15
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Editorial: The Earliest-Born Cortical Neurons as Multi-Tasking Pioneers: Expanding Roles for Subplate Neurons in Cerebral Cortex Organization and Function

      editorial
      1 , 2 , * , 3
      Frontiers in Neuroanatomy
      Frontiers Media S.A.
      cerebral cortex, development, layer 6b, neocortex, subplate

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The subplate is a unique layer in the mammalian neocortex. It consists of the earliest-born neurons in the neocortex and undergoes a massive reduction in the number of neurons during postnatal development. The subplate is also characterized by its heterogeneity in cell morphology, incomparable gene expression pattern, and an early functional maturation. This diversity in form and function is evident in its role in circuit formation processes between the cortex and thalamus and also within a local cortical area above it. Disruptions of the subplate can lead to neurodevelopmental deficits such as autism spectrum disorder. Postmitotic neurons born in the ventricular zone first form the preplate together with Cajal-Retzius cells, which originate from three distinct regions of the dorsal telencephalon (reviewed in Barber and Pierani, 2016). The preplate is then split, by later-born neurons coming in between to form the cortical plate, into the marginal zone at the surface (containing Cajal-Retzius cells) and the subplate at the base of the cortical plate. Although most of the subplate neurons are early born preplate neurons in rodents, the vast majority of subplate neurons are generated during mid-gestation in primates (Duque et al., 2016). While many subplate neurons are lost during postnatal development, not all of them disappear. Recent morphological and gene expression studies have provided evidence that layer 6b in the adult (or juvenile) cortex contains remnant subplate neurons (Hoerder-Suabedissen et al., 2013; Marx et al., 2017). Subplate neurons exhibit morphological heterogeneity in the somatodendritic structure. In addition to typical pyramidal neurons found in layers 2-6a; horizontal cells, multipolar cells, inverted pyramidal cells, fusiform cells, and polymorphous cells are among those reported in the subplate (Mrzljak et al., 1988; Hanganu et al., 2002). These cell types are maintained between the early postnatal subplate and juvenile layer 6b despite a decrease in their abundance (Marx et al., 2017). The subplate is more than a transient embryonic structure. In primates, the subplate is much thicker, and subplate neurons remain as “interstitial cells” in the white matter (Kostovic and Rakic, 1990), suggesting prominent roles of subplate neurons in primates. As pyramidal neurons increase in abundance in layer 6b, it is suggested that layer 6b consists of remnant subplate neurons and cortical pyramidal neurons. Interestingly, intermediate progenitor cells expressing Tbr2 contribute to projection neurons in all layers, including preplate Cajal-Retzius neurons and the subplate (Vasistha et al., 2015; Mihalas et al., 2016), suggesting that pyramidal neurons that increase in juveniles might derive from Tbr2-expressing progenitors. Transcriptomic analyses of cortical neurons and those focused on subplate neurons, identified genes specifically expressed in subplate/layer 6b with a differential time course (Bernard et al., 2012; Oeschger et al., 2012; Hoerder-Suabedissen et al., 2013; Tasic et al., 2016). A cell clustering analysis based on single cell RNAseq data classified layer 6b cells into two cell types (Tasic et al., 2016). Molecular markers for subplate/layer 6b neurons, however, have been shown to be expressed in overlapping populations (Hoerder-Suabedissen and Molnár, 2013; Tiong et al.), making it difficult to correlate gene expression profiles with cellular morphology, neuronal connection patterns, and electrophysiological properties. During the embryonic stage, the subplate serves as a critical interface between cortical neurons and incoming thalamocortical axons. Thalamocortical axons transiently connect with subplate neurons before they enter the cortical plate and finally reach layer 4 (Kostovic and Goldman-Rakic, 1983; Kageyama and Robertson, 1993; Herrmann et al., 1994). This transient connection is functional, as thalamic stimulations in the thalamocortical slices from rat embryos induce responses in subplate neurons (Higashi et al., 2002; Molnár et al., 2003), indicating the early maturation of subplate neurons. Furthermore, subplate neurons contain positional cues for thalamic axons to target appropriate cortical areas. When the areal identity is disorganized by mis-expressing cortical patterning molecule FGF8, in the subplate as well as in cortical plate, thalamic axons run longer in the subplate before they turn into the cortical plate (Shimogori and Grove, 2005). On the other hand, projection to the thalamus by subplate neurons was thought to pioneer the cortico-thalamic projections by neurons in layers 5 and 6. At least in ferrets, however, axons of layer 5 neurons arrive at the thalamic nuclei earlier than those of subplate and layer 6 neurons (Clascá et al., 1995), arguing against the pioneering function of subplate axons. Additionally, the subplate (layer 6b) also shapes corticofugal pathways (Grant et al., 2012) and callosal connections (deAzevedo et al., 1997). For example, retinal inputs regulate layer 6b neuronal projections, which may in turn influence the projection of layer 5 neurons (Grant et al., 2016). Subplate neurons are also indispensable for local network formation, especially in the primary sensory areas. For example, ablation of the subplate in the visual cortex affects ocular dominance column formation by affecting the maturation of thalamocortical connections to layer 4 (Ghosh and Shatz, 1992; Kanold and Shatz, 2006). In addition to the foundational studies described above, recent work has revealed new aspects of the subplate function and form, such as modulation of radial migration of later-born neurons (Ohtaka-Maruyama et al., 2018), extra-cortical origins (Pedraza et al., 2014), and fate selection of later-born neurons (Ozair et al., 2018). This Research Topic entitled The Earliest-Born Cortical Neurons as Multi-Tasking Pioneers: Expanding Roles for Subplate Neurons in Cerebral Cortex Organization and Function, consists of a collection of three Review articles that provide up-to-date overviews on multiple functions of the subplate in cortical development and two Original Research articles that report novel findings in the development and function of the subplate. Luhmann et al. summarize the electrophysiology of subplate neurons including intrinsic membrane properties and firing patterns, and input/output connection patterns of subplate neurons, discussing possible roles in cortical spindle burst and gamma oscillation. A review by Kanold et al. explains sensory-evoked plasticity of neuronal circuits of subplate neurons during development and in pathological conditions, focusing on the silent synapses formed onto them. In addition to the two Review articles above, a Mini Review by Ohtaka-Maruyama features a novel function of the subplate in the regulation of the migration of cortical plate neurons. This finding revealed another mechanism for mode switching of neuronal migration from slow multipolar migration to rapid locomotion, guided by radial fibers. Yu et al. use conditional mouse knockouts to define new functions of a well-established subplate marker gene, Ctgf, in regulating the number and dendritic complexity of subplate neurons, and maturation of oligodendrocytes in the white matter beneath the primary somatosensory cortex. Finally, an article by Tiong et al. identified a novel marker gene for the mouse embryonic subplate and shows that it is expressed in 80% of layer 6b neurons in the primary somatosensory cortex that project axons to the primary motor cortex. This marker should be a useful tool to study functions of subplate neurons at early stages of cortical development. The aim of this Research Topic is to highlight the versatility of the subplate in cortical development and to attract readers to this unique layer in the mammalian neocortex. We would like to thank all the contributors and readers and hope future work will elucidate developmental mechanisms and circuit functions of the subplate, which is important both scientifically and clinically. Author Contributions All authors listed have made a substantial, direct and intellectual contribution to the work, and approved it for publication. Conflict of Interest The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

          Related collections

          Most cited references26

          • Record: found
          • Abstract: found
          • Article: not found

          Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain.

          The cytological organization and the timetable of emergence and dissolution of the transient subplate zone subjacent to the developing visual and somatosensory cortex were studied in a series of human and monkey fetal brains. Cerebral walls processed with Nissl, Golgi, electron-microscopic, and histochemical methods show that this zone consists of migratory and postmigratory neurons, growth cones, loosely arranged axons, dendrites, synapses, and glial cells. In both species the subplate zone becomes visible at the beginning of the mid-third of gestation as a cell-poor/fiber-rich layer situated between the intermediate zone and the developing cortical plate. The subplate zone appears earlier in the somatosensory than in the visual area and reaches maximal width at the beginning of the last third of gestation in both regions. At the peak of its size the ratio between the width of the subplate zone and cortical plate in the somatosensory cortex is 2:1 in monkey and 4:1 in man while in the occipital lobe these structures have about equal width in both species. The dissolution of the subplate zone begins during the last third of gestation with degeneration of some subplate neurons and the relocation of fiber terminals into the cortex. The subplate zone disappears faster in the visual than in the somatosensory area. The present results together with our previous findings support the hypothesis that the subplate zone may serve as a "waiting" compartment for transient cellular interactions and a substrate for competition, segregation, and growth of afferents originated sequentially from the brain stem, basal forebrain, thalamus, and from the ipsi- and contralateral cerebral hemisphere. After a variable and partially overlapping time period, these fibers enter the cortical plate while the subplate zone disappears leaving only a vestige of cells scattered throughout the subcortical white matter. A comparison between species indicates that the size and duration of the subplate zone increases during mammalian evolution and culminates in human fetuses concomitantly with an enlargement of cortico-cortical fiber systems. The regional difference in the size, pattern, and resolution of the subplate zone correlates also with the pattern of cerebral convolutions. Our findings indicate that, contrary to prevailing notions, the subplate may not be a vestige of the phylogenetically old network but a transient embryonic structure that expanded during evolution to subserve the increasing number of its connections.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Transcriptional architecture of the primate neocortex.

            Genome-wide transcriptional profiling was used to characterize the molecular underpinnings of neocortical organization in rhesus macaque, including cortical areal specialization and laminar cell-type diversity. Microarray analysis of individual cortical layers across sensorimotor and association cortices identified robust and specific molecular signatures for individual cortical layers and areas, prominently involving genes associated with specialized neuronal function. Overall, transcriptome-based relationships were related to spatial proximity, being strongest between neighboring cortical areas and between proximal layers. Primary visual cortex (V1) displayed the most distinctive gene expression compared to other cortical regions in rhesus and human, both in the specialized layer 4 as well as other layers. Laminar patterns were more similar between macaque and human compared to mouse, as was the unique V1 profile that was not observed in mouse. These data provide a unique resource detailing neocortical transcription patterns in a nonhuman primate with great similarity in gene expression to human. Copyright © 2012 Elsevier Inc. All rights reserved.
              Bookmark
              • Record: found
              • Abstract: not found
              • Article: not found

              Synaptic transmission from subplate neurons controls radial migration of neocortical neurons

                Bookmark

                Author and article information

                Contributors
                Journal
                Front Neuroanat
                Front Neuroanat
                Front. Neuroanat.
                Frontiers in Neuroanatomy
                Frontiers Media S.A.
                1662-5129
                25 August 2020
                2020
                : 14
                : 43
                Affiliations
                [1] 1Department of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University , Suita, Japan
                [2] 2Division of Developmental Neuroscience, United Graduate School of Child Development, Osaka University , Suita, Japan
                [3] 3Institute of Cellular and Organismic Biology, Academia Sinica , Taipei, Taiwan
                Author notes

                Edited by: Zoltan Molnar, University of Oxford, United Kingdom

                Reviewed by: Zdravko Petanjek, University of Zagreb, Croatia; Robert Francis Hevner, University of California, San Diego, United States

                *Correspondence: Makoto Sato makosato@ 123456anat2.med.osaka-u.ac.jp
                Article
                10.3389/fnana.2020.00043
                7479822
                32982700
                c2e3d334-cb0e-4fac-ac06-9190a91bc06a
                Copyright © 2020 Sato and Chou.

                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
                : 22 May 2020
                : 25 June 2020
                Page count
                Figures: 0, Tables: 0, Equations: 0, References: 28, Pages: 3, Words: 2333
                Categories
                Neuroscience
                Editorial

                Neurosciences
                cerebral cortex,development,layer 6b,neocortex,subplate
                Neurosciences
                cerebral cortex, development, layer 6b, neocortex, subplate

                Comments

                Comment on this article