Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism

IntroductionForebrain neural networks are vital for cognitive functioning, and their excitatory-inhibitory (E-I) balance is governed by neural homeostasis. However, the homeostatic control strategies and transcriptomic mechanisms that maintain forebrain E-I balance and optimal cognition remain uncle...

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Main Authors: Tian Tian, You Cai, Xin Qin, Jiangang Wang, Yali Wang, Xin Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-02-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fncel.2023.1114037/full
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author Tian Tian
You Cai
You Cai
Xin Qin
Jiangang Wang
Yali Wang
Xin Yang
author_facet Tian Tian
You Cai
You Cai
Xin Qin
Jiangang Wang
Yali Wang
Xin Yang
author_sort Tian Tian
collection DOAJ
description IntroductionForebrain neural networks are vital for cognitive functioning, and their excitatory-inhibitory (E-I) balance is governed by neural homeostasis. However, the homeostatic control strategies and transcriptomic mechanisms that maintain forebrain E-I balance and optimal cognition remain unclear.MethodsWe used patch-clamp and RNA sequencing to investigate the patterns of neural network homeostasis with suppressing forebrain excitatory neural activity and spatial training.ResultsWe found that inhibitory transmission and receptor transcription were reduced in tamoxifen-inducible Kir2.1 conditional knock-in mice. In contrast, spatial training increased inhibitory synaptic connections and the transcription of inhibitory receptors.DiscussionOur study provides significant evidence that inhibitory systems play a critical role in the homeostatic control of the E-I balance in the forebrain during cognitive training and E-I rebalance, and we have provided insights into multiple gene candidates for cognition-related homeostasis in the forebrain.
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spelling doaj.art-6c06ec3aa7c74cb287f4e3058d757e672023-02-24T14:33:26ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022023-02-011710.3389/fncel.2023.11140371114037Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanismTian Tian0You Cai1You Cai2Xin Qin3Jiangang Wang4Yali Wang5Xin Yang6Shenzhen Key Laboratory of Translational Research for Brain Diseases, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaShenzhen Key Laboratory of Translational Research for Brain Diseases, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaDepartment of Neurology, Shenzhen Institute of Translational Medicine, Shenzhen Second People’s Hospital, The First Affiliated Hospital of Shenzhen University, Shenzhen, ChinaDepartment of Medicine, Djavad Mowafaghian Centre for Brain Health, The University of British Columbia, Vancouver, BC, CanadaHenan International Joint Laboratory of Non-Invasive Neuromodulation, Department of Physiology and Pathophysiology, Xinxiang Medical University, Xinxiang, ChinaHenan International Joint Laboratory of Non-Invasive Neuromodulation, Department of Physiology and Pathophysiology, Xinxiang Medical University, Xinxiang, ChinaShenzhen Key Laboratory of Translational Research for Brain Diseases, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, Shenzhen, ChinaIntroductionForebrain neural networks are vital for cognitive functioning, and their excitatory-inhibitory (E-I) balance is governed by neural homeostasis. However, the homeostatic control strategies and transcriptomic mechanisms that maintain forebrain E-I balance and optimal cognition remain unclear.MethodsWe used patch-clamp and RNA sequencing to investigate the patterns of neural network homeostasis with suppressing forebrain excitatory neural activity and spatial training.ResultsWe found that inhibitory transmission and receptor transcription were reduced in tamoxifen-inducible Kir2.1 conditional knock-in mice. In contrast, spatial training increased inhibitory synaptic connections and the transcription of inhibitory receptors.DiscussionOur study provides significant evidence that inhibitory systems play a critical role in the homeostatic control of the E-I balance in the forebrain during cognitive training and E-I rebalance, and we have provided insights into multiple gene candidates for cognition-related homeostasis in the forebrain.https://www.frontiersin.org/articles/10.3389/fncel.2023.1114037/fullhomeostasisGABAforebraincognitionE-I balance significance statement
spellingShingle Tian Tian
You Cai
You Cai
Xin Qin
Jiangang Wang
Yali Wang
Xin Yang
Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
Frontiers in Cellular Neuroscience
homeostasis
GABA
forebrain
cognition
E-I balance significance statement
title Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
title_full Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
title_fullStr Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
title_full_unstemmed Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
title_short Forebrain E-I balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
title_sort forebrain e i balance controlled in cognition through coordinated inhibition and inhibitory transcriptome mechanism
topic homeostasis
GABA
forebrain
cognition
E-I balance significance statement
url https://www.frontiersin.org/articles/10.3389/fncel.2023.1114037/full
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AT youcai forebraineibalancecontrolledincognitionthroughcoordinatedinhibitionandinhibitorytranscriptomemechanism
AT xinqin forebraineibalancecontrolledincognitionthroughcoordinatedinhibitionandinhibitorytranscriptomemechanism
AT jiangangwang forebraineibalancecontrolledincognitionthroughcoordinatedinhibitionandinhibitorytranscriptomemechanism
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