Generation of a whole-brain atlas for the cholinergic system and mesoscopic projectome analysis of basal forebrain cholinergic neurons

被引:224
作者
Li, Xiangning [1 ,2 ]
Yu, Bin [3 ,4 ]
Sun, Qingtao [1 ]
Zhang, Yalun [1 ]
Ren, Miao [1 ]
Zhang, Xiaoyan [1 ]
Li, Anan [1 ,2 ]
Yuan, Jing [1 ]
Madisen, Linda [5 ]
Luo, Qingming [1 ,2 ]
Zeng, Hongkui [5 ]
Gong, Hui [1 ,2 ]
Qiu, Zilong [2 ,3 ]
机构
[1] Huazhong Univ Sci & Technol, Minist Educ, Key Lab Biomed Photon, Sch Engn Sci,Wuhan Natl Lab Optoelect,Britton Chan, Wuhan 430074, Hubei, Peoples R China
[2] Chinese Acad Sci, Ctr Excellence Brain Sci & Intelligence Technol, Shanghai 200031, Peoples R China
[3] Chinese Acad Sci, State Key Lab Neurosci, Inst Neurosci, Shanghai 200031, Peoples R China
[4] Univ Chinese Acad Sci, Beijing 100049, Peoples R China
[5] Allen Inst Brain Sci, Washington, DC 98103 USA
基金
中国国家自然科学基金;
关键词
cholinergic neurons; tomography; whole-brain imaging basal forebrain; single neuron reconstruction; MOUSE-BRAIN; IMMUNOCYTOCHEMICAL LOCALIZATION; CORTEX; ACETYLTRANSFERASE; TOMOGRAPHY; COGNITION; SLEEP;
D O I
10.1073/pnas.1703601115
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The cholinergic system in the brain plays crucial roles in regulating sensory and motor functions as well as cognitive behaviors by modulating neuronal activity. Understanding the organization of the cholinergic system requires a complete map of cholinergic neurons and their axon arborizations throughout the entire brain at the level of single neurons. Here, we report a comprehensive whole-brain atlas of the cholinergic system originating from various cortical and subcortical regions of the mouse brain. Using genetically labeled cholinergic neurons together with whole-brain reconstruction of optical images at 2-mu m resolution, we obtained quantification of the number and soma volume of cholinergic neurons in 22 brain areas. Furthermore, by reconstructing the complete axonal arbors of fluorescently labeled single neurons from a subregion of the basal forebrain at 1-pm resolution, we found that their projections to the forebrain and midbrain showed neuronal subgroups with distinct projection specificity and diverse arbor distribution within the same projection area. These results suggest the existence of distinct subtypes of cholinergic neurons that serve different regulatory functions in the brain and illustrate the usefulness of complete reconstruction of neuronal distribution and axon projections at the mesoscopic level.
引用
收藏
页码:415 / 420
页数:6
相关论文
共 35 条
[1]   DISTRIBUTION OF CHOLINERGIC NEURONS IN RAT-BRAIN - DEMONSTRATED BY THE IMMUNOCYTOCHEMICAL LOCALIZATION OF CHOLINE-ACETYLTRANSFERASE [J].
ARMSTRONG, DM ;
SAPER, CB ;
LEVEY, AI ;
WAINER, BH ;
TERRY, RD .
JOURNAL OF COMPARATIVE NEUROLOGY, 1983, 216 (01) :53-68
[2]   Two-dimensional versus three-dimensional cell counting: a practical perspective [J].
Benes, FM ;
Lange, N .
TRENDS IN NEUROSCIENCES, 2001, 24 (01) :11-17
[3]   Topographic Mapping between Basal Forebrain Cholinergic Neurons and the Medial Prefrontal Cortex in Mice [J].
Bloem, Bernard ;
Schoppink, Luc ;
Rotaru, Diana C. ;
Faiz, Amu ;
Hendriks, Patrick ;
Mansvelder, Huibert D. ;
de Berg, Wilma D. J. van ;
Wouterlood, Floris G. .
JOURNAL OF NEUROSCIENCE, 2014, 34 (49) :16234-16246
[4]   Thalamic projections sustain prefrontal activity during working memory maintenance [J].
Bolkan, Scott S. ;
Stujenske, Joseph M. ;
Parnaudeau, Sebastien ;
Spellman, Timothy J. ;
Rauffenbart, Caroline ;
Abbas, Atheir I. ;
Harris, Alexander Z. ;
Gordon, Joshua A. ;
Kellendonk, Christoph .
NATURE NEUROSCIENCE, 2017, 20 (07) :987-+
[5]   Revisiting the cholinergic in the development of Alzheimer's disease [J].
Craig, Laura A. ;
Hong, Nancy S. ;
McDonald, Robert J. .
NEUROSCIENCE AND BIOBEHAVIORAL REVIEWS, 2011, 35 (06) :1397-1409
[6]  
Dong H.W., 2008, The Allen Reference Atlas, (Book + CD-ROM): A Digital Color Brain Atlas of the C57BL/6J Male Mouse
[7]   Central cholinergic systems and cognition [J].
Everitt, BJ ;
Robbins, TW .
ANNUAL REVIEW OF PSYCHOLOGY, 1997, 48 :649-684
[8]   Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? [J].
Fanselow, Michael S. ;
Dong, Hong-Wei .
NEURON, 2010, 65 (01) :7-19
[9]   The Input-Output Relationship of the Cholinergic Basal Forebrain [J].
Gielow, Matthew R. ;
Zaborszky, Laszlo .
CELL REPORTS, 2017, 18 (07) :1817-1830
[10]   High-throughput dual-colour precision imaging for brain-wide connectome with cytoarchitectonic landmarks at the cellular level [J].
Gong, Hui ;
Xu, Dongli ;
Yuan, Jing ;
Li, Xiangning ;
Guo, Congdi ;
Peng, Jie ;
Li, Yuxin ;
Schwarz, Lindsay A. ;
Li, Anan ;
Hu, Bihe ;
Xiong, Benyi ;
Sun, Qingtao ;
Zhang, Yalun ;
Liu, Jiepeng ;
Zhong, Qiuyuan ;
Xu, Tonghui ;
Zeng, Shaoqun ;
Luo, Qingming .
NATURE COMMUNICATIONS, 2016, 7