Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells

Summary: Parsing diverse nerve cells into biological types is necessary for understanding neural circuit organization. Morphology is an intuitive criterion for neuronal classification and a proxy of connectivity, but morphological diversity and variability often preclude resolving the granularity of...

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Main Authors: Xiaojun Wang, Jason Tucciarone, Siqi Jiang, Fangfang Yin, Bor-Shuen Wang, Dingkang Wang, Yao Jia, Xueyan Jia, Yuxin Li, Tao Yang, Zhengchao Xu, Masood A. Akram, Yusu Wang, Shaoqun Zeng, Giorgio A. Ascoli, Partha Mitra, Hui Gong, Qingming Luo, Z. Josh Huang
Format: Article
Language:English
Published: Elsevier 2019-03-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124719302116
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author Xiaojun Wang
Jason Tucciarone
Siqi Jiang
Fangfang Yin
Bor-Shuen Wang
Dingkang Wang
Yao Jia
Xueyan Jia
Yuxin Li
Tao Yang
Zhengchao Xu
Masood A. Akram
Yusu Wang
Shaoqun Zeng
Giorgio A. Ascoli
Partha Mitra
Hui Gong
Qingming Luo
Z. Josh Huang
spellingShingle Xiaojun Wang
Jason Tucciarone
Siqi Jiang
Fangfang Yin
Bor-Shuen Wang
Dingkang Wang
Yao Jia
Xueyan Jia
Yuxin Li
Tao Yang
Zhengchao Xu
Masood A. Akram
Yusu Wang
Shaoqun Zeng
Giorgio A. Ascoli
Partha Mitra
Hui Gong
Qingming Luo
Z. Josh Huang
Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
Cell Reports
author_facet Xiaojun Wang
Jason Tucciarone
Siqi Jiang
Fangfang Yin
Bor-Shuen Wang
Dingkang Wang
Yao Jia
Xueyan Jia
Yuxin Li
Tao Yang
Zhengchao Xu
Masood A. Akram
Yusu Wang
Shaoqun Zeng
Giorgio A. Ascoli
Partha Mitra
Hui Gong
Qingming Luo
Z. Josh Huang
author_sort Xiaojun Wang
title Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
title_short Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
title_full Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
title_fullStr Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
title_full_unstemmed Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic Cells
title_sort genetic single neuron anatomy reveals fine granularity of cortical axo-axonic cells
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2019-03-01
description Summary: Parsing diverse nerve cells into biological types is necessary for understanding neural circuit organization. Morphology is an intuitive criterion for neuronal classification and a proxy of connectivity, but morphological diversity and variability often preclude resolving the granularity of neuron types. Combining genetic labeling with high-resolution, large-volume light microscopy, we established a single neuron anatomy platform that resolves, registers, and quantifies complete neuron morphologies in the mouse brain. We discovered that cortical axo-axonic cells (AACs), a cardinal GABAergic interneuron type that controls pyramidal neuron (PyN) spiking at axon initial segments, consist of multiple subtypes distinguished by highly laminar-specific soma position and dendritic and axonal arborization patterns. Whereas the laminar arrangements of AAC dendrites reflect differential recruitment by input streams, the laminar distribution and local geometry of AAC axons enable differential innervation of PyN ensembles. This platform will facilitate genetically targeted, high-resolution, and scalable single neuron anatomy in the mouse brain. : Wang et al. combine mouse genetic labeling with high-resolution, large-volume light microscopy and establish a single-neuron anatomy platform. They show that cortical axo-axonic cells, a GABAergic interneuron type that innervates pyramidal neurons at axon initial segments, consist of multiple subtypes distinguished by laminar position and dendritic and axonal arborization. Keywords: GABAergic interneurons, axo-axonic cells, AACs, chandelier cells, ChCs, neuron subtypes, genetic single neuron anatomy, gSNA, fMOST
url http://www.sciencedirect.com/science/article/pii/S2211124719302116
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spelling doaj-ebd051a4601c4e17886da4bcff03cf4d2020-11-25T01:28:27ZengElsevierCell Reports2211-12472019-03-01261131453159.e5Genetic Single Neuron Anatomy Reveals Fine Granularity of Cortical Axo-Axonic CellsXiaojun Wang0Jason Tucciarone1Siqi Jiang2Fangfang Yin3Bor-Shuen Wang4Dingkang Wang5Yao Jia6Xueyan Jia7Yuxin Li8Tao Yang9Zhengchao Xu10Masood A. Akram11Yusu Wang12Shaoqun Zeng13Giorgio A. Ascoli14Partha Mitra15Hui Gong16Qingming Luo17Z. Josh Huang18Britton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Program in Neuroscience and Medical Scientist Training Program, Stony Brook University, Stony Brook, NY 11790, USABritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USAComputer Science and Engineering Department, The Ohio State University, Columbus, OH 43221, USABritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaCenter for Neural Informatics, Structures, and Plasticity, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA, USAComputer Science and Engineering Department, The Ohio State University, Columbus, OH 43221, USABritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaCenter for Neural Informatics, Structures, and Plasticity, Krasnow Institute for Advanced Study, George Mason University, Fairfax, VA, USACold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USABritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, ChinaBritton Chance Center for Biomedical Photonics, Wuhan National Laboratory for Optoelectronics-Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; MoE Key Laboratory for Biomedical Photonics, Collaborative Innovation Center for Biomedical Engineering, School of Engineering Sciences, Huazhong University of Science and Technology, Wuhan, Hubei 430074, China; Corresponding authorCold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA; Corresponding authorSummary: Parsing diverse nerve cells into biological types is necessary for understanding neural circuit organization. Morphology is an intuitive criterion for neuronal classification and a proxy of connectivity, but morphological diversity and variability often preclude resolving the granularity of neuron types. Combining genetic labeling with high-resolution, large-volume light microscopy, we established a single neuron anatomy platform that resolves, registers, and quantifies complete neuron morphologies in the mouse brain. We discovered that cortical axo-axonic cells (AACs), a cardinal GABAergic interneuron type that controls pyramidal neuron (PyN) spiking at axon initial segments, consist of multiple subtypes distinguished by highly laminar-specific soma position and dendritic and axonal arborization patterns. Whereas the laminar arrangements of AAC dendrites reflect differential recruitment by input streams, the laminar distribution and local geometry of AAC axons enable differential innervation of PyN ensembles. This platform will facilitate genetically targeted, high-resolution, and scalable single neuron anatomy in the mouse brain. : Wang et al. combine mouse genetic labeling with high-resolution, large-volume light microscopy and establish a single-neuron anatomy platform. They show that cortical axo-axonic cells, a GABAergic interneuron type that innervates pyramidal neurons at axon initial segments, consist of multiple subtypes distinguished by laminar position and dendritic and axonal arborization. Keywords: GABAergic interneurons, axo-axonic cells, AACs, chandelier cells, ChCs, neuron subtypes, genetic single neuron anatomy, gSNA, fMOSThttp://www.sciencedirect.com/science/article/pii/S2211124719302116