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Frontiers in Biology

Front Biol    2013, Vol. 8 Issue (3) : 295-304     https://doi.org/10.1007/s11515-013-1263-1
REVIEW
Adult neurogenesis in the mammalian brain
Simon M.G. BRAUN1,2, Sebastian JESSBERGER1,2()
1. Brain Research Institute, Faculty of Medicine, University of Zurich, 8057 Zurich, Switzerland; 2. Neuroscience Center Zurich, University of Zurich and ETH Zurich, Switzerland
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Abstract

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.

Keywords adult neurogenesis      hippocampus      stem cell      memory      neuropsychiatric disease     
Corresponding Author(s): JESSBERGER Sebastian,Email:jessberger@hifo.uzh.ch   
Issue Date: 01 June 2013
 Cite this article:   
Simon M.G. BRAUN,Sebastian JESSBERGER. Adult neurogenesis in the mammalian brain[J]. Front Biol, 2013, 8(3): 295-304.
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http://journal.hep.com.cn/fib/EN/10.1007/s11515-013-1263-1
http://journal.hep.com.cn/fib/EN/Y2013/V8/I3/295
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Simon M.G. BRAUN
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Fig.1  Neurogenic regions in the adult mouse brain. Neural stem cells (NSCs) reside in the dentate gyrus (DG) of the hippocampus as well as in the subventricular zone (SVZ) of the lateral ventricles (NSC niches shown in green). In the DG, NSCs give rise to mature granule cells. In the SVZ, progenitor cells actively proliferate and give rise to neuroblasts that migrate along the rostral migratory stream (RMS) toward the olfactory bulb (OB), where they differentiate into olfactory interneurons (neuroblast migratory path shown in red).
Fig.2  Stages of adult neurogenesis in the SVZ. Type B neural stem cells that line the lateral ventricles (LV), reside in the subventricular zone (SVZ), express Sox2 (SRY sex determining region Y-box 2, blue), GFAP (glial fibrillary acidic protein, red) and Nestin, and have a process that projects into the ventricle. The type B cells can asymmetrically divide into another B cell and a type C progenitor cell. The actively proliferating type C cells express markers such as Ascl1 (achaete-scute homolog 1) and give rise to neuroblasts (type A) that migrate to the olfactory bulb (OB) and are positive for DCX (doublecortin) and Dlx2 (distal-less homeobox 2).
Fig.3  Stages of adult neurogenesis in the DG Relatively quiescent type 1 NSCs express Sox2 and GFAP, and are labeled with GFP in the NestinGFP and Spot14GFP transgenic mouse lines. Non-radial type 2 NSCs also express Sox2 and NestinGFP and give rise to neuroblasts that actively proliferate and express MCM2 (minichromosome maintenance complex component 2) and Tbr2 (T-box brain 2) as well as the immature neuron marker DCX. The newborn neurons continue to express DCX and Prox1 for 2-3 weeks as they mature into granule cells that express Prox1, NeuN and Calbindin. During the early stages of neurogenesis, newborn neurons receive excitatory GABA input. At three weeks of age, newborn neurons switch to inhibitory GABA and excitatory glutamatergic input, and project axons toward CA3 neurons.
1 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
25 Gage F H (2000). Mammalian neural stem cells. Science , 287(5457): 1433-1438
doi: 10.1126/science.287.5457.1433 pmid:10688783
26 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
75 Squire L R (2009). The legacy of patient H.M. for neuroscience. Neuron , 61(1): 6-9
doi: 10.1016/j.neuron.2008.12.023 pmid:19146808
76 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
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