Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes

Aboitiz, Francisco; Montiel, Juan

doi:10.1111/ede.12308

Cited by 8 publications

(12 citation statements)

References 77 publications

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“…Our study was motivated by the structural changes occurring in radial glial cells during growth and was not intended to contribute to the debate on the origin and homology of the different pallial areas across different vertebrate groups (Aboitiz & Montiel, 2019; Briscoe & Ragsdale, 2019). We can conclude, however, that radial glial cells can adapt to morphological changes during growth in the adult fish brain and contribute themselves to these growth processes.…”

Section: Discussionmentioning

confidence: 99%

Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni

et al. 2021

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In the brain of teleost fish, radial glial cells are the main astroglial cell type. To understand how radial glia structures are adapting to continuous growth of the brain, we studied the astroglial cells in the telencephalon of the cichlid fish Astatotilapia burtoni in small fry to large specimens. These animals grow to a standard length of 10–12 cm in this fish species, corresponding to a more than 100‐fold increase in brain volume. Focusing on the telencephalon where glial cells are arranged radially in the everted (dorsal) pallium, immunocytochemistry for glial markers revealed an aberrant pattern of radial glial fibers in the central division of the dorsal pallium (DC, i.e., DC4 and DC5). The main glial processes curved around these nuclei, especially in the posterior part of the telencephalon. This was verified in tissue‐cleared brains stained for glial markers. We further analyzed the growth of radial glia by immunocytochemically applied stem cell (proliferating cell nuclear antigen [PCNA], Sox2) and differentiation marker (doublecortin) and found that these markers were expressed at the ventricular surface consistent with a stacking growth pattern. In addition, we detected doublecortin and Sox2 positive cells in deeper nuclei of DC areas. Our data suggest that radial glial cells give rise to migrating cells providing new neurons and glia to deeper pallial regions. This results in expansion of the central pallial areas and displacement of existing radial glial. In summary, we show that radial glial cells can adapt to morphological growth processes in the adult fish brain and contribute to this growth.

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Section: Discussionmentioning

confidence: 99%

Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni

et al. 2021

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“…Following morphogenesis of the ventricle, tangential growth of the ventricular zone, driven by telencephalic neuronal differentiation, may be one of the driving forces to expand the pallial ventricular surface ( Aboitiz and Montiel, 2019 ; present results). By 5dpf, the zebrafish telencephalon shows everted morphology ( Folgueira et al, 2012 ; present results), but there is a subsequent expansion of the telencephalic ventricular zone, which grows in lockstep with general telencephalic lobe growth.…”

Section: Discussionmentioning

confidence: 77%

A Structural Atlas of the Developing Zebrafish Telencephalon Based on Spatially-Restricted Transgene Expression

et al. 2022

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Zebrafish telencephalon acquires an everted morphology by a two-step process that occurs from 1 to 5 days post-fertilization (dpf). Little is known about how this process affects the positioning of discrete telencephalic cell populations, hindering our understanding of how eversion impacts telencephalic structural organization. In this study, we characterize the neurochemistry, cycle state and morphology of an EGFP positive (+) cell population in the telencephalon of Et(gata2:EGFP)bi105 transgenic fish during eversion and up to 20dpf. We map the transgene insertion to the early-growth-response-gene-3 (egr3) locus and show that EGFP expression recapitulates endogenous egr3 expression throughout much of the pallial telencephalon. Using the gata2:EGFPbi105 transgene, in combination with other well-characterized transgenes and structural markers, we track the development of various cell populations in the zebrafish telencephalon as it undergoes the morphological changes underlying eversion. These datasets were registered to reference brains to form an atlas of telencephalic development at key stages of the eversion process (1dpf, 2dpf, and 5dpf) and compared to expression in adulthood. Finally, we registered gata2:EGFPbi105 expression to the Zebrafish Brain Browser 6dpf reference brain (ZBB, see Marquart et al., 2015, 2017; Tabor et al., 2019), to allow comparison of this expression pattern with anatomical data already in ZBB.

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“…The literature describing the progressive organization of vertebrate brains over embryonic and evolutionary time [42, 2] has emphasized local organizational processes and their dependence on a local landscape of molecular signals [37, 1]. However, that focus neglects the more global question of how the guidance landscapes are themselves established.…”

Section: Discussionmentioning

confidence: 99%

“…By selecting a particular familial template, the growth cone tunes into the corresponding expression gradient and filters out the others. If the tuned gradient is in range, the growth cone follows it to arrive at one of that gradient’s peaks (case indicated by [1]). If the tuned gradient is not in range [3], the axonal branch of that growth cones fails.…”

Section: Rationalementioning

confidence: 99%

Constructive Connectomics: how neuronal axons get from here to there using gene-expression maps derived from their family trees

Kerstjens

Michel

Douglas

2022

Preprint

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During brain development, billions of axons must navigate over multiple spatial scales to reach specific neuronal targets, and so build the processing circuits that generate the intelligent behavior of animals. However, the limited information capacity of the zygotic genome puts a strong constraint on how, and which, axonal routes can be encoded. We propose and validate a mechanism of development that can provide an efficient encoding of this global wiring task. The key principle, confirmed through simulation, is that basic constraints on mitoses of neural stem cells—that mitotic daughters have similar gene expression to their parent and do not stray far from one another—induce a global hierarchical map of nested regions, each marked by the expression profile of its common progenitor population. Thus, a traversal of the lineal hierarchy generates a systematic sequence of expression profiles that traces a staged route, which growth cones can follow to their remote targets. We have analyzed gene expression data of developing and adult mouse brains published by the Allen Institute for Brain Science, and found them consistent with our simulations: gene expression indeed partitions the brain into a global spatial hierarchy of nested contiguous regions that is stable at least from embryonic day 11.5 to postnatal day 56. We use this experimental data to demonstrate that our axonal guidance algorithm is able to robustly extend arbors over long distances to specific targets, and that these connections result in a qualitatively plausible connectome. We conclude that, paradoxically, cell division may be the key to uniting the neurons of the brain.

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Morphological evolution of the vertebrate forebrain: From mechanical to cellular processes

Cited by 8 publications

References 77 publications

Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni

Organization of radial glia reveals growth pattern in the telencephalon of a percomorph fish Astatotilapia burtoni

A Structural Atlas of the Developing Zebrafish Telencephalon Based on Spatially-Restricted Transgene Expression

Constructive Connectomics: how neuronal axons get from here to there using gene-expression maps derived from their family trees

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