Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys

Tingting Bo; Jie Li; Ganlu Hu; Ge Zhang; Wei Wang; Qian Lv; Shaoling Zhao; Junjie Ma; Meng Qin; Xiaohui Yao; Meiyun Wang; Guang-Zhong Wang; Zheng Wang

doi:10.1038/s41467-023-37246-w

Brain-wide and cell-specific transcriptomic insights into MRI-derived cortical morphology in macaque monkeys

Nat Commun. 2023 Mar 17;14(1):1499. doi: 10.1038/s41467-023-37246-w.

Authors

Tingting Bo^#^{1

2

3}, Jie Li^#⁴, Ganlu Hu⁵, Ge Zhang⁶, Wei Wang⁴, Qian Lv⁷, Shaoling Zhao^{8

9}, Junjie Ma⁴, Meng Qin¹⁰, Xiaohui Yao^{11

12}, Meiyun Wang¹³, Guang-Zhong Wang¹⁴, Zheng Wang^{15

16}

Affiliations

¹ Department of Endocrine and Metabolic Diseases, Shanghai Institute of Endocrine and Metabolic Diseases, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
² Department of Radiology, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
³ Clinical Neuroscience Center, Ruijin Hospital Luwan Branch, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
⁴ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai, China.
⁵ Shanghai Institute for Advanced Immunochemical Studies, ShanghaiTech University, Shanghai, China.
⁶ Department of Medical Imaging, Henan Provincial People's Hospital & the People's Hospital of Zhengzhou University, No. 7 Weiwu Road, Zhengzhou, Henan, China.
⁷ School of Psychological and Cognitive Sciences; Beijing Key Laboratory of Behavior and Mental Health; IDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China.
⁸ Institute of Neuroscience, CAS Center for Excellence in Brain Science and Intelligence Technology, State Key Laboratory of Neuroscience, Chinese Academy of Sciences, Shanghai, China.
⁹ University of Chinese Academy of Sciences, Beijing, China.
¹⁰ College of Life Science and Technology, Beijing University of Chemical Technology, Beijing, China.
¹¹ Qingdao Innovation and Development Center, Harbin Engineering University, Qingdao, Shandong, China.
¹² College of Intelligent Systems Science and Engineering, Harbin Engineering University, Harbin, Heilongjiang, China.
¹³ Department of Medical Imaging, Henan Provincial People's Hospital & the People's Hospital of Zhengzhou University, No. 7 Weiwu Road, Zhengzhou, Henan, China. [email protected].
¹⁴ CAS Key Laboratory of Computational Biology, Shanghai Institute of Nutrition and Health, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Shanghai, China. [email protected].
¹⁵ School of Psychological and Cognitive Sciences; Beijing Key Laboratory of Behavior and Mental Health; IDG/McGovern Institute for Brain Research; Peking-Tsinghua Center for Life Sciences, Peking University, Beijing, China. [email protected].
¹⁶ School of Biomedical Engineering, Hainan University, Haikou, Hainan, China. [email protected].

^# Contributed equally.

Abstract

Integrative analyses of transcriptomic and neuroimaging data have generated a wealth of information about biological pathways underlying regional variability in imaging-derived brain phenotypes in humans, but rarely in nonhuman primates due to the lack of a comprehensive anatomically-defined atlas of brain transcriptomics. Here we generate complementary bulk RNA-sequencing dataset of 819 samples from 110 brain regions and single-nucleus RNA-sequencing dataset, and neuroimaging data from 162 cynomolgus macaques, to examine the link between brain-wide gene expression and regional variation in morphometry. We not only observe global/regional expression profiles of macaque brain comparable to human but unravel a dorsolateral-ventromedial gradient of gene assemblies within the primate frontal lobe. Furthermore, we identify a set of 971 protein-coding and 34 non-coding genes consistently associated with cortical thickness, specially enriched for neurons and oligodendrocytes. These data provide a unique resource to investigate nonhuman primate models of human diseases and probe cross-species evolutionary mechanisms.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brain* / metabolism
Humans
Macaca fascicularis / genetics
Magnetic Resonance Imaging
Primates / genetics
RNA / metabolism
Transcriptome*

Substances

RNA