The existence of neurogenesis in the adult human hippocampus has been under considerable debate within the past three decades due to the diverging conclusions originating mostly from immunohistochemistry studies. While some of these reports conclude that hippocampal neurogenesis in humans occurs throughout physiologic aging, others indicate that this phenomenon ends by early childhood. More recently, some groups have adopted next-generation sequencing technologies to characterize with more acuity the extent of this phenomenon in humans. Here, we review the current state of research on adult hippocampal neurogenesis in the human brain with an emphasis on the challenges and limitations of using immunohistochemistry and next-generation sequencing technologies for its study.
AlshebibYHoriTGoelAFauziAAKashiwagiT.2023. Adult human neurogenesis: a view from two schools of thought. IBRO Neurosci Rep15:342–7.
3.
AltmanJ.1963. Autoradiographic investigation of cell proliferation in the brains of rats and cats. Anat Rec145:573–91.
4.
AltmanJDasGD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol124(3):319–35.
5.
AmaralDGScharfmanHELavenexP.2007. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res163:3–22.
6.
AmmothumkandyARavinaKWolseleyVTarttANYuPNCoronaL, and others. 2022. Altered adult neurogenesis and gliogenesis in patients with mesial temporal lobe epilepsy. Nat Neurosci25(4):493–503.
7.
AmreinIIslerKLippHP. 2011. Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage. Eur J Neurosci34(6):978–87.
8.
AmreinISlomiankaLPoletaevaIIBologovaNVLippHP. 2004. Marked species and age-dependent differences in cell proliferation and neurogenesis in the hippocampus of wild-living rodents. Hippocampus14(8):1000–10.
9.
AyhanFKulkarniABertoSSivaprakasamKDouglasCLegaBC, and others. 2021. Resolving cellular and molecular diversity along the hippocampal anterior-to-posterior axis in humans. Neuron109(13):2091–105.e2096.
10.
Ben AbdallahNMSlomiankaLVyssotskiALLippHP. 2010. Early age-related changes in adult hippocampal neurogenesis in c57 mice. Neurobiol Aging31(1):151–61.
11.
BenedettiBCouillard-DespresS.2022. Why would the brain need dormant neuronal precursors?Front Neurosci16:877167.
12.
BenedettiBReisingerMHochwartnerMGabrieleGJakubecovaDBenedettiA, and others. 2023. The awakening of dormant neuronal precursors in the adult and aged brain. Aging Cell22(12):e13974.
13.
BergmannOLieblJBernardSAlkassKYeungMSSteierP, and others. 2012. The age of olfactory bulb neurons in humans. Neuron74(4):634–9.
14.
BhardwajRDCurtisMASpaldingKLBuchholzBAFinkDBjörk-ErikssonT, and others. 2006. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci U S A103:12564–8.
15.
BieblMCooperCMWinklerJKuhnHG. 2000. Analysis of neurogenesis and programmed cell death reveals a self-renewing capacity in the adult rat brain. Neurosci Lett291(1):17–20.
16.
BoldriniMFulmoreCATarttANSimeonLRPavlovaIPoposkaV, and others. 2018. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell22(4):589–99, e585.
17.
BoldriniMUnderwoodMDHenRRosoklijaGBDworkAJJohn MannJ, and others. 2009. Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology34(11):2376–89.
18.
BonfantiLLa RosaCGhibaudiMSherwoodCC. 2023. Adult neurogenesis and “immature” neurons in mammals: an evolutionary trade-off in plasticity?Brain Struct Funct. doi:10.1007/s00429-023-02717-9
19.
BonfantiLSekiT.2021. The PSA-NCAM–positive “immature” neurons: an old discovery providing new vistas on brain structural plasticity. Cells10(10):2542.
20.
BrandtMDJessbergerSSteinerBKronenbergGReuterKBick-SanderA, and others. 2003. Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci24(3):603–13.
21.
BraunEDanan-GottholdMBormLELeeKWVinslandELonnerbergP, and others. 2023. Comprehensive cell atlas of the first-trimester developing human brain. Science382(6667):eadf1226.
22.
CameronHAWoolleyCSMcEwenBSGouldE.1993. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience56:337–44.
23.
ChengMJiangYXuJMentisAAWangSZhengH, and others. 2023. Spatially resolved transcriptomics: a comprehensive review of their technological advances, applications, and challenges. J Genet Genomics50(9):625–40.
24.
CiprianiSFerrerIAronicaEKovacsGGVerneyCNardelliJ, and others. 2018. Hippocampal radial glial subtypes and their neurogenic potential in human fetuses and healthy and Alzheimer’s disease adults. Cereb Cortex28(7):2458–78.
25.
ClellandCDChoiMRombergCClemensonGDFragniereATyersP, and others. 2009. A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science325(5937):210–3.
26.
Couillard-DespresSWinnerBSchaubeckSAignerRVroemenMWeidnerN, and others. 2005. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci21(1):1–14.
27.
DengWMayfordMGageFH. 2013. Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. Elife2:e00312.
28.
DuqueAArellanoJIRakicP.2022. An assessment of the existence of adult neurogenesis in humans and value of its rodent models for neuropsychiatric diseases. Mol Psychiatry27(1):377–82.
29.
DuqueASpectorR.2019. A balanced evaluation of the evidence for adult neurogenesis in humans: implication for neuropsychiatric disorders. Brain Struct Funct224(7):2281–95.
30.
EncinasJMMichurinaTVPeunovaNParkJHTordoJPetersonDA, and others. 2011. Division-coupled astrocytic differentiation and age-related depletion of neural stem cells in the adult hippocampus. Cell Stem Cell8(5):566–79.
31.
EncinasJMVaahtokariAEnikolopovG.2006. Fluoxetine targets early progenitor cells in the adult brain. Proc Natl Acad Sci U S A103(21):8233–8.
32.
ErikssonPSPerfilievaEBjörk-ErikssonTAlbornA-MNordborgCPetersonDA, and others. 1998. Neurogenesis in the adult human hippocampus. Nature Medicine4(11):1313–7.
33.
ErnstAAlkassKBernardSSalehpourMPerlSTisdaleJ, and others. 2014. Neurogenesis in the striatum of the adult human brain. Cell156(5):1072–83.
34.
FilippovVKronenbergGPivnevaTReuterKSteinerBWangLP, and others. 2003. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci23(3):373–82.
35.
Flor-GarciaMTerreros-RoncalJMoreno-JimenezEPAvilaJRabanoALlorens-MartinM.2020. Unraveling human adult hippocampal neurogenesis. Nat Protoc15(2):668–93.
36.
FranjicDSkaricaMMaSArellanoJITebbenkampATNChoiJ, and others. 2022. Transcriptomic taxonomy and neurogenic trajectories of adult human, macaque, and pig hippocampal and entorhinal cells. Neuron110(3):452–69, e414.
GarciaADDoanNBImuraTBushTGSofroniewMV. 2004. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci7(11):1233–41.
39.
GaultNSzeleFG. 2021. Immunohistochemical evidence for adult human neurogenesis in health and disease. WIREs Mech Dis13(6):e1526.
40.
GebaraEBonaguidiMABeckervordersandforthRSultanSUdryFGijsPJ, and others. 2016. Heterogeneity of radial glia–like cells in the adult hippocampus. Stem Cells34(4):997–1010.
41.
GhibaudiMAmentaAAgostiMRivaMGraicJMBifariF, and others. 2023. Consistency and variation in doublecortin and KI67 antigen detection in the brain tissue of different mammals, including humans. Int J Mol Sci24(3):2514.
42.
GleesonJGLinPTFlanaganLAWalshCA. 1999. Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron23(2):257–71.
43.
GouldEBeylinATanapatPReevesAShorsTJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci2(3):260–5.
44.
GouldETanapatPMcEwenBSFlüggeGFuchsE.1998. Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proc Natl Acad Sci U S A95(6):3168–71.
45.
GradyCL.2020. Meta-analytic and functional connectivity evidence from functional magnetic resonance imaging for an anterior to posterior gradient of function along the hippocampal axis. Hippocampus30(5):456–71.
46.
GregoryJMMcDadeKLiveseyMRCroyIMarion de ProceSAitmanT, and others. 2020. Spatial transcriptomics identifies spatially dysregulated expression of GRM3 and USP47 in amyotrophic lateral sclerosis. Neuropathol Appl Neurobiol46(5):441–57.
47.
HabibNAvraham-DavidiIBasuABurksTShekharKHofreeM, and others. 2017. Massively parallel single-nucleus RNA-seq with DroNc-seq. Nat Methods14(10):955–8.
48.
HagiharaHMuranoTOhiraKMiwaMNakamuraKMiyakawaT.2019. Expression of progenitor cell/immature neuron markers does not present definitive evidence for adult neurogenesis. Mol Brain12(1):108.
49.
HainmuellerTBartosM.2020. Dentate gyrus circuits for encoding, retrieval and discrimination of episodic memories. Nat Rev Neurosci21(3):153–68.
50.
HaqueAEngelJTeichmannSALonnbergT.2017. A practical guide to single-cell RNA-sequencing for biomedical research and clinical applications. Genome Med9(1):75.
51.
HastingsNBGouldE.1999. Rapid extension of axons into the CA3 region by adult-generated granule cells. J Comp Neurol413(1):146–54.
52.
HochgernerHZeiselALonnerbergPLinnarssonS.2018. Conserved properties of dentate gyrus neurogenesis across postnatal development revealed by single-cell RNA sequencing. Nat Neurosci21(2):290–9.
53.
IwanoTMasudaAKiyonariHEnomotoHMatsuzakiF.2012. Prox1 postmitotically defines dentate gyrus cells by specifying granule cell identity over CA3 pyramidal cell fate in the hippocampus. Development139(16):3051–62.
54.
JinnoS.2011. Topographic differences in adult neurogenesis in the mouse hippocampus: a stereology-based study using endogenous markers. Hippocampus21(5):467–80.
55.
JustNChevillardPMMigaudM.2022. Imaging and spectroscopic methods to investigate adult neurogenesis in vivo: new models and new avenues. Front Neurosci16:933947.
56.
KaplanMSHindsJW. 1977. Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science197:1092–4.
57.
KempermannG.2008. The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for?Trends Neurosci31(4):163–9.
58.
KempermannG.2022. What is adult hippocampal neurogenesis good for?Front Neurosci16:852680.
59.
KempermannGGageFHAignerLSongHCurtisMAThuretS, and others. 2018. Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell23(1):25–30.
60.
KempermannGGastDKronenbergGYamaguchiMGageFH. 2003. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development130(2):391–9.
61.
KempermannGJessbergerSSteinerBKronenbergG.2004. Milestones of neuronal development in the adult hippocampus. Trends Neurosci27(8):447–52.
62.
KempermannGSongHGageFH. 2015. Neurogenesis in the adult hippocampus. Cold Spring Harb Perspect Biol7(9):a018812.
63.
KheirbekMAHenR.2011. Dorsal vs ventral hippocampal neurogenesis: implications for cognition and mood. Neuropsychopharmacology36(1):373–4.
64.
KimCNShinDWangANowakowskiTJ. 2023. Spatiotemporal molecular dynamics of the developing human thalamus. Science382(6667):eadf9941.
65.
KimEJAblesJLDickelLKEischAJJohnsonJE. 2011. Ascl1 (Mash1) defines cells with long-term neurogenic potential in subgranular and subventricular zones in adult mouse brain. PLoS One6(3):e18472.
66.
KintnerC.2002. Neurogenesis in embryos and in adult neural stem cells. J Neurosci22(3):639–43.
67.
KnothRSingecIDitterMPantazisGCapetianPMeyerRP, and others. 2010. Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One5(1):e8809.
68.
KohlerSJWilliamsNIStantonGBCameronJLGreenoughWT. 2011. Maturation time of new granule cells in the dentate gyrus of adult macaque monkeys exceeds six months. Proc Natl Acad Sci U S A108(25):10326–31.
69.
KornackDRRakicP.1999. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci U S A96(10):5768–73.
70.
KuhnHGDickinson-AnsonHGageFH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci16(6): 2027–33.
71.
La MannoGSoldatovRZeiselABraunEHochgernerHPetukhovV, and others. 2018. Rna velocity of single cells. Nature560(7719):494–8.
72.
La RosaCBonfantiL. 2021. Searching for alternatives to brain regeneration. Neural Regen Res16(11):2198–200.
73.
La RosaCGhibaudiMBonfantiL. 2019. Newly generated and non-newly generated “immature” neurons in the mammalian brain: a possible reservoir of young cells to prevent brain aging and disease?J Clin Med8(5):685.
74.
LaDageLDMagedRMForneyMVRothTC2ndSinervoBPravosudovVV. 2013. Interaction between territoriality, spatial environment, and hippocampal neurogenesis in male side-blotched lizards. Behav Neurosci127(4):555–65.
75.
LiSZhangPChenWYeLBrannanKWLeNT, and others. 2023. A relay velocity model infers cell-dependent RNA velocity. Nat Biotechnol42(1):99–108.
76.
LiYLiZWangCYangMHeZWangF, and others. 2023. Spatiotemporal transcriptome atlas reveals the regional specification of the developing human brain. Cell186(26):5892–909, e5822.
77.
LiYNHuDDCaiXLWangYYangCJiangJ, and others. 2023. Doublecortin-expressing neurons in human cerebral cortex layer II and amygdala from infancy to 100 years old. Mol Neurobiol60(6):3464–85.
78.
LippHPBonfantiL.2016. Adult neurogenesis in mammals: variations and confusions. Brain Behav Evol87(3):205–21.
79.
LiuJYWMatarinMReevesCMcEvoyAWMiserocchiAThompsonP, and others. 2018. Doublecortin-expressing cell types in temporal lobe epilepsy. Acta Neuropathol Commun6(1):60.
80.
LongoSKGuoMGJiALKhavariPA. 2021. Integrating single-cell and spatial transcriptomics to elucidate intercellular tissue dynamics. Nat Rev Genet22(10):627–44.
81.
LuZZhangMLeeJSzirakiAAndersonSZhangZ, and others. 2023. Tracking cell-type-specific temporal dynamics in human and mouse brains. Cell186(20):4345–64, e4324.
82.
LucassenPJStumpelMWWangQAronicaE.2010. Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology58(6):940–9.
83.
LucassenPJToniNKempermannGFrisenJGageFHSwaabDF. 2020. Limits to human neurogenesis-really?Mol Psychiatry25(10):2207–9.
84.
MaDKBonaguidiMAMingGLSongH.2009. Adult neural stem cells in the mammalian central nervous system. Cell Res19(6):672–82.
85.
MaekawaMTakashimaNAraiYNomuraTInokuchiKYuasaS, and others. 2005. Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells10(10):1001–14.
86.
ManganasLNZhangXLiYHazelRDSmithSDWagshulME, and others. 2007. Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science318(5852):980–5.
87.
ManiatisSÄijöTVickovicSBraineCKangKMollbrinkA, and others. 2019. Spatiotemporal dynamics of molecular pathology in amyotrophic lateral sclerosis. Science364(6435):89–93.
88.
MarkakisEAGageFH. 1999. Adult-generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles. J Comp Neurol406(4):449–60.
MarxV.2021. Method of the year: spatially resolved transcriptomics. Nat Methods18(1):9–14.
91.
MaynardKRCollado-TorresLWeberLMUytingcoCBarryBKWilliamsSR, and others. 2021. Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nat Neurosci24(3):425–36.
92.
Mendez-DavidIDavidDJDelomenieCTritschlerLBeaulieuJMColleR, and others. 2023. A complex relation between levels of adult hippocampal neurogenesis and expression of the immature neuron marker doublecortin. Hippocampus33(10):1075–93.
93.
MeskenaiteVKrackowSLippHP. 2016. Age-dependent neurogenesis and neuron numbers within the olfactory bulb and hippocampus of homing pigeons. Front Behav Neurosci10:126.
94.
MillerJANathansonJFranjicDShimSDalleyRAShapouriS, and others. 2013. Conserved molecular signatures of neurogenesis in the hippocampal subgranular zone of rodents and primates. Development140(22):4633–44.
95.
Moreno-JimenezEPFlor-GarciaMTerreros-RoncalJRabanoACafiniFPallas-BazarraN, and others. 2019. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat Med25(4):554–60.
96.
Moreno-JimenezEPTerreros-RoncalJFlor-GarciaMRabanoALlorens-MartinM.2021. Evidences for adult hippocampal neurogenesis in humans. J Neurosci41(12):2541–53.
97.
MosesLPachterL.2022. Museum of spatial transcriptomics. Nat Methods19(5):534–46.
98.
NgwenyaLBHeyworthNCShweYMooreTLRoseneDL. 2015. Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey. Front Syst Neurosci9:102.
99.
NgwenyaLBPetersARoseneDL. 2006. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol498(2):204–16.
100.
OomenCAMayerJLde KloetERJoelsMLucassenPJ. 2007. Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci26(12):3395–401.
101.
PalmerTDTakahashiJGageFH. 1997. The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci8(6):389–404.
102.
PereiraACHuddlestonDEBrickmanAMSosunovAAHenRMcKhannGM, and others. 2007. An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci U S A104:5638–43.
103.
PereraTDDworkAJKeeganKAThirumangalakudiLLipiraCMJoyceN, and others. 2011. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS One6(4):e17600.
104.
RamiABréhierAT M.RabiéA.1987. Cholecalcin (28-kDa calcium-binding protein) in the rat hippocampus: development in normal animals and in altered thyroid states. An immunocytochemical study. Dev Biol124(1):228–38.
105.
RammPCouillard-DespresSPlotzSRiveraFJKrampertMLehnerB, and others. 2009. A nuclear magnetic resonance biomarker for neural progenitor cells: is it all neurogenesis?Stem Cells27(2):420–3.
106.
RibakCShapiroL.2007. Dendritic development of newly generated neurons in the adult brain. Brain Res Rev55(2):390–4.
107.
RoederSSBonninEAWuTDGuerquin-KernJLJabariSBrandnerS, and others. 2023. Tracking cell turnover in human brain using (15)N-thymidine imaging mass spectrometry. Front Neurosci17:1274607.
108.
RoederSSBurkardtPRostFRodeJBruschLCorasR, and others. 2022. Evidence for postnatal neurogenesis in the human amygdala. Commun Biol5(1):366.
109.
RoybonLHjaltTStottSGuillemotFLiJYBrundinP.2009. Neurogenin2 directs granule neuroblast production and amplification while NeuroD1 specifies neuronal fate during hippocampal neurogenesis. PLoS One4(3):e4779.
110.
SantoroA.2013. Reassessing pattern separation in the dentate gyrus. Front Behav Neurosci7:96.
111.
SekiT.2002. Expression patterns of immature neuronal markers PSA-NCAM, CRMP-4 and NEUROD in the hippocampus of young adult and aged rodents. J Neurosci Res70(3):327–34.
112.
SekiT.2020. Understanding the real state of human adult hippocampal neurogenesis from studies of rodents and non-human primates. Front Neurosci14:839.
113.
SekiTHoriTMiyataHMaeharaMNambaT.2019. Analysis of proliferating neuronal progenitors and immature neurons in the human hippocampus surgically removed from control and epileptic patients. Sci Rep9(1):18194.
114.
SierraAEncinasJMDeuderoJJChanceyJHEnikolopovGOverstreet-WadicheLS, and others. 2010. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell7(4):483–95.
115.
SilettiKHodgeRMossi AlbiachALeeKWDingSLHuL, and others. 2023. Transcriptomic diversity of cell types across the adult human brain. Science382(6667):eadd7046.
116.
SorrellsSFParedesMFCebrian-SillaASandovalKQiDKelleyKW, and others. 2018. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature555(7696):377–81.
117.
SorrellsSFParedesMFVelmeshevDHerranz-PérezVSandovalKMayerS, and others. 2019. Immature excitatory neurons develop during adolescence in the human amygdala. Nat Commun10(1):2748.
118.
SorrellsSFParedesMFZhangZKangGPastor-AlonsoOBiagiottiS, and others. 2021. Positive controls in adults and children support that very few, if any, new neurons are born in the adult human hippocampus. J Neurosci41(12):2554–65.
119.
SpaldingKLBergmannOAlkassKBernardSSalehpourMHuttnerHB, and others. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell153(6):1219–27.
120.
SpaldingKLBhardwajRDBuchholzBADruidHFrisenJ.2005. Retrospective birth dating of cells in humans. Cell122(1):133–43.
121.
SteinerBKronenbergGJessbergerSBrandtMDReuterKKempermannG.2004. Differential regulation of gliogenesis in the context of adult hippocampal neurogenesis in mice. Glia46(1):41–52.
SuhHConsiglioARayJSawaiTD’AmourKAGageFH. 2007. In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell1(5):515–28.
124.
TaupinP.2007. Brdu immunohistochemistry for studying adult neurogenesis: paradigms, pitfalls, limitations, and validation. Brain Res Rev53(1):198–214.
125.
Terreros-RoncalJFlor-GarciaMMoreno-JimenezEPRodriguez-MorenoCBMarquez-ValadezBGallardo-CaballeroM, and others. 2023. Methods to study adult hippocampal neurogenesis in humans and across the phylogeny. Hippocampus33(4):271–306.
126.
Terreros-RoncalJMoreno-JimenezEPFlor-GarciaMRodriguez-MorenoCBTrincheroMFCafiniF, and others. 2021. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis. Science374(6571):1106–13.
127.
TerstegeDJAddo-OsafoKCampbell TeskeyGEppJR.2022. New neurons in old brains: implications of age in the analysis of neurogenesis in post-mortem tissue. Mol Brain15(1):38.
128.
TobinMKMusaracaKDisoukyAShettiABheriAHonerWG, and others. 2019. Human hippocampal neurogenesis persists in aged adults and Alzheimer’s disease patients. Cell Stem Cell24(6):974–82, e973.
129.
TodaTParylakSLLinkerSBGageFH. 2019. The role of adult hippocampal neurogenesis in brain health and disease. Mol Psychiatry24(1):67–87.
130.
ToniNSchinderAF. 2015. Maturation and functional integration of new granule cells into the adult hippocampus. Cold Spring Harb Perspect Biol8(1):a018903.
131.
TosoniGAyyildizDBryoisJMacnairWFitzsimonsCPLucassenPJ, and others. 2023. Mapping human adult hippocampal neurogenesis with single-cell transcriptomics: reconciling controversy or fueling the debate?Neuron111(11):1714–31, e1713.
132.
TranMNMaynardKRSpanglerAHuukiLAMontgomeryKDSadashivaiahV, and others. 2021. Single-nucleus transcriptome analysis reveals cell-type-specific molecular signatures across reward circuitry in the human brain. Neuron109(19):3088–103, e3085.
133.
VerwerRWSluiterAABalesarRABaayenJCNoskeDPDirvenCM, and others. 2007. Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain130(pt 12):3321–35.
134.
WalkerTLOverallRWVoglerSSykesAMRuhwaldSLasseD, and others. 2016. Lysophosphatidic acid receptor is a functional marker of adult hippocampal precursor cells. Stem Cell Reports6(4):552–65.
135.
WangWWangMYangMZengBQiuWMaQ, and others. 2022. Transcriptome dynamics of hippocampal neurogenesis in macaques across the lifespan and aged humans. Cell Res32(8):729–43.
136.
WestMJGundersenHJ. 1990. Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol296(1):1–22.
137.
WuMVShamyJLBediGChoiCWWallMMArangoV, and others. 2014. Impact of social status and antidepressant treatment on neurogenesis in the baboon hippocampus. Neuropsychopharmacology39(8):1861–71.
138.
YaoJDaiSZhuRTanJZhaoQYinY, and others. 2024. Deciphering molecular heterogeneity and dynamics of human hippocampal neural stem cells at different ages and injury states. eLife12:RP89507.
139.
YueLLiuFHuJYangPWangYDongJ, and others. 2023. A guidebook of spatial transcriptomic technologies, data resources and analysis approaches. Comput Struct Biotechnol J21:940–55.
140.
ZeidmanPMaguireEA. 2016. Anterior hippocampus: the anatomy of perception, imagination and episodic memory. Nat Rev Neurosci17(3):173–82.
141.
ZhaoXvan PraagH.2020. Steps towards standardized quantification of adult neurogenesis. Nat Commun11(1):4275.
142.
ZhengSCStein-O’BrienGBoukasLGoffLAHansenKD. 2023. Pumping the brakes on RNA velocity by understanding and interpreting RNA velocity estimates. Genome Biol24(1):246.
143.
ZhouYSuYLiSKennedyBCZhangDYBondAM, and others. 2022. Molecular landscapes of human hippocampal immature neurons across lifespan. Nature607(7919):527–33.
144.
ZocherSOverallRWBerdugo-VegaGRundNKarasinskyAAdusumilliVS, and others. 2021. De novo DNA methylation controls neuronal maturation during adult hippocampal neurogenesis. EMBO J40(18):e107100.
145.
ZupancGKHinschKGageFH. 2005. Proliferation, migration, neuronal differentiation, and long-term survival of new cells in the adult zebrafish brain. J Comp Neurol488(3):290–319.
