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      Synaptic configuration and reconfiguration in the neocortex are spatiotemporally selective

      review-article
      Anatomical Science International
      Springer Nature Singapore
      Cell type, Neocortex, Neural circuit, Plasticity, Synapse

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          Abstract

          Brain computation relies on the neural networks. Neurons extend the neurites such as dendrites and axons, and the contacts of these neurites that form chemical synapses are the biological basis of signal transmissions in the central nervous system. Individual neuronal outputs can influence the other neurons within the range of the axonal spread, while the activities of single neurons can be affected by the afferents in their somatodendritic fields. The morphological profile, therefore, binds the functional role each neuron can play. In addition, synaptic connectivity among neurons displays preference based on the characteristics of presynaptic and postsynaptic neurons. Here, the author reviews the “spatial” and “temporal” connection selectivity in the neocortex. The histological description of the neocortical circuitry depends primarily on the classification of cell types, and the development of gene engineering techniques allows the cell type-specific visualization of dendrites and axons as well as somata. Using genetic labeling of particular cell populations combined with immunohistochemistry and imaging at a subcellular spatial resolution, we revealed the “spatial selectivity” of cortical wirings in which synapses are non-uniformly distributed on the subcellular somatodendritic domains in a presynaptic cell type-specific manner. In addition, cortical synaptic dynamics in learning exhibit presynaptic cell type-dependent “temporal selectivity”: corticocortical synapses appear only transiently during the learning phase, while learning-induced new thalamocortical synapses persist, indicating that distinct circuits may supervise learning-specific ephemeral synapse and memory-specific immortal synapse formation. The selectivity of spatial configuration and temporal reconfiguration in the neural circuitry may govern diverse functions in the neocortex.

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          Most cited references211

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          A robust and high-throughput Cre reporting and characterization system for the whole mouse brain

          The Cre/lox system is widely used in mice to achieve cell-type-specific gene expression. However, a strong and universal responding system to express genes under Cre control is still lacking. We have generated a set of Cre reporter mice with strong, ubiquitous expression of fluorescent proteins of different spectra. The robust native fluorescence of these reporters enables direct visualization of fine dendritic structures and axonal projections of the labeled neurons, which is useful in mapping neuronal circuitry, imaging and tracking specific cell populations in vivo. Using these reporters and a high-throughput in situ hybridization platform, we are systematically profiling Cre-directed gene expression throughout the mouse brain in a number of Cre-driver lines, including novel Cre lines targeting different cell types in the cortex. Our expression data are displayed in a public online database to help researchers assess the utility of various Cre-driver lines for cell-type-specific genetic manipulation.
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            Interneurons of the neocortical inhibitory system.

            Mammals adapt to a rapidly changing world because of the sophisticated cognitive functions that are supported by the neocortex. The neocortex, which forms almost 80% of the human brain, seems to have arisen from repeated duplication of a stereotypical microcircuit template with subtle specializations for different brain regions and species. The quest to unravel the blueprint of this template started more than a century ago and has revealed an immensely intricate design. The largest obstacle is the daunting variety of inhibitory interneurons that are found in the circuit. This review focuses on the organizing principles that govern the diversity of inhibitory interneurons and their circuits.
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              A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex.

              A key obstacle to understanding neural circuits in the cerebral cortex is that of unraveling the diversity of GABAergic interneurons. This diversity poses general questions for neural circuit analysis: how are these interneuron cell types generated and assembled into stereotyped local circuits and how do they differentially contribute to circuit operations that underlie cortical functions ranging from perception to cognition? Using genetic engineering in mice, we have generated and characterized approximately 20 Cre and inducible CreER knockin driver lines that reliably target major classes and lineages of GABAergic neurons. More select populations are captured by intersection of Cre and Flp drivers. Genetic targeting allows reliable identification, monitoring, and manipulation of cortical GABAergic neurons, thereby enabling a systematic and comprehensive analysis from cell fate specification, migration, and connectivity, to their functions in network dynamics and behavior. As such, this approach will accelerate the study of GABAergic circuits throughout the mammalian brain. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                sohn.jaerin.dent@osaka-u.ac.jp
                Journal
                Anat Sci Int
                Anat Sci Int
                Anatomical Science International
                Springer Nature Singapore (Singapore )
                1447-6959
                1447-073X
                14 October 2023
                14 October 2023
                2024
                : 99
                : 1
                : 17-33
                Affiliations
                Department of Systematic Anatomy and Neurobiology, Graduate School of Dentistry, Osaka University, ( https://ror.org/035t8zc32) Suita, Osaka 565-0871 Japan
                Author information
                http://orcid.org/0000-0001-8358-327X
                Article
                743
                10.1007/s12565-023-00743-5
                10771605
                37837522
                c41f4154-e933-40bc-ad0a-b7e1f2d49ff0
                © The Author(s) 2023

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 24 May 2023
                : 14 September 2023
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: 21K15200
                Award Recipient :
                Funded by: Osaka University
                Categories
                Review Article
                Custom metadata
                © Japanese Association of Anatomists 2024

                Anatomy & Physiology
                cell type,neocortex,neural circuit,plasticity,synapse
                Anatomy & Physiology
                cell type, neocortex, neural circuit, plasticity, synapse

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