Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex.

IF 3.8 2区 生物学 Q1 BIOCHEMICAL RESEARCH METHODS
PLoS Computational Biology Pub Date : 2024-09-23 eCollection Date: 2024-09-01 DOI:10.1371/journal.pcbi.1012428
Nafiseh Atapour, Marcello G P Rosa, Shi Bai, Sylwia Bednarek, Agata Kulesza, Gabriela Saworska, Sadaf Teymornejad, Katrina H Worthy, Piotr Majka
{"title":"Distribution of calbindin-positive neurons across areas and layers of the marmoset cerebral cortex.","authors":"Nafiseh Atapour, Marcello G P Rosa, Shi Bai, Sylwia Bednarek, Agata Kulesza, Gabriela Saworska, Sadaf Teymornejad, Katrina H Worthy, Piotr Majka","doi":"10.1371/journal.pcbi.1012428","DOIUrl":null,"url":null,"abstract":"<p><p>The diversity of the mammalian cerebral cortex demands technical approaches to map the spatial distribution of neurons with different biochemical identities. This issue is magnified in the case of the primate cortex, characterized by a large number of areas with distinctive cytoarchitectures. To date, no full map of the distribution of cells expressing a specific protein has been reported for the cortex of any primate. Here we have charted the 3-dimensional distribution of neurons expressing the calcium-binding protein calbindin (CB+ neurons) across the entire marmoset cortex, using a combination of immunohistochemistry, automated cell identification, computerized reconstruction, and cytoarchitecture-aware registration. CB+ neurons formed a heterogeneous population, which together corresponded to 10-20% of the cortical neurons. They occurred in higher proportions in areas corresponding to low hierarchical levels of processing, such as sensory cortices. Although CB+ neurons were concentrated in the supragranular and granular layers, there were clear global trends in their laminar distribution. For example, their relative density in infragranular layers increased with hierarchical level along sensorimotor processing streams, and their density in layer 4 was lower in areas involved in sensorimotor integration, action planning and motor control. These results reveal new quantitative aspects of the cytoarchitectural organization of the primate cortex, and demonstrate an approach to mapping the full distribution of neurochemically distinct cells throughout the brain which is readily applicable to most other mammalian species.</p>","PeriodicalId":20241,"journal":{"name":"PLoS Computational Biology","volume":null,"pages":null},"PeriodicalIF":3.8000,"publicationDate":"2024-09-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495585/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Computational Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pcbi.1012428","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/9/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"BIOCHEMICAL RESEARCH METHODS","Score":null,"Total":0}
引用次数: 0

Abstract

The diversity of the mammalian cerebral cortex demands technical approaches to map the spatial distribution of neurons with different biochemical identities. This issue is magnified in the case of the primate cortex, characterized by a large number of areas with distinctive cytoarchitectures. To date, no full map of the distribution of cells expressing a specific protein has been reported for the cortex of any primate. Here we have charted the 3-dimensional distribution of neurons expressing the calcium-binding protein calbindin (CB+ neurons) across the entire marmoset cortex, using a combination of immunohistochemistry, automated cell identification, computerized reconstruction, and cytoarchitecture-aware registration. CB+ neurons formed a heterogeneous population, which together corresponded to 10-20% of the cortical neurons. They occurred in higher proportions in areas corresponding to low hierarchical levels of processing, such as sensory cortices. Although CB+ neurons were concentrated in the supragranular and granular layers, there were clear global trends in their laminar distribution. For example, their relative density in infragranular layers increased with hierarchical level along sensorimotor processing streams, and their density in layer 4 was lower in areas involved in sensorimotor integration, action planning and motor control. These results reveal new quantitative aspects of the cytoarchitectural organization of the primate cortex, and demonstrate an approach to mapping the full distribution of neurochemically distinct cells throughout the brain which is readily applicable to most other mammalian species.

狨猴大脑皮层各区域和各层钙蛋白酶阳性神经元的分布。
哺乳动物大脑皮层的多样性要求采用技术方法绘制具有不同生化特性的神经元的空间分布图。这一问题在灵长类动物大脑皮层中更为突出,因为灵长类动物大脑皮层有大量具有独特细胞结构的区域。迄今为止,还没有任何灵长类动物大脑皮层表达特定蛋白质的细胞分布完整图谱。在这里,我们采用免疫组化、自动细胞识别、计算机重建和细胞结构感知注册相结合的方法,绘制了表达钙结合蛋白钙宾蛋白(CB+神经元)的神经元在整个狨猴大脑皮层的三维分布图。CB+ 神经元形成了一个异质性群体,总共相当于皮层神经元的 10-20%。在感觉皮层等低层次处理区域,CB+神经元的比例较高。虽然 CB+ 神经元集中在上颗粒层和颗粒层,但它们的层状分布有明显的全球性趋势。例如,CB+神经元在下颗粒层的相对密度随着感觉运动处理流的层次而增加,而在涉及感觉运动整合、行动规划和运动控制的区域,CB+神经元在第4层的密度较低。这些结果揭示了灵长类动物大脑皮层细胞结构组织的新的定量方面,并展示了一种绘制整个大脑中不同神经化学细胞完整分布图的方法,这种方法很容易适用于大多数其他哺乳动物物种。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
PLoS Computational Biology
PLoS Computational Biology BIOCHEMICAL RESEARCH METHODS-MATHEMATICAL & COMPUTATIONAL BIOLOGY
CiteScore
7.10
自引率
4.70%
发文量
820
审稿时长
2.5 months
期刊介绍: PLOS Computational Biology features works of exceptional significance that further our understanding of living systems at all scales—from molecules and cells, to patient populations and ecosystems—through the application of computational methods. Readers include life and computational scientists, who can take the important findings presented here to the next level of discovery. Research articles must be declared as belonging to a relevant section. More information about the sections can be found in the submission guidelines. Research articles should model aspects of biological systems, demonstrate both methodological and scientific novelty, and provide profound new biological insights. Generally, reliability and significance of biological discovery through computation should be validated and enriched by experimental studies. Inclusion of experimental validation is not required for publication, but should be referenced where possible. Inclusion of experimental validation of a modest biological discovery through computation does not render a manuscript suitable for PLOS Computational Biology. Research articles specifically designated as Methods papers should describe outstanding methods of exceptional importance that have been shown, or have the promise to provide new biological insights. The method must already be widely adopted, or have the promise of wide adoption by a broad community of users. Enhancements to existing published methods will only be considered if those enhancements bring exceptional new capabilities.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信