An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex

Summary: Short-term memory (STM) is crucial for animals to hold information for a small period of time. Persistent or recurrent neural activity, together with neural oscillations, is known to encode the STM at the cellular level. However, the coding mechanisms at the microcircuitry level remain a my...

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Main Authors: Yonglu Tian, Chaojuan Yang, Yaxuan Cui, Feng Su, Yongjie Wang, Yangzhen Wang, Peijiang Yuan, Shujiang Shang, Hao Li, Jizong Zhao, Desheng Zhu, Shiming Tang, Peng Cao, Yunbo Liu, Xunli Wang, Liecheng Wang, Wenbo Zeng, Haifei Jiang, Fei Zhao, Minhua Luo, Wei Xiong, Zilong Qiu, Xiang-Yao Li, Chen Zhang
Format: Article
Language:English
Published: Elsevier 2018-02-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718300822
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author Yonglu Tian
Chaojuan Yang
Yaxuan Cui
Feng Su
Yongjie Wang
Yangzhen Wang
Peijiang Yuan
Shujiang Shang
Hao Li
Jizong Zhao
Desheng Zhu
Shiming Tang
Peng Cao
Yunbo Liu
Xunli Wang
Liecheng Wang
Wenbo Zeng
Haifei Jiang
Fei Zhao
Minhua Luo
Wei Xiong
Zilong Qiu
Xiang-Yao Li
Chen Zhang
spellingShingle Yonglu Tian
Chaojuan Yang
Yaxuan Cui
Feng Su
Yongjie Wang
Yangzhen Wang
Peijiang Yuan
Shujiang Shang
Hao Li
Jizong Zhao
Desheng Zhu
Shiming Tang
Peng Cao
Yunbo Liu
Xunli Wang
Liecheng Wang
Wenbo Zeng
Haifei Jiang
Fei Zhao
Minhua Luo
Wei Xiong
Zilong Qiu
Xiang-Yao Li
Chen Zhang
An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
Cell Reports
short-term memory
prefrontal cortex
microcircuitry
Alzheimer’s disease
author_facet Yonglu Tian
Chaojuan Yang
Yaxuan Cui
Feng Su
Yongjie Wang
Yangzhen Wang
Peijiang Yuan
Shujiang Shang
Hao Li
Jizong Zhao
Desheng Zhu
Shiming Tang
Peng Cao
Yunbo Liu
Xunli Wang
Liecheng Wang
Wenbo Zeng
Haifei Jiang
Fei Zhao
Minhua Luo
Wei Xiong
Zilong Qiu
Xiang-Yao Li
Chen Zhang
author_sort Yonglu Tian
title An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
title_short An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
title_full An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
title_fullStr An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
title_full_unstemmed An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal Cortex
title_sort excitatory neural assembly encodes short-term memory in the prefrontal cortex
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-02-01
description Summary: Short-term memory (STM) is crucial for animals to hold information for a small period of time. Persistent or recurrent neural activity, together with neural oscillations, is known to encode the STM at the cellular level. However, the coding mechanisms at the microcircuitry level remain a mystery. Here, we performed two-photon imaging on behaving mice to monitor the activity of neuronal microcircuitry. We discovered a neuronal subpopulation in the medial prefrontal cortex (mPFC) that exhibited emergent properties in a context-dependent manner underlying a STM-like behavior paradigm. These neuronal subpopulations exclusively comprise excitatory neurons and mainly represent a group of neurons with stronger functional connections. Microcircuitry plasticity was maintained for minutes and was absent in an animal model of Alzheimer’s disease (AD). Thus, these results point to a functional coding mechanism that relies on the emergent behavior of a functionally defined neuronal assembly to encode STM.
topic short-term memory
prefrontal cortex
microcircuitry
Alzheimer’s disease
url http://www.sciencedirect.com/science/article/pii/S2211124718300822
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spelling doaj-8461fa37dd394514890d9aaed7047bc52020-11-25T03:01:14ZengElsevierCell Reports2211-12472018-02-012271734174410.1016/j.celrep.2018.01.050An Excitatory Neural Assembly Encodes Short-Term Memory in the Prefrontal CortexYonglu Tian0Chaojuan Yang1Yaxuan Cui2Feng Su3Yongjie Wang4Yangzhen Wang5Peijiang Yuan6Shujiang Shang7Hao Li8Jizong Zhao9Desheng Zhu10Shiming Tang11Peng Cao12Yunbo Liu13Xunli Wang14Liecheng Wang15Wenbo Zeng16Haifei Jiang17Fei Zhao18Minhua Luo19Wei Xiong20Zilong Qiu21Xiang-Yao Li22Chen Zhang23State Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, China; Peking-Tsinghua Center for Life Sciences, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, China; School of Mechanical Engineering and Automation, Beihang University, Beijing 100191, ChinaCenter for Mitochondrial Biology and Medicine, and Key Laboratory of Biomedical Information Engineering of the Ministry of Education, School of Life Science and Technology, Frontier Institute of Science and Technology, Xi’an Jiaotong University, Xi’an, Shaanxi Province 710049, China; Department of Physiology, Institute of Neuroscience and Collaborative Innovation Center for Brain Science, School of Medicine, Zhejiang University, Hangzhou, Zhejiang Province 310058, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, China; School of Medicine, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaSchool of Mechanical Engineering and Automation, Beihang University, Beijing 100191, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, China; China National Clinical Research Center for Neurological Diseases, Beijing 100050, ChinaDepartment of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing 100050, China; China National Clinical Research Center for Neurological Diseases, Beijing 100050, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, ChinaState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, ChinaState Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences (CAS), Beijing 100101, ChinaInstitute of Laboratory Animal Science, Peking Union Medical College/Chinese Academy of Medical Science, Beijing 100021, ChinaLaboratory Animal Center, Fujian University of Tradition Chinese Medicine, Fuzhou, Fujian Province 350122, ChinaDepartment of Physiology, Anhui Medical University, Hefei, Anhui Province 230032, ChinaState Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology, Wuhan Institute of Virology, CAS, Wuhan, Hubei Province 430071, ChinaState Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology, Wuhan Institute of Virology, CAS, Wuhan, Hubei Province 430071, ChinaState Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology, Wuhan Institute of Virology, CAS, Wuhan, Hubei Province 430071, ChinaState Key Laboratory of Virology, CAS Center for Excellence in Brain Science and Intelligence Technology, Wuhan Institute of Virology, CAS, Wuhan, Hubei Province 430071, ChinaSchool of Medicine, School of Life Sciences, Tsinghua University, Beijing 100084, ChinaCAS Key Laboratory of Primate Neurobiology, Institute of Neuroscience, CAS, Shanghai 200031, China; Corresponding authorDepartment of Physiology, Institute of Neuroscience and Collaborative Innovation Center for Brain Science, School of Medicine, Zhejiang University, Hangzhou, Zhejiang Province 310058, China; Corresponding authorState Key Laboratory of Membrane Biology, PKU-IDG/McGovern Institute for Brain Research, School of Life Sciences and Key Laboratory for Neuroscience, Ministry of Education/National Health and Family Planning Commission, Peking University, Beijing 100191, China; Corresponding authorSummary: Short-term memory (STM) is crucial for animals to hold information for a small period of time. Persistent or recurrent neural activity, together with neural oscillations, is known to encode the STM at the cellular level. However, the coding mechanisms at the microcircuitry level remain a mystery. Here, we performed two-photon imaging on behaving mice to monitor the activity of neuronal microcircuitry. We discovered a neuronal subpopulation in the medial prefrontal cortex (mPFC) that exhibited emergent properties in a context-dependent manner underlying a STM-like behavior paradigm. These neuronal subpopulations exclusively comprise excitatory neurons and mainly represent a group of neurons with stronger functional connections. Microcircuitry plasticity was maintained for minutes and was absent in an animal model of Alzheimer’s disease (AD). Thus, these results point to a functional coding mechanism that relies on the emergent behavior of a functionally defined neuronal assembly to encode STM.http://www.sciencedirect.com/science/article/pii/S2211124718300822short-term memoryprefrontal cortexmicrocircuitryAlzheimer’s disease