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Nature：内侧前额叶皮层从边缘前区到扣带区的长期抑制增强网络活动和反应执行

Nature：Long-range inhibition from prelimbic to cingulate areas of the medial prefrontal cortex enhances network activity and response execution

Nature 等信源发布 2024-07-10 09:00

可切换为仅中文

AbstractIt is well established that the medial prefrontal cortex (mPFC) exerts top-down control of many behaviors, but little is known regarding how cross-talk between distinct areas of the mPFC influences top-down signaling. We performed virus-mediated tracing and functional studies in male mice, homing in on GABAergic projections whose axons are located mainly in layer 1 and that connect two areas of the mPFC, namely the prelimbic area (PrL) with the cingulate area 1 and 2 (Cg1/2).

摘要众所周知，内侧前额叶皮层（mPFC）对许多行为进行自上而下的控制，但关于mPFC不同区域之间的串扰如何影响自上而下的信号传导知之甚少。我们在雄性小鼠中进行了病毒介导的追踪和功能研究，归巢于GABA能投射，其轴突主要位于第1层，并连接mPFC的两个区域，即前边缘区域（PrL）与扣带区域1和2（Cg1/2）。

We revealed the identity of the targeted neurons that comprise two distinct types of layer 1 GABAergic interneurons, namely single-bouquet cells (SBCs) and neurogliaform cells (NGFs), and propose that this connectivity links GABAergic projection neurons with cortical canonical circuits. In vitro electrophysiological and in vivo calcium imaging studies support the notion that the GABAergic projection neurons from the PrL to the Cg1/2 exert a crucial role in regulating the activity in the target area by disinhibiting layer 5 output neurons.

我们揭示了包含两种不同类型的第1层GABA能中间神经元（即单束细胞（SBC）和神经胶质细胞（NGF））的靶向神经元的身份，并提出这种连接性将GABA能投射神经元与皮质规范回路联系起来。体外电生理和体内钙成像研究支持这样的观点，即从PrL到Cg1/2的GABA能投射神经元通过去抑制第5层输出神经元在调节靶区域的活性中发挥关键作用。

Finally, we demonstrated that recruitment of these projections affects impulsivity and mechanical responsiveness, behaviors which are known to be modulated by Cg1/2 activity..

最后，我们证明了这些预测的募集会影响冲动性和机械反应性，这些行为已知会受到Cg1/2活动的调节。。

IntroductionThe medial prefrontal cortex (mPFC) exerts modulatory top-down control of diverse behaviors, including performance in attention-demanding tasks1,2 and pain processing3,4. Based on cytoarchitectonic and functional studies, the mPFC has been subdivided in distinct areas, and, at least for some of these areas different nomenclatures have been used in rodent studies5,6,7,8.

引言内侧前额叶皮层（mPFC）对多种行为进行自上而下的调节控制，包括注意力要求任务1,2和疼痛处理3,4的表现。基于细胞结构和功能研究，mPFC被细分为不同的区域，至少对于其中一些区域，啮齿动物研究中使用了不同的命名法5,6,7,8。

In our study we homed in on specific GABAergic projections which in rodents connect the prelimbic (PrL) with the cingulate areas 1/2 (Cg1/2)9. The latter is part of the anterior cingulate cortex often referred to as area 24 in primates7,8. Notably, there is dense interconnectivity between these and other areas of the mPFC10.Given the abundant interconnectivity between mPFC areas, it can be inferred that mPFC areas interact with each other and together shape the net effect of top-down signaling.

在我们的研究中，我们专注于特定的GABA能投射，这些投射在啮齿动物中将前边缘（PrL）与扣带回区域1/2（Cg1/2）9联系起来。后者是前扣带皮层的一部分，通常在灵长类动物中被称为24区7,8。值得注意的是，mPFC10的这些区域与其他区域之间存在密集的互连。鉴于mPFC区域之间存在丰富的互连性，可以推断mPFC区域相互作用，并共同形成自上而下信号的净效应。

However, the precise nature of this cross-talk between different mPFC areas is largely unknown. Consistent with such a scenario, recruitment of glutamatergic projections from the PrL to the Cg1/2 attenuates pain-like behavior in mice11. In this study, the authors showed that PrL excitatory projections innervated preferentially inhibitory γ-aminobutyric acid-releasing interneurons (GABAergic INs) in the Cg1/2 thereby reducing neuronal activity in the target area.

然而，不同mPFC区域之间这种串扰的确切性质在很大程度上是未知的。与这种情况一致，从PrL到Cg1/2的谷氨酸能投射的募集减弱了小鼠的疼痛样行为11。在这项研究中，作者表明，PrL兴奋性投射优先支配Cg1/2中抑制性γ-氨基丁酸释放的中间神经元（GABA能INs），从而降低目标区域的神经元活性。

This prompts the question whether another projection between these areas supports the opposite effect, and if so, what is the mechanism thereof.GABAergic projection neurons are excellent candidates to subserve this role as they are ideally positioned to exert control on neuronal activity in distantly located brain areas for two reasons.

这引发了一个问题，即这些区域之间的另一个投影是否支持相反的效果，如果是，其机制是什么。GABA能投射神经元是维持这一作用的优秀候选者，因为它们处于理想的位置，可以控制远处大脑区域的神经元活动，原因有两个。

Firstly, there is ample anatomical evidence for uni- and bidirectional cortico-cortical GABAergic projections.

首先，有足够的解剖学证据表明单皮质和双向皮质GABA能投射。

Data availability

数据可用性

The data generated in this study are provided in the Source Data file. Raw imaging data are available on request from the corresponding author because of the large size of data. Source data are provided with this paper.

本研究中生成的数据在源数据文件中提供。由于数据量大，可以根据通讯作者的要求提供原始成像数据。本文提供了源数据。

Code availability

代码可用性

Our code is available in the following repository. For electrophysiology, https://github.com/Yu-Chao-Liu/HEKAexport or https://zenodo.org/records/687779293, https://github.com/Yu-Chao-Liu/IntrinsicProperties or https://zenodo.org/records/1070098694, https://github.com/Yu-Chao-Liu/Intersections or https://zenodo.org/records/1070243295.

我们的代码可在以下存储库中找到。对于电生理学，https://github.com/Yu-Chao-Liu/HEKAexport或https://zenodo.org/records/687779293，https://github.com/Yu-Chao-Liu/IntrinsicProperties或https://zenodo.org/records/1070098694，https://github.com/Yu-Chao-Liu/Intersections或https://zenodo.org/records/1070243295.

For the other experiments, https://github.com/NUtaHei/Utashiro_NatCommun2024, or https://zenodo.org/records/1071007696..

对于其他实验，https://github.com/NUtaHei/Utashiro_NatCommun2024https://zenodo.org/records/1071007696..

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Github. https://zenodo.org/records/10710076 (2024).Download referencesAcknowledgementsWe thank Drs. Linette Liqi Tan and Rohini Kuner for giving advice with the behavioral evaluation of the nociceptive response, Ulrike Amtmann for preparing solutions for the electrophysiological experiments, and Dr.

Github。https://zenodo.org/records/10710076（2024年）。下载参考文献致谢我们感谢Linette Liqi Tan博士和Rohini Kuner博士就伤害性反应的行为评估提供建议，感谢Ulrike Amtmann为电生理实验准备解决方案，感谢Dr。

Elke Fuchs for helping with the animal license (G-157/16, G-131/19). We thank and acknowledge the staff and services offered by the Light Microscopy Facility at the DKFZ. The project was funded in part by SFB1158 grant (project B06) from the Deutsche Forschungsgemeinschaft (DFG) to H.M.FundingOpen Access funding enabled and organized by Projekt DEAL.Author informationAuthor notesKaneschka YaqubiPresent address: Department of Gastroenterology, Hepatology and Infectious Diseases, University Hospital Düsseldorf and Medical Faculty of Heinrich Heine University Düsseldorf, Düsseldorf, GermanyBirgit WojakPresent address: Department of Internal Medicine III, University Hospital Ulm, Ulm, GermanyThese authors contributed equally: Nao Utashiro, Duncan Archibald Allan MacLaren, Yu-Chao Liu.Authors and AffiliationsDepartment of Clinical Neurobiology at the Medical Faculty of the Heidelberg University and of the German Cancer Research Center (DKFZ), Heidelberg, GermanyNao Utashiro, Duncan Archibald Allan MacLaren, Yu-Chao Liu, Kaneschka Yaqubi, Birgit Wojak & Hannah MonyerAuthorsNao UtashiroView author .

Elke Fuchs帮助办理动物许可证（G-157/16，G-131/19）。我们感谢并感谢DKFZ光学显微镜设施提供的工作人员和服务。该项目的部分资金来自德国科学基金会（DFG）的SFB1158赠款（项目B06），由H.M.FundingOpen Access资助，由Projekt DEAL启用和组织。作者信息作者notesKaneschka Yaqubpresent地址：德国杜塞尔多夫杜塞尔多夫大学医院消化内科，肝病学和传染病系以及德国杜塞尔多夫杜塞尔多夫海因里希海涅大学医学院目前地址：德国乌尔姆大学医院内科III这些作者做出了同样的贡献：Nao Utashiro，Duncan Bald Allan MacLaren，Yu Chao Liu。作者和附属机构海德堡大学医学院和德国癌症研究中心（DKFZ）临床神经生物学系，海德堡，GermanyNao Utashiro，Duncan Archibald Allan MacLaren，Yu Chao Liu，Kaneschka Yaqubi，Birgit Wojak＆Hannah MonyerAuthorsNao UtashiroView作者。

PubMed Google ScholarDuncan Archibald Allan MacLarenView author publicationsYou can also search for this author in

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PubMed Google ScholarYu Chao Liu查看作者出版物您也可以在

PubMed Google ScholarKaneschka YaqubiView author publicationsYou can also search for this author in

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PubMed Google ScholarContributionsThe project was coordinated by H.M. The virus-tracing experiments were executed by K.Y., N.U. and B.W. The in vitro electrophysiological experiments were performed by Y.-C.L. The behavioral studies were performed by K.Y. and D.A.A.M. The calcium imaging experiments were performed by N.U.

PubMed谷歌学术贡献该项目由H.M.协调。病毒追踪实验由K.Y.，N.U.和B.W.进行。体外电生理实验由Y.-C.L.进行。行为研究由K.Y.和D.A.A.M.进行。钙成像实验由N.U.进行。

The manuscript was written by N.U., D.A.A.M. and H.M. with the contribution of the other authors.Corresponding authorCorrespondence to.

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Reprints and permissionsAbout this articleCite this articleUtashiro, N., MacLaren, D.A.A., Liu, YC. et al. Long-range inhibition from prelimbic to cingulate areas of the medial prefrontal cortex enhances network activity and response execution.

转载和许可本文引用本文Utashiro，N.，MacLaren，D.A.A.，Liu，YC。从内侧前额叶皮层的前肢到扣带回区域的远程抑制增强了网络活动和反应执行。

Nat Commun 15, 5772 (2024). https://doi.org/10.1038/s41467-024-50055-zDownload citationReceived: 16 June 2023Accepted: 28 June 2024Published: 10 July 2024DOI: https://doi.org/10.1038/s41467-024-50055-zShare this articleAnyone you share the following link with will be able to read this content:Get shareable linkSorry, a shareable link is not currently available for this article.Copy to clipboard.

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