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      The Phylotypic Brain of Vertebrates, from Neural Tube Closure to Brain Diversification

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          Abstract

          Background: The phylotypic or intermediate stages are thought to be the most evolutionary conserved stages throughout embryonic development. The contrast with divergent early and later stages derived from the concept of the evo-devo hourglass model. Nonetheless, this developmental constraint has been studied as a whole embryo process, not at organ level. In this review, we explore brain development to assess the existence of an equivalent brain developmental hourglass. In the specific case of vertebrates, we propose to split the brain developmental stages into: (1) Early: Neurulation, when the neural tube arises after gastrulation. (2) Intermediate: Brain patterning and segmentation, when the neuromere identities are established. (3) Late: Neurogenesis and maturation, the stages when the neurons acquire their functionality. Moreover, we extend this analysis to other chordates brain development to unravel the evolutionary origin of this evo-devo constraint. Summary: Based on the existing literature, we hypothesise that a major conservation of the phylotypic brain might be due to the pleiotropy of the inductive regulatory networks, which are predominantly expressed at this stage. In turn, earlier stages such as neurulation are rather mechanical processes, whose regulatory networks seem to adapt to environment or maternal geometries. The later stages are also controlled by inductive regulatory networks, but their effector genes are mostly tissue-specific and functional, allowing diverse developmental programs to generate current brain diversity. Nonetheless, all stages of the hourglass are highly interconnected: divergent neurulation must have a vertebrate shared end product to reproduce the vertebrate phylotypic brain, and the boundaries and transcription factor code established during the highly conserved patterning will set the bauplan for the specialised and diversified adult brain. Key Messages: The vertebrate brain is conserved at phylotypic stages, but the highly conserved mechanisms that occur during these brain mid-development stages (Inducing Regulatory Networks) are also present during other stages. Oppositely, other processes as cell interactions and functional neuronal genes are more diverse and majoritarian in early and late stages of development, respectively. These phenomena create an hourglass of transcriptomic diversity during embryonic development and evolution, with a really conserved bottleneck that set the bauplan for the adult brain around the phylotypic stage.

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          Shared and distinct transcriptomic cell types across neocortical areas

          The neocortex contains a multitude of cell types that are segregated into layers and functionally distinct areas. To investigate the diversity of cell types across the mouse neocortex, here we analysed 23,822 cells from two areas at distant poles of the mouse neocortex: the primary visual cortex and the anterior lateral motor cortex. We define 133 transcriptomic cell types by deep, single-cell RNA sequencing. Nearly all types of GABA (γ-aminobutyric acid)-containing neurons are shared across both areas, whereas most types of glutamatergic neurons were found in one of the two areas. By combining single-cell RNA sequencing and retrograde labelling, we match transcriptomic types of glutamatergic neurons to their long-range projection specificity. Our study establishes a combined transcriptomic and projectional taxonomy of cortical cell types from functionally distinct areas of the adult mouse cortex.
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            Molecular Diversity of Midbrain Development in Mouse, Human, and Stem Cells

            Summary Understanding human embryonic ventral midbrain is of major interest for Parkinson’s disease. However, the cell types, their gene expression dynamics, and their relationship to commonly used rodent models remain to be defined. We performed single-cell RNA sequencing to examine ventral midbrain development in human and mouse. We found 25 molecularly defined human cell types, including five subtypes of radial glia-like cells and four progenitors. In the mouse, two mature fetal dopaminergic neuron subtypes diversified into five adult classes during postnatal development. Cell types and gene expression were generally conserved across species, but with clear differences in cell proliferation, developmental timing, and dopaminergic neuron development. Additionally, we developed a method to quantitatively assess the fidelity of dopaminergic neurons derived from human pluripotent stem cells, at a single-cell level. Thus, our study provides insight into the molecular programs controlling human midbrain development and provides a foundation for the development of cell replacement therapies.
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              Gene expression across mammalian organ development

              The evolution of gene expression in mammalian organ development remains largely uncharacterized. Here we report the transcriptomes of seven organs (cerebrum, cerebellum, heart, kidney, liver, ovary and testis) across developmental time points from early organogenesis to adulthood for human, macaque, mouse, rat, rabbit, opossum and chicken. Comparisons of gene expression patterns identified developmental stage correspondences across species, and differences in the timing of key events during the development of the gonads. We found that the breadth of gene expression and the extent of purifying selection gradually decrease during development, whereas the amount of positive selection and expression of new genes increase. We identified differences in the temporal trajectories of expression of individual genes across species, with brain tissues showing the smallest percentage of trajectory changes, and the liver and testis showing the largest. Our work provides a resource of developmental transcriptomes of seven organs across seven species, and comparative analyses that characterize the development and evolution of mammalian organs.
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                Author and article information

                Journal
                BBE
                Brain Behav Evol
                10.1159/issn.0006-8977
                Brain, Behavior and Evolution
                Brain Behav Evol
                S. Karger AG
                0006-8977
                1421-9743
                2024
                April 2024
                09 February 2024
                : 99
                : 1
                : 45-68
                Affiliations
                [a ]Achucarro Basque Center for Neuroscience, Scientific Park of the University of the Basque Country (UPV/EHU), Leioa, Spain
                [b ]Department of Neuroscience, Faculty of Medicine and Odontology, UPV/EHU, Leioa, Spain
                [c ]IKERBASQUE Foundation, Bilbao, Spain
                Author notes
                *Fernando García-Moreno, fernando.garcia-moreno@achucarro.org
                Article
                537748 Brain Behav Evol 2024;99:45–67
                10.1159/000537748
                38342091
                64abf770-fa66-4853-81b9-5090e228b1ea
                © 2024 S. Karger AG, Basel
                History
                : 30 November 2023
                : 04 February 2024
                Page count
                Figures: 5, Pages: 23
                Funding
                R. S. G. holds a predoctoral fellowship from the Tatiana Perez de Guzman el Bueno Foundation (Spain). F. G. M. is supported by IKERBASQUE and holds PID2021-125156NB-I00 grant from the Spanish Ministry MICNN and PIBA_2022_1_0027 grant from the Basque Government.
                Categories
                Review

                Medicine
                Development,Constraints,Neurodevelopment,Hourglass model,Evolution
                Medicine
                Development, Constraints, Neurodevelopment, Hourglass model, Evolution

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