IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41652-5.html
   My bibliography  Save this article

Non-uniform temporal scaling of developmental processes in the mammalian cortex

Author

Listed:
  • Annalisa Paolino

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute)

  • Elizabeth H. Haines

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute)

  • Evan J. Bailey

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute)

  • Dylan A. Black

    (The University of Queensland, Queensland Brain Institute)

  • Ching Moey

    (The University of Queensland, Queensland Brain Institute)

  • Fernando García-Moreno

    (Scientific Park of the University of the Basque Country (UPV/EHU)
    IKERBASQUE Foundation, María Díaz de Haro 3)

  • Linda J. Richards

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute
    Department of Neuroscience)

  • Rodrigo Suárez

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute)

  • Laura R. Fenlon

    (The University of Queensland, School of Biomedical Sciences
    The University of Queensland, Queensland Brain Institute)

Abstract

The time that it takes the brain to develop is highly variable across animals. Although staging systems equate major developmental milestones between mammalian species, it remains unclear how distinct processes of cortical development scale within these timeframes. Here, we compare the timing of cortical development in two mammals of similar size but different developmental pace: eutherian mice and marsupial fat-tailed dunnarts. Our results reveal that the temporal relationship between cell birth and laminar specification aligns to equivalent stages between these species, but that migration and axon extension do not scale uniformly according to the developmental stages, and are relatively more advanced in dunnarts. We identify a lack of basal intermediate progenitor cells in dunnarts that likely contributes in part to this timing difference. These findings demonstrate temporal limitations and differential plasticity of cortical developmental processes between similarly sized Therians and provide insight into subtle temporal changes that may have contributed to the early diversification of the mammalian brain.

Suggested Citation

  • Annalisa Paolino & Elizabeth H. Haines & Evan J. Bailey & Dylan A. Black & Ching Moey & Fernando García-Moreno & Linda J. Richards & Rodrigo Suárez & Laura R. Fenlon, 2023. "Non-uniform temporal scaling of developmental processes in the mammalian cortex," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41652-5
    DOI: 10.1038/s41467-023-41652-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41652-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-41652-5?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. J. P. Mortola & P. B. Frappell & P. A. Woolley, 1999. "Breathing through skin in a newborn mammal," Nature, Nature, vol. 397(6721), pages 660-660, February.
    2. Esther Klingler & Ugo Tomasello & Julien Prados & Justus M. Kebschull & Alessandro Contestabile & Gregorio L. Galiñanes & Sabine Fièvre & Antonio Santinha & Randall Platt & Daniel Huber & Alexandre Da, 2021. "Temporal controls over inter-areal cortical projection neuron fate diversity," Nature, Nature, vol. 599(7885), pages 453-457, November.
    3. David V. Hansen & Jan H. Lui & Philip R. L. Parker & Arnold R. Kriegstein, 2010. "Neurogenic radial glia in the outer subventricular zone of human neocortex," Nature, Nature, vol. 464(7288), pages 554-561, March.
    4. Tadashi Nomura & Hitoshi Gotoh & Katsuhiko Ono, 2013. "Changes in the regulation of cortical neurogenesis contribute to encephalization during amniote brain evolution," Nature Communications, Nature, vol. 4(1), pages 1-12, October.
    5. Burchett, Woodrow W. & Ellis, Amanda R. & Harrar, Solomon W. & Bathke, Arne C., 2017. "Nonparametric Inference for Multivariate Data: The R Package npmv," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 76(i04).
    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. Gunawardana, Asanka & Konietschke, Frank, 2019. "Nonparametric multiple contrast tests for general multivariate factorial designs," Journal of Multivariate Analysis, Elsevier, vol. 173(C), pages 165-180.
    2. Justin W. Bonny & Lisa M. Castaneda, 2022. "To Triumph or to Socialize? The Role of Gaming Motivations in Multiplayer Online Battle Arena Gameplay Preferences," Simulation & Gaming, , vol. 53(2), pages 157-174, April.
    3. Christina Kyrousi & Adam C. O’Neill & Agnieska Brazovskaja & Zhisong He & Pavel Kielkowski & Laure Coquand & Rossella Giaimo & Pierpaolo D’ Andrea & Alexander Belka & Andrea Forero Echeverry & Davide , 2021. "Extracellular LGALS3BP regulates neural progenitor position and relates to human cortical complexity," Nature Communications, Nature, vol. 12(1), pages 1-22, December.
    4. Panda, Deepak Kumar & Das, Saptarshi, 2021. "Economic operational analytics for energy storage placement at different grid locations and contingency scenarios with stochastic wind profiles," Renewable and Sustainable Energy Reviews, Elsevier, vol. 137(C).
    5. Aguilera, Ana M. & Acal, Christian & Aguilera-Morillo, M. Carmen & Jiménez-Molinos, Francisco & Roldán, Juan B., 2021. "Homogeneity problem for basis expansion of functional data with applications to resistive memories," Mathematics and Computers in Simulation (MATCOM), Elsevier, vol. 186(C), pages 41-51.
    6. Harrar, Solomon W. & Kong, Xiaoli, 2022. "Recent developments in high-dimensional inference for multivariate data: Parametric, semiparametric and nonparametric approaches," Journal of Multivariate Analysis, Elsevier, vol. 188(C).
    7. Dennis Dobler & Sarah Friedrich & Markus Pauly, 2020. "Nonparametric MANOVA in meaningful effects," Annals of the Institute of Statistical Mathematics, Springer;The Institute of Statistical Mathematics, vol. 72(4), pages 997-1022, August.
    8. G. Ball & S. Oldham & V. Kyriakopoulou & L. Z. J. Williams & V. Karolis & A. Price & J. Hutter & M. L. Seal & A. Alexander-Bloch & J. V. Hajnal & A. D. Edwards & E. C. Robinson & J. Seidlitz, 2024. "Molecular signatures of cortical expansion in the human foetal brain," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Norman L. Lehman & Nathalie Spassky & Müge Sak & Amy Webb & Cory T. Zumbar & Aisulu Usubalieva & Khaled J. Alkhateeb & Joseph P. McElroy & Kirsteen H. Maclean & Paolo Fadda & Tom Liu & Vineela Gangala, 2022. "Astroblastomas exhibit radial glia stem cell lineages and differential expression of imprinted and X-inactivation escape genes," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    10. Soraia Barão & Yijun Xu & José P. Llongueras & Rachel Vistein & Loyal Goff & Kristina J. Nielsen & Byoung-Il Bae & Richard S. Smith & Christopher A. Walsh & Genevieve Stein-O’Brien & Ulrich Müller, 2024. "Conserved transcriptional regulation by BRN1 and BRN2 in neocortical progenitors drives mammalian neural specification and neocortical expansion," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    11. Patrick B. Langthaler & Riccardo Ceccato & Luigi Salmaso & Rosa Arboretti & Arne C. Bathke, 2023. "Permutation testing for thick data when the number of variables is much greater than the sample size: recent developments and some recommendations," Computational Statistics, Springer, vol. 38(1), pages 101-132, March.
    12. Li Yuan & Xiaoyin Chen & Huiqing Zhan & Gilbert L. Henry & Anthony M. Zador, 2024. "Massive multiplexing of spatially resolved single neuron projections with axonal BARseq," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Delfina M. Romero & Karine Poirier & Richard Belvindrah & Imane Moutkine & Anne Houllier & Anne-Gaëlle LeMoing & Florence Petit & Anne Boland & Stephan C. Collins & Mariano Soiza-Reilly & Binnaz Yalci, 2022. "Novel role of the synaptic scaffold protein Dlgap4 in ventricular surface integrity and neuronal migration during cortical development," Nature Communications, Nature, vol. 13(1), pages 1-19, December.

    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:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41652-5. 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: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    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.