Buylla A (1996). Chain migration of neuronal precursors. Science , 271(5251): 978-981 doi: 10.1126/science.271.5251.978 pmid:8584933
48
Lugert S, Basak O, Knuckles P, Haussler U, Fabel K, G?tz M, Haas C A, Kempermann G, Taylor V, Giachino C (2010). Quiescent and active hippocampal neural stem cells with distinct morphologies respond selectively to physiological and pathological stimuli and aging. Cell Stem Cell , 6(5): 445-456 doi: 10.1016/j.stem.2010.03.017 pmid:20452319
49
Malberg J E, Eisch A J, Nestler E J, Duman R S (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci , 20(24): 9104-9110 pmid:11124987
50
Marín-Burgin A, Mongiat L A, Pardi M B, Schinder A F (2012). Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science , 335(6073): 1238-1242 doi: 10.1126/science.1214956 pmid:22282476
51
Milner B, Squire L R, Kandel E R (1998). Cognitive neuroscience and the study of memory. Neuron , 20(3): 445-468 doi: 10.1016/S0896-6273(00)80987-3 pmid:9539121
52
Mira H, Andreu Z, Suh H, Lie D C, Jessberger S, Consiglio A, San Emeterio J, Hortigüela R, Marqués-Torrejón M A, Nakashima K, Colak D, G?tz M, Fari?as I, Gage F H (2010). Signaling through BMPR-IA regulates quiescence and long-term activity of neural stem cells in the adult hippocampus. Cell Stem Cell , 7(1): 78-89 doi: 10.1016/j.stem.2010.04.016 pmid:20621052
53
Morrens J, Van Den Broeck W, Kempermann G (2012). Glial cells in adult neurogenesis. Glia , 60(2): 159-174 doi: 10.1002/glia.21247 pmid:22076934
54
Morrison S J, Shah N M, Anderson D J (1997). Regulatory mechanisms in stem cell biology. Cell , 88(3): 287-298 doi: 10.1016/S0092-8674(00)81867-X pmid:9039255
55
Nakada D, Saunders T L, Morrison S J (2010). Lkb1 regulates cell cycle and energy metabolism in haematopoietic stem cells. Nature , 468(7324): 653-658 doi: 10.1038/nature09571 pmid:21124450
56
Nissant A, Pallotto M (2011). Integration and maturation of newborn neurons in the adult olfactory bulb—from synapses to function. Eur J Neurosci , 33(6): 1069-1077 doi: 10.1111/j.1460-9568.2011.07605.x pmid:21395850
57
Palmer T D, Ray J, Gage F H (1995). FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci , 6(5): 474-486 doi: 10.1006/mcne.1995.1035 pmid:8581317
58
Parent J M, Yu T W, Leibowitz R T, Geschwind D H, Sloviter R S, Lowenstein D H (1997). Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci , 17(10): 3727-3738 pmid:9133393
59
Potten C S, Loeffler M (1987). A comprehensive model of the crypts of the small intestine of the mouse provides insight into the mechanisms of cell migration and the proliferation hierarchy. J Theor Biol , 127(4): 381-391 doi: 10.1016/S0022-5193(87)80136-4 pmid:3328018
60
Potten C S, Loeffler M (1990). Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development , 110(4): 1001-1020 pmid:2100251
61
Pun R Y K, Rolle I J, Lasarge C L, Hosford B E, Rosen J M, Uhl J D, Schmeltzer S N, Faulkner C, Bronson S L, Murphy B L, Richards D A, Holland K D, Danzer S C (2012). Excessive activation of mTOR in postnatally generated granule cells is sufficient to cause epilepsy. Neuron , 75(6): 1022-1034 doi: 10.1016/j.neuron.2012.08.002 pmid:22998871
62
Ramón y Cajal S (1928) Degeneration and regeneration of the nervous system. Oxford University Press .
63
Reynolds B A, Weiss S (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science , 255(5052): 1707-1710 doi: 1553558" target="_blank">10.1126/science. pmid:1553558 pmid:1553558
64
Rochefort C, Gheusi G, Vincent J D, Lledo P M (2002). Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory. J Neurosci , 22(7): 2679-2689 pmid:11923433
65
Rodríguez J J, Jones V C, Tabuchi M, Allan S M, Knight E M, LaFerla F M, Oddo S, Verkhratsky A (2008). Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer’s disease. PLoS ONE , 3(8): e2935 doi: 10.1371/journal.pone.0002935 pmid:18698410
66
Sahay A, Scobie K N, Hill A S, O’Carroll C M, Kheirbek M A, Burghardt N S, Fenton A A, Dranovsky A, Hen R (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature , 472(7344): 466-470 doi: 10.1038/nature09817 pmid:21460835
67
Sanai N, Nguyen T, Ihrie R A, Mirzadeh Z, Tsai H H, Wong M, Gupta N, Berger M S, Huang E, Garcia-Verdugo J M, Rowitch D H, Alvarez-Buylla A (2011). Corridors of migrating neurons in the human brain and their decline during infancy. Nature , 478(7369): 382-386 doi: 10.1038/nature10487 pmid:21964341
68
Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science , 301(5634): 805-809 doi: 10.1126/science.1083328 pmid:12907793
69
Scharfman H, Goodman J, Macleod A, Phani S, Antonelli C, Croll S (2005). Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp Neurol , 192(2): 348-356 doi: 10.1016/j.expneurol.2004.11.016 pmid:15755552
70
Schmidt-Hieber C, Jonas P, Bischofberger J (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature , 429(6988): 184-187 doi: 10.1038/nature02553 pmid:15107864
71
Seib D R M, Corsini N S, Ellwanger K, Plaas C, Mateos A, Pitzer C, Niehrs C, Celikel T, Martin-Villalba A (2013). Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell , 12(2): 204-214 doi: 10.1016/j.stem.2012.11.010 pmid:23395445
72
Seri B, García-Verdugo J M, McEwen B S, Alvarez-Buylla A (2001). Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci , 21(18): 7153-7160 pmid:11549726
73
Snyder J S, Soumier A, Brewer M, Pickel J, Cameron H A (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature , 476(7361): 458-461 doi: 10.1038/nature10287 pmid:21814201
74
Song J, Zhong C, Bonaguidi M A, Sun G J, Hsu D, Gu Y, Meletis K, Huang Z J, Ge S, Enikolopov G, Deisseroth K, Luscher B, Christian K M, Ming G L, Song H (2012). Neuronal circuitry mechanism regulating adult quiescent neural stem-cell fate decision. Nature , 489(7414): 150-154 doi: 10.1038/nature11306 pmid:22842902
Suh H, Consiglio A, Ray J, Sawai T, D’Amour K A, Gage F H (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(5): 515-528 doi: 10.1016/j.stem.2007.09.002 pmid:18371391
77
Tashiro A, Makino H, Gage F H (2007). Experience-specific functional modification of the dentate gyrus through adult neurogenesis: a critical period during an immature stage. J Neurosci , 27(12): 3252-3259 doi: 10.1523/JNEUROSCI.4941-06.2007 pmid:17376985
78
Tashiro A, Sandler V M, Toni N, Zhao C, Gage F H (2006). NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrus. Nature , 442(7105): 929-933 doi: 10.1038/nature05028 pmid:16906136
79
Toni N, Laplagne D A, Zhao C, Lombardi G, Ribak C E, Gage F H, Schinder A F (2008). Neurons born in the adult dentate gyrus form functional synapses with target cells. Nat Neurosci , 11(8): 901-907 doi: 10.1038/nn.2156 pmid:18622400
80
Toni N, Teng E M, Bushong E A, Aimone J B, Zhao C, Consiglio A, van Praag H, Martone M E, Ellisman M H, Gage F H (2007). Synapse formation on neurons born in the adult hippocampus. Nat Neurosci , 10(6): 727-734 doi: 10.1038/nn1908 pmid:17486101
81
Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T (2005). GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron , 47(6): 803-815 doi: 10.1016/j.neuron.2005.08.023 pmid:16157276
82
Vadodaria K C, Brakebusch C, Suter U, Jessberger S (2013). Stage-specific functions of the small Rho GTPases Cdc42 and Rac1 for adult hippocampal neurogenesis. J Neurosci , 33(3): 1179-1189 doi: 10.1523/JNEUROSCI.2103-12.2013 pmid:23325254
83
van Praag H, Kempermann G, Gage F H (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci , 2(3): 266-270 doi: 10.1038/6368 pmid:10195220
84
van Praag H, Schinder A F, Christie B R, Toni N, Palmer T D, Gage F H (2002). Functional neurogenesis in the adult hippocampus. Nature , 415(6875): 1030-1034 doi: 10.1038/4151030a pmid:11875571
85
Wang L P, Kempermann G, Kettenmann H (2005). A subpopulation of precursor cells in the mouse dentate gyrus receives synaptic GABAergic input. Mol Cell Neurosci , 29(2): 181-189 doi: 10.1016/j.mcn.2005.02.002 pmid:15911343
86
Winner B, Lie D C, Rockenstein E, Aigner R, Aigner L, Masliah E, Kuhn H G, Winkler J (2004). Human wild-type alpha-synuclein impairs neurogenesis. J Neuropathol Exp Neurol , 63(11): 1155-1166 pmid:15581183
87
Yamaguchi M, Saito H, Suzuki M, Mori K (2000). Visualization of neurogenesis in the central nervous system using nestin promoter-GFP transgenic mice. Neuroreport , 11(9): 1991-1996 doi: 10.1097/00001756-200006260-00037 pmid:10884058
88
Zhao C, Deng W, Gage F H (2008). Mechanisms and functional implications of adult neurogenesis. Cell , 132(4): 645-660 doi: 10.1016/j.cell.2008.01.033 pmid:18295581
89
Zhao C, Teng E M, Summers R G Jr, Ming G L, Gage F H (2006). Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci , 26(1): 3-11 doi: 10.1523/JNEUROSCI.3648-05.2006 pmid:16399667
