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Neocortex neurogenesis and maturation in the African greater cane rat

BACKGROUND: Neocortex development has been extensively studied in altricial rodents such as mouse and rat. Identification of alternative animal models along the “altricial-precocial” spectrum in order to better model and understand neocortex development is warranted. The Greater cane rat (GCR, Thyro...

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Autores principales: Mustapha, Oluwaseun, Grochow, Thomas, Olopade, James, Fietz, Simone A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10571270/
https://www.ncbi.nlm.nih.gov/pubmed/37833718
http://dx.doi.org/10.1186/s13064-023-00175-x
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author Mustapha, Oluwaseun
Grochow, Thomas
Olopade, James
Fietz, Simone A.
author_facet Mustapha, Oluwaseun
Grochow, Thomas
Olopade, James
Fietz, Simone A.
author_sort Mustapha, Oluwaseun
collection PubMed
description BACKGROUND: Neocortex development has been extensively studied in altricial rodents such as mouse and rat. Identification of alternative animal models along the “altricial-precocial” spectrum in order to better model and understand neocortex development is warranted. The Greater cane rat (GCR, Thyronomys swinderianus) is an indigenous precocial African rodent. Although basic aspects of brain development in the GCR have been documented, detailed information on neocortex development including the occurrence and abundance of the distinct types of neural progenitor cells (NPCs) in the GCR are lacking. METHODS: GCR embryos and fetuses were obtained from timed pregnant dams between gestation days 50–140 and their neocortex was analyzed by immunofluorescence staining using characteristic marker proteins for NPCs, neurons and glia cells. Data were compared with existing data on closely related precocial and altricial species, i.e. guinea pig and dwarf rabbit. RESULTS: The primary sequence of neuro- and gliogenesis, and neuronal maturation is preserved in the prenatal GCR neocortex. We show that the GCR exhibits a relatively long period of cortical neurogenesis of 70 days. The subventricular zone becomes the major NPC pool during mid-end stages of neurogenesis with Pax6 + NPCs constituting the major basal progenitor subtype in the GCR neocortex. Whereas dendrite formation in the GCR cortical plate appears to initiate immediately after the onset of neurogenesis, major aspects of axon formation and maturation, and astrogenesis do not begin until mid-neurogenesis. Similar to the guinea pig, the GCR neocortex exhibits a high maturation status, containing neurons with well-developed dendrites and myelinated axons and astrocytes at birth, thus providing further evidence for the notion that a great proportion of neocortex growth and maturation in precocial mammals occurs before birth. CONCLUSIONS: Together, this work has deepened our understanding of neocortex development of the GCR, of the timing and the cellular differences that regulate brain growth and development within the altricial–precocial spectrum and its suitability as a research model for neurodevelopmental studies. The timelines of brain development provided by this study may serve as empirical reference data and foundation in future studies in order to model and better understand neurodevelopment and associated alterations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13064-023-00175-x.
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spelling pubmed-105712702023-10-14 Neocortex neurogenesis and maturation in the African greater cane rat Mustapha, Oluwaseun Grochow, Thomas Olopade, James Fietz, Simone A. Neural Dev Research BACKGROUND: Neocortex development has been extensively studied in altricial rodents such as mouse and rat. Identification of alternative animal models along the “altricial-precocial” spectrum in order to better model and understand neocortex development is warranted. The Greater cane rat (GCR, Thyronomys swinderianus) is an indigenous precocial African rodent. Although basic aspects of brain development in the GCR have been documented, detailed information on neocortex development including the occurrence and abundance of the distinct types of neural progenitor cells (NPCs) in the GCR are lacking. METHODS: GCR embryos and fetuses were obtained from timed pregnant dams between gestation days 50–140 and their neocortex was analyzed by immunofluorescence staining using characteristic marker proteins for NPCs, neurons and glia cells. Data were compared with existing data on closely related precocial and altricial species, i.e. guinea pig and dwarf rabbit. RESULTS: The primary sequence of neuro- and gliogenesis, and neuronal maturation is preserved in the prenatal GCR neocortex. We show that the GCR exhibits a relatively long period of cortical neurogenesis of 70 days. The subventricular zone becomes the major NPC pool during mid-end stages of neurogenesis with Pax6 + NPCs constituting the major basal progenitor subtype in the GCR neocortex. Whereas dendrite formation in the GCR cortical plate appears to initiate immediately after the onset of neurogenesis, major aspects of axon formation and maturation, and astrogenesis do not begin until mid-neurogenesis. Similar to the guinea pig, the GCR neocortex exhibits a high maturation status, containing neurons with well-developed dendrites and myelinated axons and astrocytes at birth, thus providing further evidence for the notion that a great proportion of neocortex growth and maturation in precocial mammals occurs before birth. CONCLUSIONS: Together, this work has deepened our understanding of neocortex development of the GCR, of the timing and the cellular differences that regulate brain growth and development within the altricial–precocial spectrum and its suitability as a research model for neurodevelopmental studies. The timelines of brain development provided by this study may serve as empirical reference data and foundation in future studies in order to model and better understand neurodevelopment and associated alterations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13064-023-00175-x. BioMed Central 2023-10-13 /pmc/articles/PMC10571270/ /pubmed/37833718 http://dx.doi.org/10.1186/s13064-023-00175-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Mustapha, Oluwaseun
Grochow, Thomas
Olopade, James
Fietz, Simone A.
Neocortex neurogenesis and maturation in the African greater cane rat
title Neocortex neurogenesis and maturation in the African greater cane rat
title_full Neocortex neurogenesis and maturation in the African greater cane rat
title_fullStr Neocortex neurogenesis and maturation in the African greater cane rat
title_full_unstemmed Neocortex neurogenesis and maturation in the African greater cane rat
title_short Neocortex neurogenesis and maturation in the African greater cane rat
title_sort neocortex neurogenesis and maturation in the african greater cane rat
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10571270/
https://www.ncbi.nlm.nih.gov/pubmed/37833718
http://dx.doi.org/10.1186/s13064-023-00175-x
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