Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections

Subplate (SP) neurons are among the earliest-born neurons in the cerebral cortex and heterogeneous in terms of gene expression. SP neurons consist mainly of projection neurons, which begin to extend their axons to specific target areas very early during development. However, the relationships betwee...

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Main Authors: Sheena Yin Xin Tiong, Yuichiro Oka, Tatsuya Sasaki, Manabu Taniguchi, Miyuki Doi, Hisanori Akiyama, Makoto Sato
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnana.2019.00039/full
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author Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Tatsuya Sasaki
Manabu Taniguchi
Miyuki Doi
Hisanori Akiyama
Makoto Sato
Makoto Sato
Makoto Sato
Makoto Sato
author_facet Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Tatsuya Sasaki
Manabu Taniguchi
Miyuki Doi
Hisanori Akiyama
Makoto Sato
Makoto Sato
Makoto Sato
Makoto Sato
author_sort Sheena Yin Xin Tiong
collection DOAJ
description Subplate (SP) neurons are among the earliest-born neurons in the cerebral cortex and heterogeneous in terms of gene expression. SP neurons consist mainly of projection neurons, which begin to extend their axons to specific target areas very early during development. However, the relationships between axon projection and gene expression patterns of the SP neurons, and their remnant layer 6b (L6b) neurons, are largely unknown. In this study, we analyzed the corticocortical projections of L6b/SP neurons in the mouse cortex and searched for a marker gene expressed in L6b/SP neurons that have ipsilateral inter-areal projections. Retrograde tracing experiments demonstrated that L6b/SP neurons in the primary somatosensory cortex (S1) projected to the primary motor cortex (M1) within the same cortical hemisphere at postnatal day (PD) 2 but did not show any callosal projection. This unilateral projection pattern persisted into adulthood. Our microarray analysis identified the gene encoding a β subunit of voltage-gated potassium channel (Kcnab1) as being expressed in L6b/SP. Double labeling with retrograde tracing and in situ hybridization demonstrated that Kcnab1 was expressed in the unilaterally-projecting neurons in L6b/SP. Embryonic expression was specifically detected in the SP as early as embryonic day (E) 14.5, shortly after the emergence of SP. Double immunostaining experiments revealed different degrees of co-expression of the protein product Kvβ1 with L6b/SP markers Ctgf (88%), Cplx3 (79%), and Nurr1 (58%), suggesting molecular subdivision of unilaterally-projecting L6b/SP neurons. In addition to expression in L6b/SP, scattered expression of Kcnab1 was observed during postnatal stages without layer specificity. Among splicing variants with three alternative first exons, the variant 1.1 explained all the cortical expression mentioned in this study. Together, our data suggest that L6b/SP neurons have corticocortical projections and Kcnab1 expression defines a subpopulation of L6b/SP neurons with a unilateral inter-areal projection.
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spelling doaj.art-6a28b6cbd188401e871106951b236b712022-12-22T03:00:30ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292019-05-011310.3389/fnana.2019.00039441971Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal ProjectionsSheena Yin Xin Tiong0Sheena Yin Xin Tiong1Sheena Yin Xin Tiong2Yuichiro Oka3Yuichiro Oka4Yuichiro Oka5Yuichiro Oka6Tatsuya Sasaki7Manabu Taniguchi8Miyuki Doi9Hisanori Akiyama10Makoto Sato11Makoto Sato12Makoto Sato13Makoto Sato14Department of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDivision of Developmental Neuroscience, Department of Child Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Osaka, JapanInstitute of Biological Sciences, Faculty of Science, University of Malaya, Kuala Lumpur, MalaysiaDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDivision of Developmental Neuroscience, Department of Child Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Osaka, JapanDivision of Cell Biology and Neuroscience, Department of Morphological and Physiological Sciences, Faculty of Medical Sciences, University of Fukui, Fukui, JapanResearch Center for Child Mental Development, University of Fukui, Fukui, JapanDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDepartment of Anatomy and Neuroscience, Graduate School of Medicine, Osaka University, Osaka, JapanDivision of Developmental Neuroscience, Department of Child Development, United Graduate School of Child Development, Osaka University, Kanazawa University, Hamamatsu University School of Medicine, Chiba University and University of Fukui, Osaka, JapanDivision of Cell Biology and Neuroscience, Department of Morphological and Physiological Sciences, Faculty of Medical Sciences, University of Fukui, Fukui, JapanResearch Center for Child Mental Development, University of Fukui, Fukui, JapanSubplate (SP) neurons are among the earliest-born neurons in the cerebral cortex and heterogeneous in terms of gene expression. SP neurons consist mainly of projection neurons, which begin to extend their axons to specific target areas very early during development. However, the relationships between axon projection and gene expression patterns of the SP neurons, and their remnant layer 6b (L6b) neurons, are largely unknown. In this study, we analyzed the corticocortical projections of L6b/SP neurons in the mouse cortex and searched for a marker gene expressed in L6b/SP neurons that have ipsilateral inter-areal projections. Retrograde tracing experiments demonstrated that L6b/SP neurons in the primary somatosensory cortex (S1) projected to the primary motor cortex (M1) within the same cortical hemisphere at postnatal day (PD) 2 but did not show any callosal projection. This unilateral projection pattern persisted into adulthood. Our microarray analysis identified the gene encoding a β subunit of voltage-gated potassium channel (Kcnab1) as being expressed in L6b/SP. Double labeling with retrograde tracing and in situ hybridization demonstrated that Kcnab1 was expressed in the unilaterally-projecting neurons in L6b/SP. Embryonic expression was specifically detected in the SP as early as embryonic day (E) 14.5, shortly after the emergence of SP. Double immunostaining experiments revealed different degrees of co-expression of the protein product Kvβ1 with L6b/SP markers Ctgf (88%), Cplx3 (79%), and Nurr1 (58%), suggesting molecular subdivision of unilaterally-projecting L6b/SP neurons. In addition to expression in L6b/SP, scattered expression of Kcnab1 was observed during postnatal stages without layer specificity. Among splicing variants with three alternative first exons, the variant 1.1 explained all the cortical expression mentioned in this study. Together, our data suggest that L6b/SP neurons have corticocortical projections and Kcnab1 expression defines a subpopulation of L6b/SP neurons with a unilateral inter-areal projection.https://www.frontiersin.org/article/10.3389/fnana.2019.00039/fullsubplateaxon projectionKcnab1cerebral cortexpotassium channelcorticocortical projection
spellingShingle Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Sheena Yin Xin Tiong
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Yuichiro Oka
Tatsuya Sasaki
Manabu Taniguchi
Miyuki Doi
Hisanori Akiyama
Makoto Sato
Makoto Sato
Makoto Sato
Makoto Sato
Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
Frontiers in Neuroanatomy
subplate
axon projection
Kcnab1
cerebral cortex
potassium channel
corticocortical projection
title Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
title_full Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
title_fullStr Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
title_full_unstemmed Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
title_short Kcnab1 Is Expressed in Subplate Neurons With Unilateral Long-Range Inter-Areal Projections
title_sort kcnab1 is expressed in subplate neurons with unilateral long range inter areal projections
topic subplate
axon projection
Kcnab1
cerebral cortex
potassium channel
corticocortical projection
url https://www.frontiersin.org/article/10.3389/fnana.2019.00039/full
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