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      Shifting Developmental Trajectories During Critical Periods of Brain Formation

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          Abstract

          Critical periods of brain development are epochs of heightened plasticity driven by environmental influence necessary for normal brain function. Recent studies are beginning to shed light on the possibility that timely interventions during critical periods hold potential to reorient abnormal developmental trajectories in animal models of neurological and neuropsychiatric disorders. In this review, we re-examine the criteria defining critical periods, highlighting the recently discovered mechanisms of developmental plasticity in health and disease. In addition, we touch upon technological improvements for modeling critical periods in human-derived neural networks in vitro. These scientific advances associated with the use of developmental manipulations in the immature brain of animal models are the basic preclinical systems that will allow the future translatability of timely interventions into clinical applications for neurodevelopmental disorders such as intellectual disability, autism spectrum disorders (ASD) and schizophrenia.

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          Most cited references158

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          Stress and the brain: from adaptation to disease.

          In response to stress, the brain activates several neuropeptide-secreting systems. This eventually leads to the release of adrenal corticosteroid hormones, which subsequently feed back on the brain and bind to two types of nuclear receptor that act as transcriptional regulators. By targeting many genes, corticosteroids function in a binary fashion, and serve as a master switch in the control of neuronal and network responses that underlie behavioural adaptation. In genetically predisposed individuals, an imbalance in this binary control mechanism can introduce a bias towards stress-related brain disease after adverse experiences. New candidate susceptibility genes that serve as markers for the prediction of vulnerable phenotypes are now being identified.
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            Assembly of Functional Forebrain Spheroids from Human Pluripotent Cells

            SUMMARY The development of the nervous system involves a coordinated succession of events including the migration of GABAergic neurons from ventral to dorsal forebrain and their integration into cortical circuits. However, these interregional interactions have not yet been modelled with human cells. Here, we generate from human pluripotent cells three-dimensional spheroids resembling either the dorsal or ventral forebrain and containing cortical glutamatergic or GABAergic neurons. These subdomain-specific forebrain spheroids can be assembled to recapitulate the saltatory migration of interneurons similar to migration in fetal forebrain. Using this system, we find that in Timothy syndrome– a neurodevelopmental disorder that is caused by mutations in the CaV1.2 calcium channel, interneurons display abnormal migratory saltations. We also show that after migration, interneurons functionally integrate with glutamatergic neurons to form a microphysiological system. We anticipate that this approach will be useful for studying development and disease, and for deriving spheroids that resemble other brain regions to assemble circuits in vitro.
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              Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models.

              Vulnerable periods during the development of the nervous system are sensitive to environmental insults because they are dependent on the temporal and regional emergence of critical developmental processes (i.e., proliferation, migration, differentiation, synaptogenesis, myelination, and apoptosis). Evidence from numerous sources demonstrates that neural development extends from the embryonic period through adolescence. In general, the sequence of events is comparable among species, although the time scales are considerably different. Developmental exposure of animals or humans to numerous agents (e.g., X-ray irradiation, methylazoxymethanol, ethanol, lead, methyl mercury, or chlorpyrifos) demonstrates that interference with one or more of these developmental processes can lead to developmental neurotoxicity. Different behavioral domains (e.g., sensory, motor, and various cognitive functions) are subserved by different brain areas. Although there are important differences between the rodent and human brain, analogous structures can be identified. Moreover, the ontogeny of specific behaviors can be used to draw inferences regarding the maturation of specific brain structures or neural circuits in rodents and primates, including humans. Furthermore, various clinical disorders in humans (e.g., schizophrenia, dyslexia, epilepsy, and autism) may also be the result of interference with normal ontogeny of developmental processes in the nervous system. Of critical concern is the possibility that developmental exposure to neurotoxicants may result in an acceleration of age-related decline in function. This concern is compounded by the fact that developmental neurotoxicity that results in small effects can have a profound societal impact when amortized across the entire population and across the life span of humans. Images Figure 2 Figure 3 Figure 4 Figure 5 Figure 6 Figure 8 Figure 9 Figure 12 Figure 14 Figure 16 Figure 17
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                Author and article information

                Contributors
                Journal
                Front Cell Neurosci
                Front Cell Neurosci
                Front. Cell. Neurosci.
                Frontiers in Cellular Neuroscience
                Frontiers Media S.A.
                1662-5102
                10 September 2020
                2020
                : 14
                : 283
                Affiliations
                [1] 1Eccles Institute of Neuroscience, The John Curtin School of Medical Research, Australian National University , Canberra, ACT, Australia
                [2] 2Principe Felipe Research Center (Centro de Investigación Principe Felipe, CIPF) , Valencia, Spain
                Author notes

                Edited by: Robert C. Froemke, New York University, United States

                Reviewed by: Tommaso Pizzorusso, University of Florence, Italy; Marina Guizzetti, Oregon Health and Science University, United States

                *Correspondence: Isabel Del Pino idelpino@ 123456cipf.es

                These authors have contributed equally to this work

                Specialty section: This article was submitted to Cellular Neurophysiology, a section of the journal Frontiers in Cellular Neuroscience

                Article
                10.3389/fncel.2020.00283
                7513795
                33132842
                9ff8a7ef-f6b0-4910-8481-c5546947638c
                Copyright © 2020 Dehorter and Del Pino.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 20 May 2020
                : 10 August 2020
                Page count
                Figures: 4, Tables: 0, Equations: 0, References: 158, Pages: 14, Words: 12303
                Funding
                Funded by: Ministerio de Ciencia, Innovación y Universidades 10.13039/100014440
                Funded by: Australian National University 10.13039/501100000995
                Categories
                Cellular Neuroscience
                Review

                Neurosciences
                development,plasticity,critical period,neurodevelopmental disorders,brain organoids
                Neurosciences
                development, plasticity, critical period, neurodevelopmental disorders, brain organoids

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