title: Opposite monosynaptic scaling of BLP-vCA1 inputs governs hopefulness- and helplessness-modulated spatial learning and memory.
abstract: Different emotional states lead to distinct behavioural consequences even when faced with the same challenging events. Emotions affect learning and memory capacities, but the underlying neurobiological mechanisms remain elusive. Here we establish models of learned helplessness (LHL) and learned hopefulness (LHF) by exposing animals to inescapable foot shocks or with anticipated avoidance trainings. The LHF animals show spatial memory potentiation with excitatory monosynaptic upscaling between posterior basolateral amygdale (BLP) and ventral hippocampal CA1 (vCA1), whereas the LHL show memory deficits with an attenuated BLP-vCA1 connection. Optogenetic disruption of BLP-vCA1 inputs abolishes the effects of LHF and impairs synaptic plasticity. By contrast, targeted BLP-vCA1 stimulation rescues the LHL-induced memory deficits and mimics the effects of LHF. BLP-vCA1 stimulation increases synaptic transmission and dendritic plasticity with the upregulation of CREB and intrasynaptic AMPA receptors in CA1. These findings indicate that opposite excitatory monosynaptic scaling of BLP-vCA1 controls LHF- and LHL-modulated spatial memory, revealing circuit-specific mechanisms linking emotions to memory.
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Ying
authors.initials: Y
authors.lastname: Yang
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Zhi-Hao
authors.initials: ZH
authors.lastname: Wang
authors.affiliation: Wuhan Institute of Physics and Mathematics, CAS Center for Excellence in Brain Science, Chinese Academy of Sciences, Wuhan 430071, China.
authors.forename: Sen
authors.initials: S
authors.lastname: Jin
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Di
authors.initials: D
authors.lastname: Gao
authors.affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
authors.forename: Nan
authors.initials: N
authors.lastname: Liu
authors.affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
authors.forename: Shan-Ping
authors.initials: SP
authors.lastname: Chen
authors.affiliation: Wuhan Institute of Physics and Mathematics, CAS Center for Excellence in Brain Science, Chinese Academy of Sciences, Wuhan 430071, China.
authors.forename: Sinan
authors.initials: S
authors.lastname: Zhang
authors.affiliation: Wuhan Institute of Physics and Mathematics, CAS Center for Excellence in Brain Science, Chinese Academy of Sciences, Wuhan 430071, China.
authors.forename: Qing
authors.initials: Q
authors.lastname: Liu
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Enjie
authors.initials: E
authors.lastname: Liu
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Xin
authors.initials: X
authors.lastname: Wang
authors.affiliation: School of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China.
authors.forename: Xiao
authors.initials: X
authors.lastname: Liang
authors.affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
authors.forename: Pengfei
authors.initials: P
authors.lastname: Wei
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Xiaoguang
authors.initials: X
authors.lastname: Li
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Yin
authors.initials: Y
authors.lastname: Li
authors.affiliation: Wuhan Institute of Physics and Mathematics, CAS Center for Excellence in Brain Science, Chinese Academy of Sciences, Wuhan 430071, China.
authors.forename: Chenyu
authors.initials: C
authors.lastname: Yue
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Hong-Lian
authors.initials: HL
authors.lastname: Li
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Ya-Li
authors.initials: YL
authors.lastname: Wang
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Qun
authors.initials: Q
authors.lastname: Wang
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.
authors.forename: Dan
authors.initials: D
authors.lastname: Ke
authors.affiliation: School of Life Science and Technology, Huazhong University of Science and Technology, Wuhan 430074, China.
authors.forename: Qingguo
authors.initials: Q
authors.lastname: Xie
authors.affiliation: Wuhan Institute of Physics and Mathematics, CAS Center for Excellence in Brain Science, Chinese Academy of Sciences, Wuhan 430071, China.
authors.forename: Fuqiang
authors.initials: F
authors.lastname: Xu
authors.affiliation: Shenzhen Key Lab of Neuropsychiatric Modulation and Collaborative Innovation Center for Brain Science, CAS Center for Excellence in Brain Science, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
authors.forename: Liping
authors.initials: L
authors.lastname: Wang
authors.affiliation: Department of Pathophysiology, School of Basic Medicine and the Collaborative Innovation Center for Brain Science, Key Laboratory of Ministry of Education of China for Neurological Disorders, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China.|Co-innovation Center of Neuroregeneration, Nantong 226000, China.
authors.forename: Jian-Zhi
authors.initials: JZ
authors.lastname: Wang
mesh_terms: D000818:Animals; D066272:Basolateral Nuclear Complex / Q000502:physiology*; D056547:CA1 Region, Hippocampal / Q000502:physiology*; D006380:Helplessness, Learned; D065026:Hope; D008297:Male; D008568:Memory / Q000502:physiology*; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D008959:Models, Neurological; D009473:Neuronal Plasticity / Q000502:physiology; D065853:Spatial Learning / Q000502:physiology*; D013569:Synapses / Q000502:physiology*