IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0017689.html
   My bibliography  Save this article

When Are New Hippocampal Neurons, Born in the Adult Brain, Integrated into the Network That Processes Spatial Information?

Author

Listed:
  • C Jimena Sandoval
  • Marisela Martínez-Claros
  • Paola C Bello-Medina
  • Oswaldo Pérez
  • Víctor Ramírez-Amaya

Abstract

Adult-born neurons in the dentate gyrus (DG) functionally integrate into the behaviorally relevant hippocampal networks, showing a specific Arc-expression response to spatial exploration when mature. However, it is not clear when, during the 4- to 6-week interval that is critical for survival and maturation of these neurons, this specific response develops. Therefore, we characterized Arc expression after spatial exploration or cage control conditions in adult-born neurons from rats that were injected with BrdU on one day and were sacrificed 1, 7, 15, 30, and 45 days post-BrdU injection (PBI). Triple immunostaining for NeuN, Arc, and BrdU was analyzed through the different DG layers. Arc protein expression in BrdU-positive cells was observed from day 1 to day 15 PBI but was not related to behavioral stimulation. The specific Arc-expression response to spatial exploration was observed from day 30 and 45 in about 5% of the BrdU-positive cell population. Most of the BrdU-positive neurons expressing Arc in response to spatial exploration (∼90%) were located in DG layer 1, and no Arc expression was observed in cells located in the subgranular zone (SGZ). Using the current data and that obtained previously, we propose a mathematical model suggesting that new neurons are unlikely to respond to exploration by expressing Arc after they are 301 days old, and also that in a 7-month-old rat the majority (60%) of the neurons that respond to exploration must have been born during adulthood; thus, suggesting that adult neurogenesis in the DG is highly relevant for spatial information processing.

Suggested Citation

  • C Jimena Sandoval & Marisela Martínez-Claros & Paola C Bello-Medina & Oswaldo Pérez & Víctor Ramírez-Amaya, 2011. "When Are New Hippocampal Neurons, Born in the Adult Brain, Integrated into the Network That Processes Spatial Information?," PLOS ONE, Public Library of Science, vol. 6(3), pages 1-12, March.
    • Handle: RePEc:plo:pone00:0017689
    DOI: 10.1371/journal.pone.0017689
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0017689
    Download Restriction: no
    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0017689&type=printable
    Download Restriction: no
    File URL: https://libkey.io/10.1371/journal.pone.0017689?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Gerd Kempermann & H. Georg Kuhn & Fred H. Gage, 1997. "More hippocampal neurons in adult mice living in an enriched environment," Nature, Nature, vol. 386(6624), pages 493-495, April.
    2. Shaoyu Ge & Eyleen L. K. Goh & Kurt A. Sailor & Yasuji Kitabatake & Guo-li Ming & Hongjun Song, 2006. "GABA regulates synaptic integration of newly generated neurons in the adult brain," Nature, Nature, vol. 439(7076), pages 589-593, February.
    3. Henriette van Praag & Alejandro F. Schinder & Brian R. Christie & Nicolas Toni & Theo D. Palmer & Fred H. Gage, 2002. "Functional neurogenesis in the adult hippocampus," Nature, Nature, vol. 415(6875), pages 1030-1034, February.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Wen-Chung Liu & Chih-Wei Wu & Pi-Lien Hung & Julie Y. H. Chan & You-Lin Tain & Mu-Hui Fu & Lee-Wei Chen & Chih-Kuang Liang & Chun-Ying Hung & Hong-Ren Yu & I-Chun Chen & Kay L.H. Wu, 2020. "Environmental Stimulation Counteracts the Suppressive Effects of Maternal High-Fructose Diet on Cell Proliferation and Neuronal Differentiation in the Dentate Gyrus of Adult Female Offspring via Histo," IJERPH, MDPI, vol. 17(11), pages 1-15, June.
    2. Lucas A Mongiat & M Soledad Espósito & Gabriela Lombardi & Alejandro F Schinder, 2009. "Reliable Activation of Immature Neurons in the Adult Hippocampus," PLOS ONE, Public Library of Science, vol. 4(4), pages 1-11, April.
    3. Kai Diederich & Wolf-Rüdiger Schäbitz & Katharina Kuhnert & Nina Hellström & Norbert Sachser & Armin Schneider & Hans-Georg Kuhn & Stefan Knecht, 2009. "Synergetic Effects of Granulocyte-Colony Stimulating Factor and Cognitive Training on Spatial Learning and Survival of Newborn Hippocampal Neurons," PLOS ONE, Public Library of Science, vol. 4(4), pages 1-7, April.
    4. Woodley of Menie, Michael A. & Peñaherrera-Aguirre, Mateo & Sarraf, Matthew A., 2022. "Signs of a Flynn effect in rodents? Secular differentiation of the manifold of general cognitive ability in laboratory mice (Mus musculus) and Norwegian rats (Rattus norvegicus) over a century—Results," Intelligence, Elsevier, vol. 95(C).
    5. Jamie L Hanson & Amitabh Chandra & Barbara L Wolfe & Seth D Pollak, 2011. "Association between Income and the Hippocampus," PLOS ONE, Public Library of Science, vol. 6(5), pages 1-8, May.
    6. Manvendra Singh & Ying Zhao & Vinicius Daguano Gastaldi & Sonja M. Wojcik & Yasmina Curto & Riki Kawaguchi & Ricardo M. Merino & Laura Fernandez Garcia-Agudo & Holger Taschenberger & Nils Brose & Dani, 2023. "Erythropoietin re-wires cognition-associated transcriptional networks," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Jessica L Reed & Enrico D’Ambrosio & Stefano Marenco & Gianluca Ursini & Amanda B Zheutlin & Giuseppe Blasi & Barbara E Spencer & Raffaella Romano & Jesse Hochheiser & Ann Reifman & Justin Sturm & Kar, 2018. "Interaction of childhood urbanicity and variation in dopamine genes alters adult prefrontal function as measured by functional magnetic resonance imaging (fMRI)," PLOS ONE, Public Library of Science, vol. 13(4), pages 1-20, April.
    8. P. Bielefeld & A. Martirosyan & S. Martín-Suárez & A. Apresyan & G. F. Meerhoff & F. Pestana & S. Poovathingal & N. Reijner & W. Koning & R. A. Clement & I. Veen & E. M. Toledo & O. Polzer & I. Durá &, 2024. "Traumatic brain injury promotes neurogenesis at the cost of astrogliogenesis in the adult hippocampus of male mice," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Salman Sadullah Usmani & Hyun-Gug Jung & Qichao Zhang & Min Woo Kim & Yuna Choi & Ahmet Burak Caglayan & Dongsheng Cai, 2024. "Targeting the hypothalamus for modeling age-related DNA methylation and developing OXT-GnRH combinational therapy against Alzheimer’s disease-like pathologies in male mouse model," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    10. Sven Akkerman & Jos Prickaerts & Ann K Bruder & Kevin H M Wolfs & Jochen De Vry & Tim Vanmierlo & Arjan Blokland, 2014. "PDE5 Inhibition Improves Object Memory in Standard Housed Rats but Not in Rats Housed in an Enriched Environment: Implications for Memory Models?," PLOS ONE, Public Library of Science, vol. 9(11), pages 1-11, November.
    11. Alexandros A. Lavdas & Nikos A. Salingaros, 2021. "Can Suboptimal Visual Environments Negatively Affect Children’s Cognitive Development?," Challenges, MDPI, vol. 12(2), pages 1-12, November.
    12. Alexander Kotrschal & Barbara Taborsky, 2010. "Environmental Change Enhances Cognitive Abilities in Fish," PLOS Biology, Public Library of Science, vol. 8(4), pages 1-7, April.
    13. Ruy Gómez-Ocádiz & Massimiliano Trippa & Chun-Lei Zhang & Lorenzo Posani & Simona Cocco & Rémi Monasson & Christoph Schmidt-Hieber, 2022. "A synaptic signal for novelty processing in the hippocampus," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Obregon, Carlos, 2023. "Institutionalism and Liberalism," MPRA Paper 122455, University Library of Munich, Germany.
    15. M. Agustina Frechou & Sunaina S. Martin & Kelsey D. McDermott & Evan A. Huaman & Şölen Gökhan & Wolfgang A. Tomé & Ruben Coen-Cagli & J. Tiago Gonçalves, 2024. "Adult neurogenesis improves spatial information encoding in the mouse hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    16. James O Groves & Isla Leslie & Guo-Jen Huang & Stephen B McHugh & Amy Taylor & Richard Mott & Marcus Munafò & David M Bannerman & Jonathan Flint, 2013. "Ablating Adult Neurogenesis in the Rat Has No Effect on Spatial Processing: Evidence from a Novel Pharmacogenetic Model," PLOS Genetics, Public Library of Science, vol. 9(9), pages 1-16, September.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pone00:0017689. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.