Single-cell spatial transcriptome atlas and whole-brain connectivity of the macaque claustrum
Ying Lei, Yuxuan Liu, Mingli Wang, Nini Yuan, Yujie Hou, Lingjun Ding, Zhiyong Zhu, Zihan Wu, Chao Li, Mingyuan Zheng, Ruiyi Zhang, Ana Rita Ribeiro Gomes, Yuanfang Xu, Zhaoke Luo, Zhen Liu, Qinwen Chai, Pierre Misery, Yanqing Zhong, Xinxiang Song, Camille Lamy, Cui Wei, Qian Yu, Fang Jiao, Yingjie An, Ye Tian, Yiwen Liu, Xing Sun, Ruiqi Wang, Huanhuan Li, Jingjing Song, Xing Tan, He Wang, Shiwen Wang, Ling Han, Yong Zhang, S. D. Li, Kexin Wang, Guangling Wang, Wanqiu Zhou, Jianfeng Liu, Cong Yu, Shuzhen Zhang, Liangtang Chang, Dafina Toplanaj, Mengni Chen, Jiabing Liu, Yun Zhao, Biyu Ren, Hanyu Shi, Hui Zhang, Haotian Yan, Jianyun Ma, Lina Wang, Yan Li, Yichen Zuo, Linjie Lu, Liqin Gu, Shuting Li, Yaqian Wang, Y. He, Shengkang Li, Qi Zhang, Yanbing Lu, Yannong Dou, Yuan Liu, Anqi Zhao, Minyuan Zhang, Xinyan Zhang, Ying Xia, Wei Zhang, Huateng Cao, Zhiyue Lu, Zixian Yu, Xin Li, Xiaofei Wang, Zhifeng Liang, Shengjin Xu, Cirong Liu, Changhong Zheng, Chun Xu, Zhiyong Liu, Chengyu Li, Yan-Gang Sun, Xun Xu, Colette Dehay, Julien Vezoli, Mu‐ming Poo, Jianhua Yao, Longqi Liu, Wei Wu, Henry Kennedy, Zhiming Shen
Abstract
Claustrum orchestrates brain functions via its connections with numerous brain regions, but its molecular and cellular organization remains unresolved. Single-nucleus RNA sequencing of 227,750 macaque claustral cells identified 48 transcriptome-defined cell types, with most glutamatergic neurons similar to deep-layer insular neurons. Comparison of macaque, marmoset, and mouse transcriptomes revealed macaque-specific cell types. Retrograde tracer injections at 67 cortical and 7 subcortical regions defined four distinct distribution zones of retrogradely labeled claustral neurons. Joint analysis of whole-brain connectivity and single-cell spatial transcriptome showed that these four zones containing distinct compositions of glutamatergic (but not GABAergic) cell types preferentially connected to specific brain regions with a strong ipsilateral bias. Several macaque-specific glutamatergic cell types in ventral vs. dorsal claustral zones selectively co-projected to two functionally related areas-entorhinal cortex and hippocampus vs. motor cortex and putamen, respectively. These data provide the basis for elucidating the neuronal organization underlying diverse claustral functions.