Primate preoptic neurons drive hypothermia and cold defense

Maintaining body temperature within a narrow range is vital for warm-blooded animals. In rodents, the preoptic area (POA) of the hypothalamus detects and regulates core body temperature. However, knowledge about the thermal regulation center in primates remains limited. Here, we show that activating...

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Main Authors: Zhiting Zhang, Liang Shan, Yuyin Wang, Wenfang Li, Minqing Jiang, Feng Liang, Shijing Feng, Zhonghua Lu, Hong Wang, Ji Dai
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:The Innovation
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2666675822001540
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author Zhiting Zhang
Liang Shan
Yuyin Wang
Wenfang Li
Minqing Jiang
Feng Liang
Shijing Feng
Zhonghua Lu
Hong Wang
Ji Dai
author_facet Zhiting Zhang
Liang Shan
Yuyin Wang
Wenfang Li
Minqing Jiang
Feng Liang
Shijing Feng
Zhonghua Lu
Hong Wang
Ji Dai
author_sort Zhiting Zhang
collection DOAJ
description Maintaining body temperature within a narrow range is vital for warm-blooded animals. In rodents, the preoptic area (POA) of the hypothalamus detects and regulates core body temperature. However, knowledge about the thermal regulation center in primates remains limited. Here, we show that activating a subpopulation of POA neurons by a chemogenetic strategy reliably induces hypothermia in anesthetized and freely moving macaques. Comprehensive monitoring of physiological parameters reveals that such hypothermia is accompanied by autonomic changes including a rise in heart rate, skeletal muscle activity, and correlated biomarkers in blood. Consistent with enhanced ambulatory movement during hypothermia, the animals show a full range of cold-defense behaviors. Resting-state fMRI confirms the chemogenetic activation of POA and charts a brain-wide network of thermoregulation. Altogether, our findings demonstrate the central regulation of body temperature in primates and pave the way for future application in clinical practice.
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spelling doaj.art-14d41c19579948aa919e8aee022d6ef52022-12-22T03:54:52ZengElsevierThe Innovation2666-67582023-01-0141100358Primate preoptic neurons drive hypothermia and cold defenseZhiting Zhang0Liang Shan1Yuyin Wang2Wenfang Li3Minqing Jiang4Feng Liang5Shijing Feng6Zhonghua Lu7Hong Wang8Ji Dai9CAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shenzhen Technological Research Center for Primate Translational Medicine, Shenzhen 518055, ChinaCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shenzhen Key Laboratory of Drug Addiction, Shenzhen 518055, China; Corresponding authorCAS Key Laboratory of Brain Connectome and Manipulation, the Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Shenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research Institutions, Shenzhen 518055, China; University of Chinese Academy of Sciences, Beijing 100049, China; Shenzhen Technological Research Center for Primate Translational Medicine, Shenzhen 518055, China; Corresponding authorMaintaining body temperature within a narrow range is vital for warm-blooded animals. In rodents, the preoptic area (POA) of the hypothalamus detects and regulates core body temperature. However, knowledge about the thermal regulation center in primates remains limited. Here, we show that activating a subpopulation of POA neurons by a chemogenetic strategy reliably induces hypothermia in anesthetized and freely moving macaques. Comprehensive monitoring of physiological parameters reveals that such hypothermia is accompanied by autonomic changes including a rise in heart rate, skeletal muscle activity, and correlated biomarkers in blood. Consistent with enhanced ambulatory movement during hypothermia, the animals show a full range of cold-defense behaviors. Resting-state fMRI confirms the chemogenetic activation of POA and charts a brain-wide network of thermoregulation. Altogether, our findings demonstrate the central regulation of body temperature in primates and pave the way for future application in clinical practice.http://www.sciencedirect.com/science/article/pii/S2666675822001540hypothermiamacaquecentral thermoregulationpreoptic areachemogenetics
spellingShingle Zhiting Zhang
Liang Shan
Yuyin Wang
Wenfang Li
Minqing Jiang
Feng Liang
Shijing Feng
Zhonghua Lu
Hong Wang
Ji Dai
Primate preoptic neurons drive hypothermia and cold defense
The Innovation
hypothermia
macaque
central thermoregulation
preoptic area
chemogenetics
title Primate preoptic neurons drive hypothermia and cold defense
title_full Primate preoptic neurons drive hypothermia and cold defense
title_fullStr Primate preoptic neurons drive hypothermia and cold defense
title_full_unstemmed Primate preoptic neurons drive hypothermia and cold defense
title_short Primate preoptic neurons drive hypothermia and cold defense
title_sort primate preoptic neurons drive hypothermia and cold defense
topic hypothermia
macaque
central thermoregulation
preoptic area
chemogenetics
url http://www.sciencedirect.com/science/article/pii/S2666675822001540
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AT liangshan primatepreopticneuronsdrivehypothermiaandcolddefense
AT yuyinwang primatepreopticneuronsdrivehypothermiaandcolddefense
AT wenfangli primatepreopticneuronsdrivehypothermiaandcolddefense
AT minqingjiang primatepreopticneuronsdrivehypothermiaandcolddefense
AT fengliang primatepreopticneuronsdrivehypothermiaandcolddefense
AT shijingfeng primatepreopticneuronsdrivehypothermiaandcolddefense
AT zhonghualu primatepreopticneuronsdrivehypothermiaandcolddefense
AT hongwang primatepreopticneuronsdrivehypothermiaandcolddefense
AT jidai primatepreopticneuronsdrivehypothermiaandcolddefense