Regulation and Function of Adult Neurogenesis. From Genes to Cognition

Aimone, J. B.; Li, Y.; Lee, S. W.; Clemenson, G. D.; Deng, W.; Gage, F. H.

doi:10.1152/physrev.00004.2014

Title: Regulation and Function of Adult Neurogenesis. From Genes to Cognition

Journal Article · Wed Oct 01 00:00:00 EDT 2014 · Physiological Reviews

DOI:https://doi.org/10.1152/physrev.00004.2014· OSTI ID:1114606

Aimone, J. B. ^[1]; Li, Y. ^[1]; Lee, S. W. ^[1]; Clemenson, G. D. ^[1]; Deng, W. ^[1]; Gage, F. H. ^[1]

Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Salt Inst. for Biological Studies, La Jolla, CA (United States)

Adult neurogenesis in the hippocampus is a notable process due not only to its uniqueness and potential impact on cognition but also to its localized vertical integration of different scales of neuroscience, ranging from molecular and cellular biology to behavior. Our review summarizes the recent research regarding the process of adult neurogenesis from these different perspectives, with particular emphasis on the differentiation and development of new neurons, the regulation of the process by extrinsic and intrinsic factors, and their ultimate function in the hippocampus circuit. Arising from a local neural stem cell population, new neurons progress through several stages of maturation, ultimately integrating into the adult dentate gyrus network. Furthermore, the increased appreciation of the full neurogenesis process, from genes and cells to behavior and cognition, makes neurogenesis both a unique case study for how scales in neuroscience can link together and suggests neurogenesis as a potential target for therapeutic intervention for a number of disorders.

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Research Organization:: Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC04-94AL85000

OSTI ID:: 1114606

Report Number(s):: SAND-2013-8756J; 476985

Journal Information:: Physiological Reviews, Vol. 94, Issue 4; ISSN 0031-9333

Publisher:: American Physiological SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 414 works

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Spatial geometry of stem cell proliferation in the adult hippocampus Mineyeva, Olga A.; Enikolopov, Grigori; Koulakov, Alexei A. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-21078-6	journal	February 2018
BMP and WNT signalling cooperate through LEF1 in the neuronal specification of adult hippocampal neural stem and progenitor cells Armenteros, Tomás; Andreu, Zoraida; Hortigüela, Rafael Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-27581-0	journal	June 2018
Growth Differentiation Factor 11 treatment leads to neuronal and vascular improvements in the hippocampus of aged mice Ozek, Ceren; Krolewski, Richard C.; Buchanan, Sean M. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-35716-6	journal	November 2018
RBFOX3/NeuN is Required for Hippocampal Circuit Balance and Function Wang, Han-Ying; Hsieh, Pei-Fen; Huang, De-Fong Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep17383	journal	December 2015
Time-lapse imaging reveals highly dynamic structural maturation of postnatally born dentate granule cells in organotypic entorhino-hippocampal slice cultures Radic, Tijana; Jungenitz, Tassilo; Singer, Mathias Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43724	journal	March 2017
Glypican-2 levels in cerebrospinal fluid predict the status of adult hippocampal neurogenesis Lugert, S.; Kremer, T.; Jagasia, R. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep46543	journal	April 2017
Noggin rescues age-related stem cell loss in the brain of senescent mice with neurodegenerative pathology Díaz-Moreno, María; Armenteros, Tomás; Gradari, Simona Proceedings of the National Academy of Sciences, Vol. 115, Issue 45 https://doi.org/10.1073/pnas.1813205115	journal	October 2018
Dlk1 dosage regulates hippocampal neurogenesis and cognition Montalbán-Loro, Raquel; Lassi, Glenda; Lozano-Ureña, Anna Proceedings of the National Academy of Sciences, Vol. 118, Issue 11 https://doi.org/10.1073/pnas.2015505118	journal	March 2021
Neural stem cell lineage-specific cannabinoid type-1 receptor regulates neurogenesis and plasticity in the adult mouse hippocampus Zimmermann, Tina; Maroso, Mattia; Beer, Annika Cerebral Cortex, Vol. 28, Issue 12 https://doi.org/10.1093/cercor/bhy258	journal	October 2018
Evaluation of hippocampal volume and serum brain-derived neurotrophic factor as potential diagnostic markers of conversion from amnestic mild cognitive impairment to Alzheimer disease Fang, Yan; Du, Naiyi; Xing, Longyan Medicine, Vol. 98, Issue 30 https://doi.org/10.1097/md.0000000000016604	journal	July 2019
Top-down inputs drive neuronal network rewiring and context-enhanced sensory processing in olfaction Adams, Wayne; Graham, James N.; Han, Xuchen PLOS Computational Biology https://doi.org/10.1101/271197	journal	February 2018
Resilience to cognitive aging is associated with responsiveness of dentate neurons generated throughout adult life Montaron, Marie-Francoise; Charrier, VAnessa; Blin, Nicolas BioRxiv https://doi.org/10.1101/290676	posted_content	January 2020
An immune-CNS axis activates remote hippocampal stem cells following Spinal Transection Injury Dehler, Sascha; Lou, Pak-Kin; Skabkin, Maxim Frontiers in Molecular Neuroscience https://doi.org/10.1101/361535	journal	July 2018
Evidence for reduced neurogenesis in the aging human hippocampus despite stable stem cell markers Mathews, Kathryn J.; Allen, Katherine M.; Boerrigter, Danny Aging Cell, Vol. 16, Issue 5 https://doi.org/10.1111/acel.12641	journal	August 2017
Transmembrane protein 108 involves in adult neurogenesis in the hippocampal dentate gyrus Yu, Zheng; Lin, Dong; Zhong, Yanzi Cell & Bioscience, Vol. 9, Issue 1 https://doi.org/10.1186/s13578-019-0272-4	journal	January 2019
ADrosophilamodel to investigate the neurotoxic side effects of radiation exposure Sudmeier, Lisa J.; Howard, Steven P.; Ganetzky, Barry Disease Models & Mechanisms, Vol. 8, Issue 7 https://doi.org/10.1242/dmm.019786	journal	July 2015
Aerobic Fitness and Neurocognitive Function Scores in Young Faroese Adults and Potential Modification by Prenatal Methylmercury Exposure Oulhote, Youssef; Debes, Frodi; Vestergaard, Sonja Environmental Health Perspectives, Vol. 125, Issue 4 https://doi.org/10.1289/ehp274	journal	April 2017
Presenilin-1 Dependent Neurogenesis Regulates Hippocampal Learning and Memory Bonds, Jacqueline A.; Kuttner-Hirshler, Yafit; Bartolotti, Nancy PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0131266	journal	June 2015
Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla) de Morais Magalhães, Nara Gyzely; Guerreiro Diniz, Cristovam; Guerreiro Diniz, Daniel PLOS ONE, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pone.0179134	journal	June 2017
Dominance behaviour in a non-aggressive flatfish, Senegalese sole (Solea senegalensis) and brain mRNA abundance of selected transcripts Fatsini, Elvira; Rey, Sonia; Ibarra-Zatarain, Zohar PLOS ONE, Vol. 12, Issue 9 https://doi.org/10.1371/journal.pone.0184283	journal	September 2017
Functional Integration of Adult-Born Hippocampal Neurons after Traumatic Brain Injury Villasana, Laura E.; Kim, Kristine N.; Westbrook, Gary L. eneuro, Vol. 2, Issue 5 https://doi.org/10.1523/eneuro.0056-15.2015	journal	September 2015
BACE1 Regulates Proliferation and Neuronal Differentiation of Newborn Cells in the Adult Hippocampus in Mice Chatila, Zena K.; Kim, Eunhee; Berlé, Clara eneuro, Vol. 5, Issue 4 https://doi.org/10.1523/eneuro.0067-18.2018	journal	July 2018
Switching roles: the functional plasticity of adult tissue stem cells Wabik, Agnieszka; Jones, Philip H. The EMBO Journal, Vol. 34, Issue 9 https://doi.org/10.15252/embj.201490386	journal	March 2015
The rostral migratory stream generates hippocampal CA1 pyramidal-like neurons in a novel organotypic slice co-culture model Singec, Ilyas; Knoth, Rolf; Vida, Imre Charité - Universitätsmedizin Berlin https://doi.org/10.17169/refubium-18249	text	January 2015
Impact of Swiprosin-1/Efhd2 on Adult Hippocampal Neurogenesis Regensburger, Martin; Prots, Iryna; Reimer, Dorothea Charité - Universitätsmedizin Berlin https://doi.org/10.17169/refubium-24279	text	January 2018
Fluoxetine attenuates the impairment of spatial learning ability and prevents neuron loss in middle-aged APPswe/PSEN1dE9 double transgenic Alzheimer's disease mice Ma, Jing; Gao, Yuan; Jiang, Lin Oncotarget, Vol. 8, Issue 17 https://doi.org/10.18632/oncotarget.15398	journal	February 2017
Chronic pain and adult hippocampal neurogenesis: translational implications from preclinical studies Grilli, Mariagrazia Journal of Pain Research, Vol. Volume 10 https://doi.org/10.2147/jpr.s146399	journal	September 2017
Stress, Depression, Resilience and Ageing: A Role for the LPA-LPA1 Pathway Dario, Moreno-Fernandez Roman; Sara, Tabbai; Estela, Castilla-Ortega Current Neuropharmacology, Vol. 16, Issue 3 https://doi.org/10.2174/1570159x15666170710200352	journal	March 2018
Mitochondrial Metabolism-Mediated Regulation of Adult Neurogenesis Beckervordersandforth, Ruth Brain Plasticity, Vol. 3, Issue 1 https://doi.org/10.3233/bpl-170044	journal	November 2017
Rewiring of Memory Circuits: Connecting Adult Newborn Neurons With the Help of Microglia Rodríguez-Iglesias, Noelia; Sierra, Amanda; Valero, Jorge Frontiers in Cell and Developmental Biology, Vol. 7 https://doi.org/10.3389/fcell.2019.00024	journal	March 2019
The Mineralocorticoid Agonist Fludrocortisone Promotes Survival and Proliferation of Adult Hippocampal Progenitors Gesmundo, Iacopo; Villanova, Tania; Gargantini, Eleonora Frontiers in Endocrinology, Vol. 7 https://doi.org/10.3389/fendo.2016.00066	journal	June 2016
Role of physical and mental training in brain network configuration Foster, Philip P. Frontiers in Aging Neuroscience, Vol. 7 https://doi.org/10.3389/fnagi.2015.00117	journal	June 2015
Differential Change in Hippocampal Radial Astrocytes and Neurogenesis in Shorebirds With Contrasting Migratory Routes Mendes de Lima, Camila; Douglas Corrêa Pereira, Patrick; Pereira Henrique, Ediely Frontiers in Neuroanatomy, Vol. 13 https://doi.org/10.3389/fnana.2019.00082	journal	September 2019
Social Plasticity Relies on Different Neuroplasticity Mechanisms across the Brain Social Decision-Making Network in Zebrafish Teles, Magda C.; Cardoso, Sara D.; Oliveira, Rui F. Frontiers in Behavioral Neuroscience, Vol. 10 https://doi.org/10.3389/fnbeh.2016.00016	journal	February 2016
Sex Differences in Stress and Group Housing Effects on the Number of Newly Proliferated Cells and Neuroblasts in Middle-Aged Dentate Gyrus Tzeng, Wen-Yu; Wu, Hsin-Hua; Wang, Ching-Yi Frontiers in Behavioral Neuroscience, Vol. 10 https://doi.org/10.3389/fnbeh.2016.00249	journal	January 2017
Involvement of calpains in adult neurogenesis: implications for stroke Machado, Vanessa M.; Morte, Maria I.; Carreira, Bruno P. Frontiers in Cellular Neuroscience, Vol. 9 https://doi.org/10.3389/fncel.2015.00022	journal	February 2015
Osteogenic and Neurogenic Stem Cells in Their Own Place: Unraveling Differences and Similarities Between Niches Lattanzi, Wanda; Parolisi, Roberta; Barba, Marta Frontiers in Cellular Neuroscience, Vol. 9 https://doi.org/10.3389/fncel.2015.00455	journal	November 2015
Exosomes as Novel Regulators of Adult Neurogenic Niches Bátiz, Luis Federico; Castro, Maite A.; Burgos, Patricia V. Frontiers in Cellular Neuroscience, Vol. 9 https://doi.org/10.3389/fncel.2015.00501	journal	January 2016
Abnormal Development of Dendrites in Adult-Born Rat Hippocampal Granule Cells Induced by Cyclophosphamide Wu, Lin; Guo, Dandan; Liu, Qi Frontiers in Cellular Neuroscience, Vol. 11 https://doi.org/10.3389/fncel.2017.00171	journal	June 2017
Adult neurogenesis 20 years later: physiological function vs. brain repair Peretto, Paolo; Bonfanti, Luca Frontiers in Neuroscience, Vol. 9 https://doi.org/10.3389/fnins.2015.00071	journal	March 2015
Altered Hippocampal Neurogenesis and Amygdalar Neuronal Activity in Adult Mice with Repeated Experience of Aggression Smagin, Dmitry A.; Park, June-Hee; Michurina, Tatyana V. Frontiers in Neuroscience, Vol. 9 https://doi.org/10.3389/fnins.2015.00443	journal	December 2015
Adult Neurogenesis 50 Years Later: Limits and Opportunities in Mammals Bonfanti, Luca Frontiers in Neuroscience, Vol. 10 https://doi.org/10.3389/fnins.2016.00044	journal	February 2016
Tamoxifen Activation of Cre-Recombinase Has No Persisting Effects on Adult Neurogenesis or Learning and Anxiety Rotheneichner, Peter; Romanelli, Pasquale; Bieler, Lara Frontiers in Neuroscience, Vol. 11 https://doi.org/10.3389/fnins.2017.00027	journal	February 2017
From Mice to Mole-Rats: Species-Specific Modulation of Adult Hippocampal Neurogenesis Oosthuizen, Maria K. Frontiers in Neuroscience, Vol. 11 https://doi.org/10.3389/fnins.2017.00602	journal	October 2017
Decreased Hippocampal Neuroplasticity and Behavioral Impairment in an Animal Model of Inhalant Abuse Malloul, Hanaa; Bennis, Mohammed; Bonzano, Sara Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.00035	journal	February 2018
Radiation Induces Distinct Changes in Defined Subpopulations of Neural Stem and Progenitor Cells in the Adult Hippocampus Mineyeva, Olga A.; Bezriadnov, Dmitri V.; Kedrov, Alexander V. Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.01013	journal	January 2019
Ginseng-Angelica-Sansheng-Pulvis Boosts Neurogenesis Against Focal Cerebral Ischemia-Induced Neurological Deficiency Liu, Bowen; Zhang, Qian; Ke, Chienchih Frontiers in Neuroscience, Vol. 13 https://doi.org/10.3389/fnins.2019.00515	journal	May 2019
Calpastatin Overexpression Preserves Cognitive Function Following Seizures, While Maintaining Post-Injury Neurogenesis Machado, Vanessa M.; Lourenço, Ana Sofia; Florindo, Cláudia Frontiers in Molecular Neuroscience, Vol. 10 https://doi.org/10.3389/fnmol.2017.00060	journal	March 2017
RNA-Sequencing Reveals Unique Transcriptional Signatures of Running and Running-Independent Environmental Enrichment in the Adult Mouse Dentate Gyrus Grégoire, Catherine-Alexandra; Tobin, Stephanie; Goldenstein, Brianna L. Frontiers in Molecular Neuroscience, Vol. 11 https://doi.org/10.3389/fnmol.2018.00126	journal	April 2018
Intrinsic Cholinergic Neurons in the Hippocampus: Fact or Artifact? Blusztajn, Jan Krzysztof; Rinnofner, Jasmine Frontiers in Synaptic Neuroscience, Vol. 8 https://doi.org/10.3389/fnsyn.2016.00006	journal	March 2016
DISC1-mediated dysregulation of adult hippocampal neurogenesis in rats Lee, Heekyung; Kang, Eunchai; GoodSmith, Douglas Frontiers in Systems Neuroscience, Vol. 9 https://doi.org/10.3389/fnsys.2015.00093	journal	June 2015
Adult hippocampal neurogenesis and pattern separation in DG: a role for feedback inhibition in modulating sparseness to govern population-based coding McAvoy, Kathleen; Besnard, Antoine; Sahay, Amar Frontiers in Systems Neuroscience, Vol. 9 https://doi.org/10.3389/fnsys.2015.00120	journal	August 2015
Opiate Analgesics as Negative Modulators of Adult Hippocampal Neurogenesis: Potential Implications in Clinical Practice Bortolotto, Valeria; Grilli, Mariagrazia Frontiers in Pharmacology, Vol. 8 https://doi.org/10.3389/fphar.2017.00254	journal	May 2017
Thinking after Drinking: Impaired Hippocampal-Dependent Cognition in Human Alcoholics and Animal Models of Alcohol Dependence Staples, Miranda C.; Mandyam, Chitra D. Frontiers in Psychiatry, Vol. 7 https://doi.org/10.3389/fpsyt.2016.00162	journal	September 2016
Brain Plasticity in Mammals: An Example for the Role of Comparative Medicine in the Neurosciences La Rosa, Chiara; Bonfanti, Luca Frontiers in Veterinary Science, Vol. 5 https://doi.org/10.3389/fvets.2018.00274	journal	November 2018
Inhibitory Effects of Auraptene and Naringin on Astroglial Activation, Tau Hyperphosphorylation, and Suppression of Neurogenesis in the Hippocampus of Streptozotocin-Induced Hyperglycemic Mice Okuyama, Satoshi; Nakashima, Tatsumi; Nakamura, Kumi Antioxidants, Vol. 7, Issue 8 https://doi.org/10.3390/antiox7080109	journal	August 2018
The Possible Roles of the Dentate Granule Cell’s Leptin and Other Ciliary Receptors in Alzheimer’s Neuropathology Whitfield, James; Chiarini, Anna; Dal Prà, Ilaria Cells, Vol. 4, Issue 3 https://doi.org/10.3390/cells4030253	journal	July 2015
α-Tocopherol and Hippocampal Neural Plasticity in Physiological and Pathological Conditions Ambrogini, Patrizia; Betti, Michele; Galati, Claudia International Journal of Molecular Sciences, Vol. 17, Issue 12 https://doi.org/10.3390/ijms17122107	journal	December 2016
Newly Generated and Non-Newly Generated “Immature” Neurons in the Mammalian Brain: A Possible Reservoir of Young Cells to Prevent Brain Aging and Disease? La Rosa, Chiara; Ghibaudi, Marco; Bonfanti, Luca Journal of Clinical Medicine, Vol. 8, Issue 5 https://doi.org/10.3390/jcm8050685	journal	May 2019
Protective effects of ethyl pyruvate on lipopolysaccharide-induced acute lung injury through inhibition of autophagy in neutrophils Zhu, Qingteng; Wang, Hui; Wang, Hairong Molecular Medicine Reports, Vol. 15, Issue 3 https://doi.org/10.3892/mmr.2017.6118	journal	January 2017
Novel insights into the role of NF-κB p50 in astrocyte-mediated fate specification of adult neural progenitor cells Grilli, Mariagrazia; Bortolotto, Valeria Neural Regeneration Research, Vol. 12, Issue 3 https://doi.org/10.4103/1673-5374.202919	journal	January 2017
Molecular Mechanism of Adult Neurogenesis and its Association with Human Brain Diseases Liu, He; Song, Ni Journal of Central Nervous System Disease, Vol. 8 https://doi.org/10.4137/jcnsd.s32204	journal	January 2016
The Role of Adult Hippocampal Neurogenesis in Learning and Memory Function Kaptan, Zülal; Üzüm, Gülay Turkish Journal Of Neurology, Vol. 22, Issue 4 https://doi.org/10.4274/tnd.68889	journal	December 2016
Repeated restraint stress promotes hippocampal neuronal cell ciliogenesis and proliferation in mice Lee, Kyounghye; Ko, Hyuk Wan Laboratory Animal Research, Vol. 34, Issue 4 https://doi.org/10.5625/lar.2018.34.4.203	journal	January 2018

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