利用层状群体分析揭示小鼠视觉系统细胞外电位的群体贡献。

IF 3.6 2区 生物学 Q1 BIOCHEMICAL RESEARCH METHODS
PLoS Computational Biology Pub Date : 2024-12-12 eCollection Date: 2024-12-01 DOI:10.1371/journal.pcbi.1011830
Atle E Rimehaug, Anders M Dale, Anton Arkhipov, Gaute T Einevoll
{"title":"利用层状群体分析揭示小鼠视觉系统细胞外电位的群体贡献。","authors":"Atle E Rimehaug, Anders M Dale, Anton Arkhipov, Gaute T Einevoll","doi":"10.1371/journal.pcbi.1011830","DOIUrl":null,"url":null,"abstract":"<p><p>The local field potential (LFP), the low-frequency part of the extracellular potential, reflects transmembrane currents in the vicinity of the recording electrode. Thought mainly to stem from currents caused by synaptic input, it provides information about neural activity complementary to that of spikes, the output of neurons. However, the many neural sources contributing to the LFP, and likewise the derived current source density (CSD), can often make it challenging to interpret. Efforts to improve its interpretability have included the application of statistical decomposition tools like principal component analysis (PCA) and independent component analysis (ICA) to disentangle the contributions from different neural sources. However, their underlying assumptions of, respectively, orthogonality and statistical independence are not always valid for the various processes or pathways generating LFP. Here, we expand upon and validate a decomposition algorithm named Laminar Population Analysis (LPA), which is based on physiological rather than statistical assumptions. LPA utilizes the multiunit activity (MUA) and LFP jointly to uncover the contributions of different populations to the LFP. To perform the validation of LPA, we used data simulated with the large-scale, biophysically detailed model of mouse V1 developed by the Allen Institute. We find that LPA can identify laminar positions within V1 and the temporal profiles of laminar population firing rates from the MUA. We also find that LPA can estimate the salient current sinks and sources generated by feedforward input from the lateral geniculate nucleus (LGN), recurrent activity in V1, and feedback input from the lateromedial (LM) area of visual cortex. LPA identifies and distinguishes these contributions with a greater accuracy than the alternative statistical decomposition methods, PCA and ICA. The contributions from different cortical layers within V1 could however not be robustly separated and identified with LPA. This is likely due to substantial synchrony in population firing rates across layers, which may be reduced with other stimulus protocols in the future. Lastly, we also demonstrate the application of LPA on experimentally recorded MUA and LFP from 24 animals in the publicly available Visual Coding dataset. Our results suggest that LPA can be used both as a method to estimate positions of laminar populations and to uncover salient features in LFP/CSD contributions from different populations.</p>","PeriodicalId":20241,"journal":{"name":"PLoS Computational Biology","volume":"20 12","pages":"e1011830"},"PeriodicalIF":3.6000,"publicationDate":"2024-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11670981/pdf/","citationCount":"0","resultStr":"{\"title\":\"Uncovering population contributions to the extracellular potential in the mouse visual system using Laminar Population Analysis.\",\"authors\":\"Atle E Rimehaug, Anders M Dale, Anton Arkhipov, Gaute T Einevoll\",\"doi\":\"10.1371/journal.pcbi.1011830\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>The local field potential (LFP), the low-frequency part of the extracellular potential, reflects transmembrane currents in the vicinity of the recording electrode. Thought mainly to stem from currents caused by synaptic input, it provides information about neural activity complementary to that of spikes, the output of neurons. However, the many neural sources contributing to the LFP, and likewise the derived current source density (CSD), can often make it challenging to interpret. Efforts to improve its interpretability have included the application of statistical decomposition tools like principal component analysis (PCA) and independent component analysis (ICA) to disentangle the contributions from different neural sources. However, their underlying assumptions of, respectively, orthogonality and statistical independence are not always valid for the various processes or pathways generating LFP. Here, we expand upon and validate a decomposition algorithm named Laminar Population Analysis (LPA), which is based on physiological rather than statistical assumptions. LPA utilizes the multiunit activity (MUA) and LFP jointly to uncover the contributions of different populations to the LFP. To perform the validation of LPA, we used data simulated with the large-scale, biophysically detailed model of mouse V1 developed by the Allen Institute. We find that LPA can identify laminar positions within V1 and the temporal profiles of laminar population firing rates from the MUA. We also find that LPA can estimate the salient current sinks and sources generated by feedforward input from the lateral geniculate nucleus (LGN), recurrent activity in V1, and feedback input from the lateromedial (LM) area of visual cortex. LPA identifies and distinguishes these contributions with a greater accuracy than the alternative statistical decomposition methods, PCA and ICA. The contributions from different cortical layers within V1 could however not be robustly separated and identified with LPA. This is likely due to substantial synchrony in population firing rates across layers, which may be reduced with other stimulus protocols in the future. Lastly, we also demonstrate the application of LPA on experimentally recorded MUA and LFP from 24 animals in the publicly available Visual Coding dataset. Our results suggest that LPA can be used both as a method to estimate positions of laminar populations and to uncover salient features in LFP/CSD contributions from different populations.</p>\",\"PeriodicalId\":20241,\"journal\":{\"name\":\"PLoS Computational Biology\",\"volume\":\"20 12\",\"pages\":\"e1011830\"},\"PeriodicalIF\":3.6000,\"publicationDate\":\"2024-12-12\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11670981/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"PLoS Computational Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1371/journal.pcbi.1011830\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/12/1 0:00:00\",\"PubModel\":\"eCollection\",\"JCR\":\"Q1\",\"JCRName\":\"BIOCHEMICAL RESEARCH METHODS\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Computational Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pcbi.1011830","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/12/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"BIOCHEMICAL RESEARCH METHODS","Score":null,"Total":0}
引用次数: 0

摘要

局部场电位(LFP)是细胞外电位的低频部分,反映了记录电极附近的跨膜电流。人们认为 LFP 主要来源于突触输入引起的电流,它提供的神经活动信息与神经元输出的尖峰信息相辅相成。然而,由于 LFP 的神经源众多,衍生出的电流源密度(CSD)也不尽相同,因此对它的解读往往具有挑战性。为提高其可解释性所做的努力包括应用主成分分析(PCA)和独立成分分析(ICA)等统计分解工具来区分不同神经源的贡献。然而,这两种方法的基本假设,即正交性和统计独立性,并不总是适用于产生 LFP 的各种过程或通路。在此,我们扩展并验证了一种名为层状群体分析(LPA)的分解算法,该算法基于生理假设而非统计假设。LPA 联合使用多单位活动(MUA)和 LFP 来揭示不同群体对 LFP 的贡献。为了对 LPA 进行验证,我们使用了由艾伦研究所开发的大规模、生物物理详细的小鼠 V1 模型模拟的数据。我们发现,LPA 可以识别 V1 中的层状位置,并从 MUA 中识别层状群体发射率的时间曲线。我们还发现,LPA 可以估计来自外侧膝状核 (LGN) 的前馈输入、V1 中的循环活动以及来自视觉皮层侧内侧 (LM) 区域的反馈输入所产生的突出电流汇和源。与其他统计分解方法(PCA 和 ICA)相比,LPA 能更准确地识别和区分这些贡献。然而,LPA 无法稳健地分离和识别来自 V1 内不同皮层的贡献。这可能是由于各层之间的群体发射率存在很大的同步性,而这种同步性可能会在未来的其他刺激方案中有所降低。最后,我们还展示了 LPA 在实验记录的 MUA 和 LFP 上的应用,这些记录来自公开的视觉编码数据集中的 24 只动物。我们的研究结果表明,LPA 既可用作估计层状群位置的方法,也可用于发现来自不同层状群的 LFP/CSD 贡献的显著特征。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
Uncovering population contributions to the extracellular potential in the mouse visual system using Laminar Population Analysis.

The local field potential (LFP), the low-frequency part of the extracellular potential, reflects transmembrane currents in the vicinity of the recording electrode. Thought mainly to stem from currents caused by synaptic input, it provides information about neural activity complementary to that of spikes, the output of neurons. However, the many neural sources contributing to the LFP, and likewise the derived current source density (CSD), can often make it challenging to interpret. Efforts to improve its interpretability have included the application of statistical decomposition tools like principal component analysis (PCA) and independent component analysis (ICA) to disentangle the contributions from different neural sources. However, their underlying assumptions of, respectively, orthogonality and statistical independence are not always valid for the various processes or pathways generating LFP. Here, we expand upon and validate a decomposition algorithm named Laminar Population Analysis (LPA), which is based on physiological rather than statistical assumptions. LPA utilizes the multiunit activity (MUA) and LFP jointly to uncover the contributions of different populations to the LFP. To perform the validation of LPA, we used data simulated with the large-scale, biophysically detailed model of mouse V1 developed by the Allen Institute. We find that LPA can identify laminar positions within V1 and the temporal profiles of laminar population firing rates from the MUA. We also find that LPA can estimate the salient current sinks and sources generated by feedforward input from the lateral geniculate nucleus (LGN), recurrent activity in V1, and feedback input from the lateromedial (LM) area of visual cortex. LPA identifies and distinguishes these contributions with a greater accuracy than the alternative statistical decomposition methods, PCA and ICA. The contributions from different cortical layers within V1 could however not be robustly separated and identified with LPA. This is likely due to substantial synchrony in population firing rates across layers, which may be reduced with other stimulus protocols in the future. Lastly, we also demonstrate the application of LPA on experimentally recorded MUA and LFP from 24 animals in the publicly available Visual Coding dataset. Our results suggest that LPA can be used both as a method to estimate positions of laminar populations and to uncover salient features in LFP/CSD contributions from different populations.

求助全文
通过发布文献求助,成功后即可免费获取论文全文。 去求助
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:604180095
Book学术官方微信