Molecular states underlying neuronal cell type development and plasticity in the postnatal whisker cortex.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences
PLoS Biology Pub Date : 2025-05-14 eCollection Date: 2025-05-01 DOI:10.1371/journal.pbio.3003176
Salwan Butrus, Hannah R Monday, Christopher J Yoo, Daniel E Feldman, Karthik Shekhar
{"title":"Molecular states underlying neuronal cell type development and plasticity in the postnatal whisker cortex.","authors":"Salwan Butrus, Hannah R Monday, Christopher J Yoo, Daniel E Feldman, Karthik Shekhar","doi":"10.1371/journal.pbio.3003176","DOIUrl":null,"url":null,"abstract":"<p><p>Mouse whisker somatosensory cortex (wS1) is a major model system to study the experience-dependent plasticity of cortical neuron physiology, morphology, and sensory coding. However, the role of sensory experience in regulating neuronal cell type development and gene expression in wS1 remains poorly understood. We assembled a transcriptomic atlas of wS1 during postnatal development comprising 45 molecularly distinct neuronal types that can be grouped into eight excitatory and four inhibitory neuron subclasses. Between postnatal day (P) 12, the onset of active whisking, and P22, when classical critical periods close, ~ 250 genes were regulated in a neuronal subclass-specific fashion when whisker experience was normal. At the resolution of neuronal types, only the composition of layer (L) 2/3 glutamatergic neurons, but not other neuronal types, changed substantially between P12 and P22. These postnatal compositional changes in L2/3 neuronal types resemble those observed previously in the primary visual cortex (V1), and the temporal gene expression changes were also highly conserved between the regions. Unlike V1, however, cell type maturation in wS1 is not substantially dependent on sensory experience, as 10-day full-face whisker deprivation from P12 to P22 did not influence the transcriptomic identity nor composition of L2/3 neuronal types. A one-day competitive whisker deprivation protocol from P21 to P22 also did not affect cell type identity but induced moderate changes in plasticity-related gene expression. Thus, developmental maturation of cell types is similar in V1 and wS1, but sensory deprivation minimally affects cell type development in wS1.</p>","PeriodicalId":49001,"journal":{"name":"PLoS Biology","volume":"23 5","pages":"e3003176"},"PeriodicalIF":9.8000,"publicationDate":"2025-05-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pbio.3003176","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/5/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0

Abstract

Mouse whisker somatosensory cortex (wS1) is a major model system to study the experience-dependent plasticity of cortical neuron physiology, morphology, and sensory coding. However, the role of sensory experience in regulating neuronal cell type development and gene expression in wS1 remains poorly understood. We assembled a transcriptomic atlas of wS1 during postnatal development comprising 45 molecularly distinct neuronal types that can be grouped into eight excitatory and four inhibitory neuron subclasses. Between postnatal day (P) 12, the onset of active whisking, and P22, when classical critical periods close, ~ 250 genes were regulated in a neuronal subclass-specific fashion when whisker experience was normal. At the resolution of neuronal types, only the composition of layer (L) 2/3 glutamatergic neurons, but not other neuronal types, changed substantially between P12 and P22. These postnatal compositional changes in L2/3 neuronal types resemble those observed previously in the primary visual cortex (V1), and the temporal gene expression changes were also highly conserved between the regions. Unlike V1, however, cell type maturation in wS1 is not substantially dependent on sensory experience, as 10-day full-face whisker deprivation from P12 to P22 did not influence the transcriptomic identity nor composition of L2/3 neuronal types. A one-day competitive whisker deprivation protocol from P21 to P22 also did not affect cell type identity but induced moderate changes in plasticity-related gene expression. Thus, developmental maturation of cell types is similar in V1 and wS1, but sensory deprivation minimally affects cell type development in wS1.

出生后须皮层神经元细胞类型发育和可塑性的分子状态。
小鼠须体感觉皮层(wS1)是研究皮层神经元生理、形态和感觉编码的经验依赖可塑性的主要模型系统。然而,在wS1中,感觉体验在调节神经元细胞类型发育和基因表达中的作用仍然知之甚少。我们组装了出生后发育过程中wS1的转录组图谱,包括45种分子上不同的神经元类型,可分为8个兴奋性神经元亚类和4个抑制性神经元亚类。在出生后第12天(即活性须形成的开始)和第22天(即经典关键时期结束)之间,当须形成正常时,约250个基因以神经元亚类特异性方式受到调控。在神经元类型上,P12和P22之间只有(L) 2/3层谷氨酸能神经元的组成有明显变化,而其他神经元类型没有明显变化。这些出生后L2/3神经元类型的变化与先前在初级视觉皮层(V1)中观察到的相似,并且时间基因表达的变化在区域之间也高度保守。然而,与V1不同的是,wS1中的细胞类型成熟并不完全依赖于感官体验,因为从P12到P22的10天全面须剥夺并不影响L2/3神经元类型的转录组特性和组成。从P21到P22为期一天的竞争性须剥夺方案也不影响细胞类型识别,但诱导可塑性相关基因表达的适度变化。因此,V1和wS1中细胞类型的发育成熟相似,但感觉剥夺对wS1中细胞类型发育的影响最小。
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 Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
×
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