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Science (New York, N.Y.) Dec 2017Systematic analyses of spatiotemporal gene expression trajectories during organogenesis have been challenging because diverse cell types at different stages of...
Systematic analyses of spatiotemporal gene expression trajectories during organogenesis have been challenging because diverse cell types at different stages of maturation and differentiation coexist in the emerging tissues. We identified discrete cell types as well as temporally and spatially restricted trajectories of radial glia maturation and neurogenesis in developing human telencephalon. These lineage-specific trajectories reveal the expression of neurogenic transcription factors in early radial glia and enriched activation of mammalian target of rapamycin signaling in outer radial glia. Across cortical areas, modest transcriptional differences among radial glia cascade into robust typological distinctions among maturing neurons. Together, our results support a mixed model of topographical, typological, and temporal hierarchies governing cell-type diversity in the developing human telencephalon, including distinct excitatory lineages emerging in rostral and caudal cerebral cortex.
Topics: Cerebral Cortex; Gene Expression Regulation, Developmental; Humans; Neurogenesis; Neuroglia; Neurons; Telencephalon
PubMed: 29217575
DOI: 10.1126/science.aap8809 -
Science (New York, N.Y.) Oct 2023During early telencephalic development, intricate processes of regional patterning and neural stem cell (NSC) fate specification take place. However, our understanding...
During early telencephalic development, intricate processes of regional patterning and neural stem cell (NSC) fate specification take place. However, our understanding of these processes in primates, including both conserved and species-specific features, remains limited. Here, we profiled 761,529 single-cell transcriptomes from multiple regions of the prenatal macaque telencephalon. We deciphered the molecular programs of the early organizing centers and their cross-talk with NSCs, revealing primate-biased galanin-like peptide () signaling in the anteroventral telencephalon. Regional transcriptomic variations were observed along the frontotemporal axis during early stages of neocortical NSC progression and in neurons and astrocytes. Additionally, we found that genes associated with neuropsychiatric disorders and brain cancer risk might play critical roles in the early telencephalic organizers and during NSC progression.
Topics: Animals; Female; Pregnancy; Macaca; Neural Stem Cells; Neurons; Telencephalon; Neurogenesis; Galanin-Like Peptide; Gene Expression Regulation, Developmental; Mental Disorders; Nervous System Diseases; Brain Neoplasms
PubMed: 37824652
DOI: 10.1126/science.adf3786 -
AJNR. American Journal of Neuroradiology Feb 2018
Topics: Cerebrum; Humans; Neoplasms; Telencephalon
PubMed: 29051211
DOI: 10.3174/ajnr.A5447 -
Brain, Behavior and Evolution 2022The pallium is the largest part of the telencephalon in amniotes, and comparison of its subdivisions across species has been extremely difficult and controversial due to... (Review)
Review
The pallium is the largest part of the telencephalon in amniotes, and comparison of its subdivisions across species has been extremely difficult and controversial due to its high divergence. Comparative embryonic genoarchitecture studies have greatly contributed to propose models of pallial fundamental divisions, which can be compared across species and be used to extract general organizing principles as well as to ask more focused and insightful research questions. The use of these models is crucial to discern between conservation, convergence or divergence in the neural populations and networks found in the pallium. Here we provide a critical review of the models proposed using this approach, including tetrapartite, hexapartite and double-ring models, and compare them to other models. While recognizing the power of these models for understanding brain architecture, development and evolution, we also highlight limitations and comment on aspects that require attention for improvement. We also discuss on the use of transcriptomic data for understanding pallial evolution and advise for better contextualization of these data by discerning between gene regulatory networks involved in the generation of specific units and cell populations versus genes expressed later, many of which are activity dependent and their expression is more likely subjected to convergent evolution.
Topics: Animals; Brain; Cerebral Cortex; Telencephalon
PubMed: 34657034
DOI: 10.1159/000519260 -
Current Biology : CB Jul 2019The dramatic evolutionary expansion of the neocortex, together with a proliferation of specialized cortical areas, is believed to underlie the emergence of human... (Review)
Review
The dramatic evolutionary expansion of the neocortex, together with a proliferation of specialized cortical areas, is believed to underlie the emergence of human cognitive abilities. In a broader phylogenetic context, however, neocortex evolution in mammals, including humans, is remarkably conservative, characterized largely by size variations on a shared six-layered neuronal architecture. By contrast, the telencephalon in non-mammalian vertebrates, including reptiles, amphibians, bony and cartilaginous fishes, and cyclostomes, features a great variety of very different tissue structures. Our understanding of the evolutionary relationships of these telencephalic structures, especially those of basally branching vertebrates and invertebrate chordates, remains fragmentary and is impeded by conceptual obstacles. To make sense of highly divergent anatomies requires a hierarchical view of biological organization, one that permits the recognition of homologies at multiple levels beyond neuroanatomical structure. Here we review the origin and diversification of the telencephalon with a focus on key evolutionary innovations shaping the neocortex at multiple levels of organization.
Topics: Animals; Biological Evolution; Chordata; Telencephalon
PubMed: 31287987
DOI: 10.1016/j.cub.2019.05.026 -
Brain, Behavior and Evolution 2010Birds have excellent visual abilities that are comparable or superior to those of primates, but how the bird brain solves complex visual problems is poorly understood.... (Comparative Study)
Comparative Study Review
Birds have excellent visual abilities that are comparable or superior to those of primates, but how the bird brain solves complex visual problems is poorly understood. More specifically, we lack knowledge about how such superb abilities are used in nature and how the brain, especially the telencephalon, is organized to process visual information. Here we review the results of several studies that examine the organization of the avian telencephalon and the relevance of visual abilities to avian social and reproductive behavior. Video playback and photographic stimuli show that birds can detect and evaluate subtle differences in local facial features of potential mates in a fashion similar to that of primates. These techniques have also revealed that birds do not attend well to global configural changes in the face, suggesting a fundamental difference between birds and primates in face perception. The telencephalon plays a major role in the visual and visuo-cognitive abilities of birds and primates, and anatomical data suggest that these animals may share similar organizational characteristics in the visual telencephalon. As is true in the primate cerebral cortex, different visual features are processed separately in the avian telencephalon where separate channels are organized in the anterior-posterior axis roughly parallel to the major laminae. Furthermore, the efferent projections from the primary visual telencephalon form an extensive column-like continuum involving the dorsolateral pallium and the lateral basal ganglia. Such a column-like organization may exist not only for vision, but for other sensory modalities and even for a continuum that links sensory and limbic areas of the avian brain. Behavioral and neural studies must be integrated in order to understand how birds have developed their amazing visual systems through 150 million years of evolution.
Topics: Animals; Biological Evolution; Birds; Brain Mapping; Columbidae; Coturnix; Courtship; Female; Limbic System; Male; Pattern Recognition, Visual; Primates; Species Specificity; Superior Colliculi; Telencephalon; Visual Pathways; Visual Perception
PubMed: 20733296
DOI: 10.1159/000314283 -
Science (New York, N.Y.) Sep 2022The evolution of advanced cognition in vertebrates is associated with two independent innovations in the forebrain: the six-layered neocortex in mammals and the dorsal...
The evolution of advanced cognition in vertebrates is associated with two independent innovations in the forebrain: the six-layered neocortex in mammals and the dorsal ventricular ridge (DVR) in sauropsids (reptiles and birds). How these innovations arose in vertebrate ancestors remains unclear. To reconstruct forebrain evolution in tetrapods, we built a cell-type atlas of the telencephalon of the salamander . Our molecular, developmental, and connectivity data indicate that parts of the sauropsid DVR trace back to tetrapod ancestors. By contrast, the salamander dorsal pallium is devoid of cellular and molecular characteristics of the mammalian neocortex yet shares similarities with the entorhinal cortex and subiculum. Our findings chart the series of innovations that resulted in the emergence of the mammalian six-layered neocortex and the sauropsid DVR.
Topics: Animals; Atlases as Topic; Biological Evolution; Neocortex; Neurons; Pleurodeles; Telencephalon; Transcriptome
PubMed: 36048957
DOI: 10.1126/science.abp9186 -
International Journal of Molecular... Mar 2021We studied cell proliferation in the postnatal mouse brain between the ages of 2 and 30 months and identified four compartments with different densities of proliferating...
We studied cell proliferation in the postnatal mouse brain between the ages of 2 and 30 months and identified four compartments with different densities of proliferating cells. The first identified compartment corresponds to the postnatal pallial neurogenic (PPN) zone in the telencephalon; the second to the subpallial postnatal neurogenic (SPPN) zone in the telencephalon; the third to the white matter bundles in the telencephalon; and the fourth to all brain parts outside of the other three compartments. We estimated that about 3.4 million new cells, including 0.8 million in the subgranular zone (SGZ) in the hippocampus, are produced in the PPN zone. About 21 million new cells, including 10 million in the subependymal zone (SEZ) in the lateral walls of the lateral ventricle and 2.7 million in the rostral migratory stream (RMS), are produced in the SPPN zone. The third and fourth compartments together produced about 31 million new cells. The analysis of cell proliferation in neurogenic zones shows that postnatal neurogenesis is the direct continuation of developmental neurogenesis in the telencephalon and that adult neurogenesis has characteristics of the late developmental process. As a developmental process, adult neurogenesis supports only compensatory regeneration, which is very inefficient.
Topics: Animals; Brain; Brain Mapping; Cell Movement; Cell Proliferation; Hippocampus; Lateral Ventricles; Male; Mice; Mice, Inbred C57BL; Neural Stem Cells; Neurogenesis; Neurons; Regeneration; Telencephalon
PubMed: 33810614
DOI: 10.3390/ijms22073449 -
Journal of Anatomy Oct 2010In the adult human telencephalon, subcortical (gyral) white matter contains a special population of interstitial neurons considered to be surviving descendants of fetal... (Review)
Review
In the adult human telencephalon, subcortical (gyral) white matter contains a special population of interstitial neurons considered to be surviving descendants of fetal subplate neurons [Kostovic & Rakic (1980) Cytology and the time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. J Neurocytol9, 219]. We designate this population of cells as superficial (gyral) interstitial neurons and describe their morphology and distribution in the postnatal and adult human cerebrum. Human fetal subplate neurons cannot be regarded as interstitial, because the subplate zone is an essential part of the fetal cortex, the major site of synaptogenesis and the 'waiting' compartment for growing cortical afferents, and contains both projection neurons and interneurons with distinct input-output connectivity. However, although the subplate zone is a transient fetal structure, many subplate neurons survive postnatally as superficial (gyral) interstitial neurons. The fetal white matter is represented by the intermediate zone and well-defined deep periventricular tracts of growing axons, such as the corpus callosum, anterior commissure, internal and external capsule, and the fountainhead of the corona radiata. These tracts gradually occupy the territory of transient fetal subventricular and ventricular zones.The human fetal white matter also contains distinct populations of deep fetal interstitial neurons, which, by virtue of their location, morphology, molecular phenotypes and advanced level of dendritic maturation, remain distinct from subplate neurons and neurons in adjacent structures (e.g. basal ganglia, basal forebrain). We describe the morphological, histochemical (nicotinamide-adenine dinucleotide phosphate-diaphorase) and immunocytochemical (neuron-specific nuclear protein, microtubule-associated protein-2, calbindin, calretinin, neuropeptide Y) features of both deep fetal interstitial neurons and deep (periventricular) interstitial neurons in the postnatal and adult deep cerebral white matter (i.e. corpus callosum, anterior commissure, internal and external capsule and the corona radiata/centrum semiovale). Although these deep interstitial neurons are poorly developed or absent in the brains of rodents, they represent a prominent feature of the significantly enlarged white matter of human and non-human primate brains.
Topics: Humans; Immunohistochemistry; Infant, Newborn; Neurons; Phenotype; Telencephalon
PubMed: 20979586
DOI: 10.1111/j.1469-7580.2010.01284.x -
The EMBO Journal Nov 2021The dorsal and ventral human telencephalons contain different neuronal subtypes, including glutamatergic, GABAergic, and cholinergic neurons, and how these neurons are...
The dorsal and ventral human telencephalons contain different neuronal subtypes, including glutamatergic, GABAergic, and cholinergic neurons, and how these neurons are generated during early development is not well understood. Using scRNA-seq and stringent validations, we reveal here a developmental roadmap for human telencephalic neurons. Both dorsal and ventral telencephalic radial glial cells (RGs) differentiate into neurons via dividing intermediate progenitor cells (IPCs_div) and early postmitotic neuroblasts (eNBs). The transcription factor ASCL1 plays a key role in promoting fate transition from RGs to IPCs_div in both regions. RGs from the regionalized neuroectoderm show heterogeneity, with restricted glutamatergic, GABAergic, and cholinergic differentiation potencies. During neurogenesis, IPCs_div gradually exit the cell cycle and branch into sister eNBs to generate distinct neuronal subtypes. Our findings highlight a general RGs-IPCs_div-eNBs developmental scheme for human telencephalic progenitors and support that the major neuronal fates of human telencephalon are predetermined during dorsoventral regionalization with neuronal diversity being further shaped during neurogenesis and neural circuit integration.
Topics: Basic Helix-Loop-Helix Transcription Factors; Cell Cycle; Cell Differentiation; Cell Lineage; Choline; Doublecortin Protein; Fetus; Gene Expression Regulation, Developmental; Gene Ontology; Glutamate Decarboxylase; Glutamic Acid; Humans; LIM-Homeodomain Proteins; Molecular Sequence Annotation; Nerve Tissue Proteins; Neural Stem Cells; Neurogenesis; Neuroglia; Neurons; SOXC Transcription Factors; Signal Transduction; Stathmin; Telencephalon; Transcription Factors; gamma-Aminobutyric Acid
PubMed: 34558085
DOI: 10.15252/embj.2020107277