Volume 44 Issue 2
Mar.  2023
Turn off MathJax
Article Contents
Ye Li, Na-Na Xu, Zhao-Zhe Hao, Sheng Liu. Adult neurogenesis in the primate hippocampus. Zoological Research, 2023, 44(2): 315-322. doi: 10.24272/j.issn.2095-8137.2022.399
Citation: Ye Li, Na-Na Xu, Zhao-Zhe Hao, Sheng Liu. Adult neurogenesis in the primate hippocampus. Zoological Research, 2023, 44(2): 315-322. doi: 10.24272/j.issn.2095-8137.2022.399

Adult neurogenesis in the primate hippocampus

doi: 10.24272/j.issn.2095-8137.2022.399
#Authors contributed equally to this work
Funds:  This work was supported by the Natural Science Foundation of China (81961128021, 81870682), National Key R&D Program of China (2022YEF0203200), Guangdong Provincial Key R&D Programs (2018B030335001), and Science and Technology Program of Guangzhou (202007030011, 202007030010,202007030001)
More Information
  • Corresponding author: E-mail: liush87@mail.sysu.edu.cn
  • Received Date: 2023-01-05
  • Accepted Date: 2023-02-10
  • Published Online: 2023-02-11
  • Publish Date: 2023-03-18
  • Adult hippocampal neurogenesis (AHN) is crucial for learning, memory, and emotion. Deficits of AHN may lead to reduced cognitive abilities and neurodegenerative disorders, such as Alzheimer's disease. Extensive studies on rodent AHN have clarified the developmental and maturation processes of adult neural stem/progenitor cells. However, to what extent these findings apply to primates remains controversial. Recent advances in next-generation sequencing technologies have enabled in-depth investigation of the transcriptome of AHN-related populations at single-cell resolution. Here, we summarize studies of AHN in primates. Results suggest that neurogenesis is largely shared across species, but substantial differences also exist. Marker gene expression patterns in primates differ from those of rodents. Compared with rodents, the primate hippocampus has a higher proportion of immature dentate granule cells and a longer maturation period of newly generated granule cells. Future research on species divergence may deepen our understanding of the mechanisms underlying adult neurogenesis in primates.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Abrous DN, Wojtowicz JM. 2015. Interaction between neurogenesis and hippocampal memory system: new vistas. Cold Spring Harbor Perspectives in Biology, 7(6): a018952. doi: 10.1101/cshperspect.a018952
    Aizawa K, Ageyama N, Terao K, et al. 2011. Primate-specific alterations in neural stem/progenitor cells in the aged hippocampus. Neurobiology of Aging, 32(1): 140−150. doi: 10.1016/j.neurobiolaging.2008.12.011
    Aizawa K, Ageyama N, Yokoyama C, et al. 2009. Age-dependent alteration in hippocampal neurogenesis correlates with learning performance of macaque monkeys. Experimental Animals, 58(4): 403−407. doi: 10.1538/expanim.58.403
    Ammothumkandy A, Ravina K, Wolseley V, et al. 2022. Altered adult neurogenesis and gliogenesis in patients with mesial temporal lobe epilepsy. Nature Neuroscience, 25(4): 493−503. doi: 10.1038/s41593-022-01044-2
    Amrein I, Isler K, Lipp HP. 2011. Comparing adult hippocampal neurogenesis in mammalian species and orders: influence of chronological age and life history stage. European Journal of Neuroscience, 34(6): 978−987. doi: 10.1111/j.1460-9568.2011.07804.x
    Amrein I, Slomianka L, Poletaeva II, et al. 2004. Marked species and age-dependent differences in cell proliferation and neurogenesis in the hippocampus of wild-living rodents. Hippocampus, 14(8): 1000−1010. doi: 10.1002/hipo.20018
    Artegiani B, Lyubimova A, Muraro M, et al. 2017. A single-cell RNA sequencing study reveals cellular and molecular dynamics of the hippocampal neurogenic niche. Cell Reports, 21(11): 3271−3284. doi: 10.1016/j.celrep.2017.11.050
    Babcock KR, Page JS, Fallon JR, et al. 2021. Adult Hippocampal Neurogenesis in Aging and Alzheimer's Disease. Stem Cell Reports, 16(4): 681−693. doi: 10.1016/j.stemcr.2021.01.019
    Bakken TE, Jorstad NL, Hu QW, et al. 2021a. Comparative cellular analysis of motor cortex in human, marmoset and mouse. Nature, 598(7879): 111−119. doi: 10.1038/s41586-021-03465-8
    Bakken TE, van Velthoven CTJ, Menon V, et al. 2021b. Single-cell and single-nucleus RNA-seq uncovers shared and distinct axes of variation in dorsal LGN neurons in mice, non-human primates, and humans. eLife, 10: e64875. doi: 10.7554/eLife.64875
    Berg J, Sorensen SA, Ting JT, et al. 2021. Human neocortical expansion involves glutamatergic neuron diversification. Nature, 598(7879): 151−158. doi: 10.1038/s41586-021-03813-8
    Boldrini M, Fulmore CA, Tartt AN, et al. 2018. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell, 22(4): 589−599.e5. doi: 10.1016/j.stem.2018.03.015
    Cadwell CR, Palasantza A, Jiang XL, et al. 2016. Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq. Nature Biotechnology, 34(2): 199−203. doi: 10.1038/nbt.3445
    Cassé F, Richetin K, Toni N. 2018. Astrocytes' contribution to adult neurogenesis in physiology and Alzheimer's disease. Frontiers in Cellular Neuroscience, 12: 432.
    Cipriani S, Ferrer I, Aronica E, et al. 2018. Hippocampal radial glial subtypes and their neurogenic potential in human fetuses and healthy and Alzheimer's disease adults. Cerebral Cortex, 28(7): 2458−2478. doi: 10.1093/cercor/bhy096
    Deng W, Aimone JB, Gage FH. 2010. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nature Reviews Neuroscience, 11(5): 339−350. doi: 10.1038/nrn2822
    Dennis CV, Suh LS, Rodriguez ML, et al. 2016. Human adult neurogenesis across the ages: an immunohistochemical study. Neuropathology and Applied Neurobiology, 42(7): 621−638. doi: 10.1111/nan.12337
    Eckenhoff MF, Rakic P. 1988. Nature and fate of proliferative cells in the hippocampal dentate gyrus during the life span of the rhesus monkey. The Journal of Neuroscience, 8(8): 2729−2747. doi: 10.1523/JNEUROSCI.08-08-02729.1988
    Eriksson PS, Perfilieva E, Björk-Eriksson T, et al. 1998. Neurogenesis in the adult human hippocampus. Nature Medicine, 4(11): 1313−1317. doi: 10.1038/3305
    Ernst A, Alkass K, Bernard S, et al. 2014. Neurogenesis in the striatum of the adult human brain. Cell, 156(5): 1072−1083. doi: 10.1016/j.cell.2014.01.044
    Essa H, Peyton L, Hasan W, et al. 2022. Implication of Adult Hippocampal Neurogenesis in Alzheimer's Disease and Potential Therapeutic Approaches. Cells, 11(2).
    Flor-García M, Terreros-Roncal J, Moreno-Jiménez EP, et al. 2020. Unraveling human adult hippocampal neurogenesis. Nature Protocols, 15(2): 668−693. doi: 10.1038/s41596-019-0267-y
    Franjic D, Skarica M, Ma S, et al. 2022. Transcriptomic taxonomy and neurogenic trajectories of adult human, macaque, and pig hippocampal and entorhinal cells. Neuron, 110(3): 452−469.e14. doi: 10.1016/j.neuron.2021.10.036
    Gould E, Reeves AJ, Fallah M, et al. 1999. Hippocampal neurogenesis in adult Old World primates. Proceedings of the National Academy of Sciences of the United States of America, 96(9): 5263−5267. doi: 10.1073/pnas.96.9.5263
    Gould E, Vail N, Wagers M, et al. 2001. Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proceedings of the National Academy of Sciences of the United States of America, 98(19): 10910−10917. doi: 10.1073/pnas.181354698
    Habib N, Avraham-Davidi I, Basu A, et al. 2017. Massively parallel single-nucleus RNA-seq with DroNc-seq. Nature Methods, 14(10): 955−958. doi: 10.1038/nmeth.4407
    Habib N, Li YQ, Heidenreich M, et al. 2016. Div-Seq: single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons. Science, 353(6302): 925−928. doi: 10.1126/science.aad7038
    Han L, Wei XY, Liu CY, et al. 2022. Cell transcriptomic atlas of the non-human primate Macaca fascicularis. Nature, 604(7907): 723–731.
    Hao ZZ, Wei JR, Xiao DC, et al. 2022. Single-cell transcriptomics of adult macaque hippocampus reveals neural precursor cell populations. Nature Neuroscience, 25(6): 805−817. doi: 10.1038/s41593-022-01073-x
    Harris KD, Hochgerner H, Skene NG, et al. 2018. Classes and continua of hippocampal CA1 inhibitory neurons revealed by single-cell transcriptomics. PLoS Biology, 16(6): e2006387. doi: 10.1371/journal.pbio.2006387
    Harris L, Rigo P, Stiehl T, et al. 2021. Coordinated changes in cellular behavior ensure the lifelong maintenance of the hippocampal stem cell population. Cell Stem Cell, 28(5): 863−876.e6. doi: 10.1016/j.stem.2021.01.003
    Hernández-Rabaza V, Llorens-Martín M, Velázquez-Sánchez C, 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(1): 59−68. doi: 10.1016/j.neuroscience.2008.11.054
    Hochgerner H, Zeisel A, Lönnerberg P, et al. 2018. Conserved properties of dentate gyrus neurogenesis across postnatal development revealed by single-cell RNA sequencing. Nature Neuroscience, 21(2): 290−299. doi: 10.1038/s41593-017-0056-2
    Hodge RD, Bakken TE, Miller JA, et al. 2019. Conserved cell types with divergent features in human versus mouse cortex. Nature, 573(7772): 61−68. doi: 10.1038/s41586-019-1506-7
    Hodge RD, Miller JA, Novotny M, et al. 2020. Transcriptomic evidence that von Economo neurons are regionally specialized extratelencephalic-projecting excitatory neurons. Nature Communications, 11(1): 1172. doi: 10.1038/s41467-020-14952-3
    Huang WJ, Xu Q, Su J, et al. 2022. Linking transcriptomes with morphological and functional phenotypes in mammalian retinal ganglion cells. Cell Reports, 40(11): 111322. doi: 10.1016/j.celrep.2022.111322
    Kempermann G. 2014. Off the beaten track: new neurons in the adult human striatum. Cell, 156(5): 870−871. doi: 10.1016/j.cell.2014.02.027
    Kempermann G, Gage FH, Aigner L, et al. 2018. Human adult neurogenesis: evidence and remaining questions. Cell Stem Cell, 23(1): 25−30. doi: 10.1016/j.stem.2018.04.004
    Kent BA, Hvoslef-Eide M, Saksida LM, et al. 2016. The representational-hierarchical view of pattern separation: not just hippocampus, not just space, not just memory?. Neurobiology of Learning and Memory, 129: 99−106. doi: 10.1016/j.nlm.2016.01.006
    Kim TA, Syty MD, Wu K, et al. 2022. Adult hippocampal neurogenesis and its impairment in Alzheimer's disease. Zoological Research, 43(3): 481−496. doi: 10.24272/j.issn.2095-8137.2021.479
    Knoth R, Singec I, Ditter M, et al. 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
    Korsunsky I, Millard N, Fan J, et al. 2019. Fast, sensitive and accurate integration of single-cell data with Harmony. Nature Methods, 16(12): 1289−1296. doi: 10.1038/s41592-019-0619-0
    Kozareva V, Martin C, Osorno T, et al. 2021. A transcriptomic atlas of mouse cerebellar cortex comprehensively defines cell types. Nature, 598(7879): 214−219. doi: 10.1038/s41586-021-03220-z
    La Manno G, Soldatov R, Zeisel A, et al. 2018. RNA velocity of single cells. Nature, 560(7719): 494−498. doi: 10.1038/s41586-018-0414-6
    Lake BB, Chen S, Sos BC, et al. 2018. Integrative single-cell analysis of transcriptional and epigenetic states in the Human Adult Brain. Nature Biotechnology, 36(1): 70−80. doi: 10.1038/nbt.4038
    Lemaire V, Koehl M, Le Moal M, et al. 2000. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 97(20): 11032−11037. doi: 10.1073/pnas.97.20.11032
    Leng F, Edison P. 2021. Neuroinflammation and microglial activation in Alzheimer disease: where do we go from here. Nature Reviews Neurology, 17(3): 157−172. doi: 10.1038/s41582-020-00435-y
    Leuner B, Kozorovitskiy Y, Gross CG, et al. 2007. Diminished adult neurogenesis in the marmoset brain precedes old age. Proceedings of the National Academy of Sciences of the United States of America, 104(43): 17169−17173. doi: 10.1073/pnas.0708228104
    Luo YP, Coskun V, Liang AB, et al. 2015. Single-cell transcriptome analyses reveal signals to activate dormant neural stem cells. Cell, 161(5): 1175−1186. doi: 10.1016/j.cell.2015.04.001
    Masuda T, Sankowski R, Staszewski O, et al. 2020. Microglia heterogeneity in the single-cell era. Cell Reports, 30(5): 1271−1281. doi: 10.1016/j.celrep.2020.01.010
    Maynard KR, Collado-Torres L, Weber LM, et al. 2021. Transcriptome-scale spatial gene expression in the human dorsolateral prefrontal cortex. Nature Neuroscience, 24(3): 425−436. doi: 10.1038/s41593-020-00787-0
    Moreno-Jiménez EP, Flor-García M, Terreros-Roncal J, et al. 2019. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer's disease. Nature Medicine, 25(4): 554−560. doi: 10.1038/s41591-019-0375-9
    Moreno-Jiménez EP, Terreros-Roncal J, Flor-García M, et al. 2021. Evidences for adult hippocampal neurogenesis in humans. Journal of Neuroscience, 41(12): 2541−2553. doi: 10.1523/JNEUROSCI.0675-20.2020
    Ngwenya LB, Peters A, Rosene DL. 2006. Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. Journal of Comparative Neurology, 498(2): 204−216. doi: 10.1002/cne.21045
    Ngwenya LB, Rosene DL, Peters A. 2008. An ultrastructural characterization of the newly generated cells in the adult monkey dentate gyrus. Hippocampus, 18(2): 210−220. doi: 10.1002/hipo.20384
    Ngwenya LB, Heyworth NC, Shwe Y, et al. 2015. Age-related changes in dentate gyrus cell numbers, neurogenesis, and associations with cognitive impairments in the rhesus monkey. Frontiers in systems neuroscience, 9: 102−102.
    Nicola Z, Fabel K, Kempermann G. 2015. Development of the adult neurogenic niche in the hippocampus of mice. Frontiers in Neuroanatomy, 9: 53.
    Perera TD, Coplan JD, Lisanby SH, et al. 2007. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. Journal of Neuroscience, 27(18): 4894−4901. doi: 10.1523/JNEUROSCI.0237-07.2007
    Pollen AA, Nowakowski TJ, Chen JD, et al. 2015. Molecular identity of human outer radial glia during cortical development. Cell, 163(1): 55−67. doi: 10.1016/j.cell.2015.09.004
    Qian XY, Su YJ, Adam CD, et al. 2020. Sliced human cortical organoids for modeling distinct cortical layer formation. Cell Stem Cell, 26(5): 766−781.e9. doi: 10.1016/j.stem.2020.02.002
    Rakic P. 1985. Limits of neurogenesis in primates. Science, 227(4690): 1054−1056. doi: 10.1126/science.3975601
    Rosenberg AB, Roco CM, Muscat RA, et al. 2018. Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding. Science, 360(6385): 176−182. doi: 10.1126/science.aam8999
    Sahay A, Scobie KN, Hill AS, et al. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature, 472(7344): 466−470. doi: 10.1038/nature09817
    Schmitz MT, Sandoval K, Chen CP, et al. 2022. The development and evolution of inhibitory neurons in primate cerebrum. Nature, 603(7903): 871−877. doi: 10.1038/s41586-022-04510-w
    Shin J, Berg DA, Zhu YH, et al. 2015. Single-cell RNA-Seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell, 17(3): 360−372. doi: 10.1016/j.stem.2015.07.013
    Sierra A, Encinas JM, Maletic-Savatic M. 2011. Adult human neurogenesis: from microscopy to magnetic resonance imaging. Frontiers in Neuroscience, 5: 47.
    Sorrells SF, Paredes MF, Cebrian-Silla A, et al. 2018. Human hippocampal neurogenesis drops sharply in children to undetectable levels in adults. Nature, 555(7696): 377−381. doi: 10.1038/nature25975
    Sorrells SF, Paredes MF, Zhang ZZ, et al. 2021. Positive controls in adults and children support that very few, if any, new neurons are born in the adult human hippocampus. Journal of Neuroscience, 41(12): 2554−2565. doi: 10.1523/JNEUROSCI.0676-20.2020
    Spalding KL, Arner E, Westermark PO, et al. 2008. Dynamics of fat cell turnover in humans. Nature, 453(7196): 783−787. doi: 10.1038/nature06902
    Spalding KL, Bergmann O, Alkass K, et al. 2013. Dynamics of hippocampal neurogenesis in adult humans. Cell, 153(6): 1219−1227. doi: 10.1016/j.cell.2013.05.002
    Spalding KL, Bhardwaj RD, Buchholz BA, et al. 2005. Retrospective birth dating of cells in humans. Cell, 122(1): 133−143. doi: 10.1016/j.cell.2005.04.028
    Sultan S, Li LY, Moss J, et al. 2015. Synaptic integration of adult-born hippocampal neurons is locally controlled by astrocytes. Neuron, 88(5): 957−972. doi: 10.1016/j.neuron.2015.10.037
    Terreros-Roncal J, Moreno-Jiménez EP, Flor-García M, et al. 2021. Impact of neurodegenerative diseases on human adult hippocampal neurogenesis. Science, 374(6571): 1106−1113. doi: 10.1126/science.abl5163
    Tobin MK, Musaraca K, Disouky A, et al. 2019. Human hippocampal neurogenesis persists in aged adults and Alzheimer's disease patients. Cell Stem Cell, 24(6): 974−982.e3. doi: 10.1016/j.stem.2019.05.003
    Trapnell C, Cacchiarelli D, Grimsby J, et al. 2014. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nature Biotechnology, 32(4): 381−386. doi: 10.1038/nbt.2859
    van Galen P, Hovestadt V, Wadsworth II MH, et al. 2019. Single-cell RNA-Seq reveals AML hierarchies relevant to disease progression and immunity. Cell, 176(6): 1265−1281.e24. doi: 10.1016/j.cell.2019.01.031
    Wang W, Wang MD, Yang M, et al. 2022. Transcriptome dynamics of hippocampal neurogenesis in macaques across the lifespan and aged humans. Cell Research, 32(8): 729−743. doi: 10.1038/s41422-022-00678-y
    Wei JR, Hao ZZ, Xu C, et al. 2022. Identification of visual cortex cell types and species differences using single-cell RNA sequencing. Nature Communications, 13(1): 6902−6902. doi: 10.1038/s41467-022-34590-1
    Welch JD, Kozareva V, Ferreira A, et al. 2019. Single-cell multi-omic integration compares and contrasts features of brain cell identity. Cell, 177(7): 1873−1887.e17. doi: 10.1016/j.cell.2019.05.006
    Wolf FA, Angerer P, Theis FJ. 2018. SCANPY: large-scale single-cell gene expression data analysis. Genome Biology, 19(1): 15. doi: 10.1186/s13059-017-1382-0
    Yao ZZ, van Velthoven CTJ, Nguyen TN, et al. 2021. A taxonomy of transcriptomic cell types across the isocortex and hippocampal formation. Cell, 184(12): 3222−3241.e26. doi: 10.1016/j.cell.2021.04.021
    Zeisel A, Hochgerner H, Lönnerberg P, et al. 2018. Molecular architecture of the mouse nervous system. Cell, 174(4): 999−1014.e22. doi: 10.1016/j.cell.2018.06.021
    Zeisel A, Muñoz-Manchado AB, Codeluppi S, et al. 2015. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science, 347(6226): 1138−1142. doi: 10.1126/science.aaa1934
    Zhang H, Li JM, Ren J, et al. 2021. Single-nucleus transcriptomic landscape of primate hippocampal aging. Protein & Cell, 12(9): 695−716.
    Zhong SJ, Ding WY, Sun L, et al. 2020. Decoding the development of the human hippocampus. Nature, 577(7791): 531−536. doi: 10.1038/s41586-019-1917-5
    Zhong SJ, Zhang S, Fan XY, et al. 2018. A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex. Nature, 555(7697): 524−528. doi: 10.1038/nature25980
    Zhou Y, Su YJ, Li SY, et al. 2022. Molecular landscapes of human hippocampal immature neurons across lifespan. Nature, 607(7919): 527−533. doi: 10.1038/s41586-022-04912-w
    Zhu Y, Sousa AMM, Gao TLY, et al. 2018. Spatiotemporal transcriptomic divergence across human and macaque brain development. Science, 362(6420): eaat8077. doi: 10.1126/science.aat8077
    Ziffra RS, Kim CN, Ross JM, et al. 2021. Single-cell epigenomics reveals mechanisms of human cortical development. Nature, 598(7879): 205−213. doi: 10.1038/s41586-021-03209-8
    Zywitza V, Misios A, Bunatyan L, et al. 2018. Single-cell transcriptomics characterizes cell types in the subventricular zone and uncovers molecular defects impairing adult neurogenesis. Cell Reports, 25(9): 2457−2469.e8. doi: 10.1016/j.celrep.2018.11.003
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(3)  / Tables(1)

    Article Metrics

    Article views (1238) PDF downloads(340) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint