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Cell Rep. 2017 Nov 28;21(9):2407-2418. doi: 10.1016/j.celrep.2017.11.012.

Astrocytic l-Lactate Signaling Facilitates Amygdala-Anterior Cingulate Cortex Synchrony and Decision Making in Rats.

Author information

1
Department of Biomedical Sciences, College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong.
2
Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Brain Cognition and Brain Disease Institute for Collaboration Research of SIAT at CAS and the McGovern Institute at MIT, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
3
Department of Biomedical Sciences, College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong.
4
Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong; Department of Electronic Engineering, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong.
5
Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China; Brain Cognition and Brain Disease Institute for Collaboration Research of SIAT at CAS and the McGovern Institute at MIT, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China. Electronic address: lp.wang@siat.ac.cn.
6
Department of Biomedical Sciences, College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Tat Chee Avenue, Kowloon, Hong Kong; Brain Cognition and Brain Disease Institute for Collaboration Research of SIAT at CAS and the McGovern Institute at MIT, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China. Electronic address: yingli@cityu.edu.hk.

Abstract

Human brain imaging studies have revealed the anterior cingulate cortex (ACC) as a key brain region for mediating visceral-pain-cognitive interactions. Recently, we characterized impairments of long-term potentiation and spike-field coherence in the basolateral amygdala (BLA)-ACC network in association with a decision-making deficit in rats with visceral hypersensitivity (VH). Now, by combining integrative neurobiological approaches, we show that ACC-reactive astrogliosis and activity-dependent impairment of lactate release occur in VH rats. Exogenous lactate supply rescues chronic-visceral-pain-caused impairments of ACC phase locking and decision making, which can be mimicked by optogenetic activation of ACC astrocytes. Large-scale electrophysiological recordings in free-moving animals during a decision-making task indicate that optogenetic astrocytic activation improves decision-making performance and engages ACC phase locking and BLA-to-ACC information flow. Collectively, these observations support the idea of an "astrocyte-neuron l-lactate shuttle" and suggest that targeting astrocytes may help with cognitive dysfunctions under chronic visceral pain.

KEYWORDS:

anterior cingulate cortex; astrocyte; basolateral amygdala; decision making; l-lactate; neural information flow; phase locking

PMID:
29186680
DOI:
10.1016/j.celrep.2017.11.012
[Indexed for MEDLINE]
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