Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development

During development of the vertebrate retina, mitotic activity is defined as apical when is located at the external surface of the neuroepithelium or as non-apical when is found in more internal regions. Apical mitoses give rise to all retinal cell types. Non-apical mitoses are linked to committed ho...

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Main Authors: Guadalupe Álvarez-Hernán, José Antonio de Mera-Rodríguez, Ismael Hernández-Núñez, Abel Acedo, Alfonso Marzal, Yolanda Gañán, Gervasio Martín-Partido, Joaquín Rodríguez-León, Javier Francisco-Morcillo
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Neuroscience
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Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2022.853544/full
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author Guadalupe Álvarez-Hernán
José Antonio de Mera-Rodríguez
Ismael Hernández-Núñez
Abel Acedo
Alfonso Marzal
Yolanda Gañán
Gervasio Martín-Partido
Joaquín Rodríguez-León
Javier Francisco-Morcillo
author_facet Guadalupe Álvarez-Hernán
José Antonio de Mera-Rodríguez
Ismael Hernández-Núñez
Abel Acedo
Alfonso Marzal
Yolanda Gañán
Gervasio Martín-Partido
Joaquín Rodríguez-León
Javier Francisco-Morcillo
author_sort Guadalupe Álvarez-Hernán
collection DOAJ
description During development of the vertebrate retina, mitotic activity is defined as apical when is located at the external surface of the neuroepithelium or as non-apical when is found in more internal regions. Apical mitoses give rise to all retinal cell types. Non-apical mitoses are linked to committed horizontal cell precursors that subsequently migrate vitreo-sclerally, reaching their final position in the outer surface of the inner nuclear layer, where they differentiate. Previous studies have suggested differences in the timing of retinal maturation between altricial and precocial bird species. In the present study we analyze qualitatively and quantitatively the mitotic activity in the developing retina of an altricial (zebra finch, Taeniopygia guttata) and a precocial (Japanese quail, Coturnix coturnix) bird species. We found that pHisH3-immunoreactive apical and non-apical mitoses were abundant in the T. guttata retina at the hatching stage. In contrast, pHisH3 immunoreactivity almost disappeared from the quail retina at the embryonic day 10 (E10). Furthermore, we also found that the onset of the appearance of non-apical mitoses occurred at later stages in the altricial bird species than in the precocial one. The disappearance of apical mitoses and the spatiotemporal distribution of non-apical mitoses followed central to peripheral and dorsal to ventral gradients, similar to gradients of cell differentiation described in the retina of birds. Therefore, these results suggest that retinal neurogenesis is active at the hatching stage in T. guttata, and that horizontal cell differentiation is delayed in the altricial bird species compared to the precocial one. Together, this study reveals important insights into the timing differences that regulate bird retinal maturation and provides a better understanding of the evolution of avian altriciality and precociality.
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spelling doaj.art-a2e01e36df1f40f4810c3e14eac2bf6e2022-12-22T02:53:55ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-05-011610.3389/fnins.2022.853544853544Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian DevelopmentGuadalupe Álvarez-Hernán0José Antonio de Mera-Rodríguez1Ismael Hernández-Núñez2Abel Acedo3Alfonso Marzal4Yolanda Gañán5Gervasio Martín-Partido6Joaquín Rodríguez-León7Javier Francisco-Morcillo8Departamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Medicina y Ciencias de la Salud, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Medicina y Ciencias de la Salud, Universidad de Extremadura, Badajoz, SpainDepartamento de Anatomía, Biología Celular y Zoología, Facultad de Ciencias, Universidad de Extremadura, Badajoz, SpainDuring development of the vertebrate retina, mitotic activity is defined as apical when is located at the external surface of the neuroepithelium or as non-apical when is found in more internal regions. Apical mitoses give rise to all retinal cell types. Non-apical mitoses are linked to committed horizontal cell precursors that subsequently migrate vitreo-sclerally, reaching their final position in the outer surface of the inner nuclear layer, where they differentiate. Previous studies have suggested differences in the timing of retinal maturation between altricial and precocial bird species. In the present study we analyze qualitatively and quantitatively the mitotic activity in the developing retina of an altricial (zebra finch, Taeniopygia guttata) and a precocial (Japanese quail, Coturnix coturnix) bird species. We found that pHisH3-immunoreactive apical and non-apical mitoses were abundant in the T. guttata retina at the hatching stage. In contrast, pHisH3 immunoreactivity almost disappeared from the quail retina at the embryonic day 10 (E10). Furthermore, we also found that the onset of the appearance of non-apical mitoses occurred at later stages in the altricial bird species than in the precocial one. The disappearance of apical mitoses and the spatiotemporal distribution of non-apical mitoses followed central to peripheral and dorsal to ventral gradients, similar to gradients of cell differentiation described in the retina of birds. Therefore, these results suggest that retinal neurogenesis is active at the hatching stage in T. guttata, and that horizontal cell differentiation is delayed in the altricial bird species compared to the precocial one. Together, this study reveals important insights into the timing differences that regulate bird retinal maturation and provides a better understanding of the evolution of avian altriciality and precociality.https://www.frontiersin.org/articles/10.3389/fnins.2022.853544/fullaltricialapical mitosesbird retinaembryohorizontal cellsimmunohistochemistry
spellingShingle Guadalupe Álvarez-Hernán
José Antonio de Mera-Rodríguez
Ismael Hernández-Núñez
Abel Acedo
Alfonso Marzal
Yolanda Gañán
Gervasio Martín-Partido
Joaquín Rodríguez-León
Javier Francisco-Morcillo
Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
Frontiers in Neuroscience
altricial
apical mitoses
bird retina
embryo
horizontal cells
immunohistochemistry
title Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
title_full Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
title_fullStr Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
title_full_unstemmed Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
title_short Timing and Distribution of Mitotic Activity in the Retina During Precocial and Altricial Modes of Avian Development
title_sort timing and distribution of mitotic activity in the retina during precocial and altricial modes of avian development
topic altricial
apical mitoses
bird retina
embryo
horizontal cells
immunohistochemistry
url https://www.frontiersin.org/articles/10.3389/fnins.2022.853544/full
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