State‐specific Regulation of Electrical Stimulation in the Intralaminar Thalamus of Macaque Monkeys: Network and Transcriptional Insights into Arousal

Author:

Zhang Zhao1ORCID,Huang Yichun2,Chen Xiaoyu3,Li Jiahui2,Yang Yi4,Lv Longbao5,Wang Jianhong5,Wang Meiyun6,Wang Yingwei1,Wang Zheng27ORCID

Affiliation:

1. Department of Anesthesiology Huashan Hospital, Fudan University 12 Urumqi Middle Rd, Jing'an District Shanghai 200040 China

2. School of Psychological and Cognitive Sciences Beijing Key Laboratory of Behavior and Mental Health State Key Laboratory of General Artificial Intelligence IDG/McGovern Institute for Brain Research Peking‐Tsinghua Center for Life Sciences Peking University 5 Yiheyuan Rd, Haidian District Beijing 100871 China

3. Institute of Natural Sciences and School of Mathematical Sciences Shanghai Jiao Tong University 800 Dongchuan RD, Minhang District Shanghai 200240 China

4. Department of Neurosurgery Brain Computer Interface Transition Research Center Beijing Tiantan Hospital Capital Medical University 119 South Fourth Ring Rd West, Fengtai District Beijing 100070 China

5. National Resource Center for Non‐Human Primates Kunming Primate Research Center National Research Facility for Phenotypic & Genetic Analysis of Model Animals (Primate Facility) Kunming Institute of Zoology Chinese Academy of Sciences 32 East of Jiaochang Rd Kunming Yunnan 650223 China

6. Department of Medical Imaging Henan Provincial People's Hospital & the People's Hospital of Zhengzhou University No. 7 Weiwu Road Zhengzhou Henan 450003 China

7. School of Biomedical Engineering Hainan University 58 Renmin Avenue Haikou Hainan 570228 China

Abstract

AbstractLong‐range thalamocortical communication is central to anesthesia‐induced loss of consciousness and its reversal. However, isolating the specific neural networks connecting thalamic nuclei with various cortical regions for state‐specific anesthesia regulation is challenging, with the biological underpinnings still largely unknown. Here, simultaneous electroencephalogram‐fuctional magnetic resonance imaging (EEG‐fMRI) and deep brain stimulation are applied to the intralaminar thalamus in macaques under finely‐tuned propofol anesthesia. This approach led to the identification of an intralaminar‐driven network responsible for rapid arousal during slow‐wave oscillations. A network‐based RNA‐sequencing analysis is conducted of region‐, layer‐, and cell‐specific gene expression data from independent transcriptomic atlases and identifies 2489 genes preferentially expressed within this arousal network, notably enriched in potassium channels and excitatory, parvalbumin‐expressing neurons, and oligodendrocytes. Comparison with human RNA‐sequencing data highlights conserved molecular and cellular architectures that enable the matching of homologous genes, protein interactions, and cell types across primates, providing novel insight into network‐focused transcriptional signatures of arousal.

Funder

National Natural Science Foundation of China

Publisher

Wiley

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