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Potentiation of the lateral habenula-ventral tegmental area pathway underlines the susceptibility to depression in mice with chronic pain

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Science China(Life Sciences) 2024年第1期67卷 67-82页

作者： Chun-Kui Zhang Pan Wang Yuan-Yuan Ji Jian-Shuai Zhao Jun-Xiang Gu Xian-Xia Yan Hong-Wei Fan Ming-Ming Zhang Yu Qiao Xiao-Die Liu Bao-Juan Li Ming-Hui Wang Hai-Long Dong Hao-Hong Li Peng-Cheng Huang Yun-Qing Li Wu-Gang Hou Jin-Lian Li Tao Chen Department of Anatomy and K.K.Leung Brain Research Centre Fourth Military Medical UniversityXi’an 710032China Beijing Institute of Basic Medical Sciences Beijing 100850China Key Laboratory of Ministry of Public Health for Forensic Science Xi’an Jiaotong UniversityXi’an 710061China Department of Anesthesiology Xijing HospitalFourth Military Medical UniversityXi’an 710032China Department of Neurosurgery the Second Affiliated Hospital of Xian Jiaotong UniversityXi’an 710004China School of Biomedical Engineering Fourth Military Medical UniversityXi’an 710032China Affiliated Mental Health Centre and Hangzhou Seventh People’s Hospital Zhejiang University School of MedicineHangzhou 310013China The MOE Frontier Research Center of Brain&Brain-machine Integration Zhejiang University School of Brain Science and Brain MedicineHangzhou 310058China Department of Neurology The First Affiliated Hospital of Nanchang UniversityNanchang 330006China Department of Anatomy School of MedicineNorthwest UniversityXi’an 710069China

Chronic pain often develops severe mood changes such as ***,how chronic pain leads to depression remains elusive and the mechanisms determining individuals’responses to depression are largely *** we found that depression-like behaviors could only be observed in 67.9%of mice with chronic neuropathic pain,leaving 32.1%of mice with depression *** determined that the spike discharges of the ventral tegmental area(VTA)-projecting lateral habenula(LHb)glutamatergic(Glu)neurons were sequentially increased in sham,resilient and susceptible mice,which consequently inhibited VTA dopaminergic(DA)neurons through a LHbGlu-VTAGABA-VTADA ***,the LHbGlu-VTADA excitatory inputs were dampened via GABAB receptors in a pre-synaptic *** of LHb-VTA pathway largely affected the development of depressive symptoms caused by chronic *** study thus identifies a pivotal role of the LHb-VTA pathway in coupling chronic pain with depression and highlights the activity-dependent contribution of LHbGlu-to-VTADA inhibition in depressive behavioral regulation.

关键词： chronic pain depression lateral habenula ventral tegmental area dopamine susceptibility

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Sexual Dimorphism of Inputs to the lateral habenula in Mice

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Neuroscience Bulletin 2022年第12期38卷 1439-1456页

作者： Xue Liu Hongren Huang Yulin Zhang Liping Wang Feng Wang Shenzhen Key Lab of Neuropsychiatric Modulation Guangdong Provincial Key Laboratory of Brain Connectome and BehaviorCAS Key Laboratory of Brain Connectome and Manipulationthe Brain Cognition and Brain Disease InstituteShenzhen Institute of Advanced TechnologyChinese Academy of SciencesShenzhen-Hong Kong Institute of Brain Science-Shenzhen Fundamental Research InstitutionsShenzhen 518055China University of the Chinese Academy of Sciences Beijing 100049China

The lateral habenula(LHb),which is a critical neuroanatomical hub and a regulator of midbrain monoaminergic centers,is activated by events resulting in negative valence and contributes to the expression of both appetitive and aversive ***,whole-brain cell-type-specific monosynaptic inputs to the LHb in both sexes remain incompletely *** this study,we used viral tracing combined with in situ hybridization targeting vesicular glutamate transporter 2(vGlut2)and glutamic acid decarboxylase 2(Gad2)to generate a comprehensive whole-brain atlas of inputs to glutamatergic andγ-aminobutyric acid(GABA)ergic neurons in the *** found>30 ipsilateral and contralateral brain regions that projected to the *** these,there were significantly more monosynaptic LHb-projecting neurons from the lateral septum,anterior hypothalamus,dorsomedial hypothalamus,and ventromedial hypothalamus in females than in *** interestingly,we found a stronger GABAergic projection from the medial septum to the LHb in males than in *** results reveal a comprehensive connectivity atlas of glutamatergic and GABAergic inputs to the LHb in both sexes,which may facilitate a better understanding of sexual dimorphism in physiological and pathological brain functions.

关键词： vGlut2 Gad2 Monosynaptic inputs lateral habenula Sex differences Rabies retrograde tracing

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lateral Hypothalamic Area Glutamatergic Neurons and Their Projections to the lateral habenula Modulate the Anesthetic Potency of Isoflurane in Mice

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Neuroscience Bulletin 2021年第7期37卷 934-946页

作者： Shiyi Zhao Rui Li Huiming Li Sa Wang Xinxin Zhang Dan Wang Juan Guo Huihui Li Ao Li Tingting Tong Haixing Zhong Qianzi Yang Hailong Dong Department of Anesthesiology and Perioperative Medicine Xijing HospitalFourth Military Medical UniversityXi’an 710032China

The lateral hypothalamic area(LHA)plays a pivotal role in regulating consciousness transition,in which orexinergic neurons,GABAergic neurons,and melanin-concentrating hormone neurons are *** neurons have a large population in the LHA,but their anesthesia-related effect has not been ***,we found that genetic ablation of LHA glutamatergic neurons shortened the induction time and prolonged the recovery time of isoflurane anesthesia in *** contrast,chemogenetic activation of LHA glutamatergic neurons increased the time to anesthesia and decreased the time to *** activation of LHA glutamatergic neurons during the maintenance of anesthesia reduced the burst suppression pattern of the electroencephalogram(EEG)and shifted EEG features to an arousal *** of LHA glutamatergic projections to the lateral habenula(LHb)also facilitated the emergence from anesthesia and the transition of anesthesia depth to a lighter ***,LHA glutamatergic neurons and their projections to the LHb regulate anesthetic potency and EEG features.

关键词： Anesthesia Isoflurane lateral hypothalamic area lateral habenula Glutamatergic neuron

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Modulation of T-type calcium channels by 17β-estradiol in the lateral habenula of rats

Modulation of T-type calcium channels by 17β-estradiol in t...

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中国神经科学学会第十届全国学术会议

作者： Mei-Ying SONG Chun-Ying LI Hua ZHAO Neuroscience research center First Hospital of Jilin University Department of Physiology Norman Bethune College of MedicineJilin University

Estrogen is a steroid hormone,regulated a variety of physiological functions,and distributed in many parts of the *** report demonstrated that estrogen regulation of T-type calcium channel activity in the barin through binding to its *** lateral habenula（LHb） is an important hinge linked the limbic system and the midbrain,it involved in many physiological functions,meanwhile play a role on the estrogen-dependent behaviours,such as increase the sexual receptivity and maternal behavior during pregnancy and *** contained estrogen receptor,and also expressed a higher density of T-type calcium channels subtypes,Cav3.1 and Cav3.3,which play an important role in regulation neuronal *** speculate estrogen may affect the LHb neurons function by regulating the activation of T-type calcium *** this study,we assessed the effect of estrogen on T-type calcium current in LHb neurons by patch clamp techniques with ovariectomized oil-treated and E2-treated *** evaluated the expression of T-type calcium channels protein and mRNA by real-time PCR,western *** found that compare with oil-treated group,the expression of Cav3.1 and Cav3.3 mRNA decrease significantly in LHb in E2-treated group,The protein expression of the two subunits also decrease in E2-treated ***-cell patch recordings in LHb neurons revealed that E2 treatment significantly attenuated T-type current,and increased decay time and recovery time of T-type calcium channels,increased the slope factor of activation and inactivation *** together,these data indicate the impact of estrogen to LHb may be related to change the activity of T-type calcium channels.

关键词： lateral habenula T-type calcium channel estrogen

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A potential target for Parkinson’s disease treatment:effect of lateral habenula lesions

A potential target for Parkinson’s disease treatment:effect...

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中国生理学会第24届全国会员代表大会暨生理学学术大会

作者： Bing Han Huijuan Jin Tian Wang Hua Zhao Department of Physiology Norman Bethune College of MedicineJilin University School of Pharmacy Yantai University Neuroscience Research Center First Hospital of Jilin University

Parkinson’s disease（PD）is a progressive neurodegenerative movement disorder,which caused predominantly by the degeneration of the nigrostriatal dopaminergic *** habenula（LHb）has efferent projections that terminate in the substantia nigra pars compacta（SNpc）and electrical stimulation of the LHb effectively suppresses the activity of dopamine-containing neurons in the *** study was aimed at investigating whether LHb lesions can ameliorate the syndromes of PD via affecting the activities of SNpc neurons in 6-hydroxydopamine hydrochloride（6-OHDA）-induced PD model ***（DA）and its metabolites dihydroxyphenylacetic acid（DOPAC）and homovanillic acid（HVA）in the striatum,which is the area projected by the SNpc dopaminergic neurons were assayed by high-performance liquid chromatography coupled with fluorescence *** immunohistochemical method was employed to detect the numbers of tyrosine hydorxylase（TH）in the substantia *** results showed that LHb lesions induced a significant reduction in apomorphine-induced rotational *** DA,DOPAC and HVA levels in the striatum of PD model rats were increased by the LHb *** we speculated that the LHb lesions induced a significant amelioration in motor disorders via increasing the DA levels in the striatum,which may lead to potential therapeutic strategies for the treatment of PD.

关键词： lateral habenula Parkinson Dopamine Substantia nigra pars compacta

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Why depression and pain often coexist and mutually reinforce: Role of the lateral habenula

Why depression and pain often coexist and mutually reinforce...

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中国神经科学学会第十二届全国学术会议

作者： Jicheng Li Yang Li Beilin Zhang Xiangfeng Shen Hua Zhao Department of Physiology College of Basic Medical Sciences Jilin University

The interrelation of depression and pain is increasingly coming under scrutiny. Although the lateral habenula（LHb） is widely implicated in the pathogenesis of depression and pain, its role in the interaction of depression and pain remains unknown. Thus, the aim of current study was to investigate the role of LHb in rat depression-pain comorbidity. Single extracellular firing recording and immunofluorescence methods were used to compare firing rates and c-Fos expression of the LHb neurons in normal and model rats. Following subcutaneous injection of formalin into the hind paw to simulate natural pain, we assessed pain behavior in rats subjected to the chronic, unpredictable mild stress procedure（CUMS, a model of depression）. Pain sensitivity in the model rats was increased over that of controls. These rats showed a significant increase in the firing activity of LHb neurons compared with normal rats. Significantly, about 73% of neurons with high discharge frequency in LHb of model rats were pain-activated neurons（PANs）, and the firing rates of PANs were inhibited by intraperitoneal injection of a tricyclic antidepressant, clomipramine. Immunofluorescence showed that the percentage of c-Fos positive cells in LHb was significantly increased in rats receiving CUMS alone, rats receiving pain stimulation alone, and rats receiving both CUMS and pain stimulation, but especially the last. The interaction effect was inhibited by injection of clomipramine. The LHb lesion can improve both depression-like behavior and pain sensitivity in depression model rats with pain. These suggest that hyperactivity of the LHb neurons contributes to depression-pain comorbidity in rats.

关键词： Depression Pain lateral habenula Dorsal raphe nucleus C-Fos protein Comorbidity

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Increased c-Fos expression in the medial part of the lateral habenula during cue-evoked heroin-seeking in rats

Increased c-Fos expression in the medial part of the lateral...

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中国神经科学学会第六届学术会议暨学会成立十周年庆祝大会

作者：张富强周文华刘惠芬朱华强唐甩恩赖苗军杨国栋宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所宁波市微循环与莨菪类药研究所

＜正＞Conditioned environmental stimuli are known to be important determinants of drug seeking behavior. c-Fos, the protein product of the protooncogene c-fos, is expressed in neurons when there are drug-associated cue-induced drug-seeking behaviour. Therefore, its expression could serve as a marker of regional neuronal activation. Using an extinction/reinstatement paradigm of relapse animal model, we

关键词： c-Fos lateral habenula heroin cue drug seeking

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A potentiation of REM sleep-active neurons in the lateral habenula may be responsible for the sleep disturbance in depression

A potentiation of REM sleep-active neurons in the lateral ha...

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中国睡眠研究会第16届全国学术年会暨湖北科学技术学术年会

作者： Zehui Zhang Hua Zhao Department of Physiology College of Basic Medical SciencesJilin University

Psychiatric disorders with dysfunction of the lateral habenula(LHb) show sleep disturbance,especially a disinhibition of rapid eye movement(REM) sleep in major ***,the role of LHb in physiological sleep control and how LHb contributes to sleep disturbance in major depression remain ***,we found that functional manipulations of LHb glutamatergic neurons bidirectionally modulated both non-REM(NREM) sleep and REM *** recording revealed heterogeneous activity patterns of LHb neurons across sleep/wakefulness cycles,but LHb neurons were preferentially active during REM *** an activity-dependent tagging method,we selectively labeled a population of REM sleep-active LHb neurons and demonstrated that these neurons specifically promoted REM *** circuit studies showed that LHb neurons regulated REM sleep via projections to the ventral tegmental area but not to the rostromedial tegmental ***,we found that the increased REM sleep in a depression mouse model was associated with a potentiation of REM sleep-active LHb neurons,including an increased proportion,elevated spike firing,and altered activity ***,inhibition of REM sleep-active LHb neurons not only attenuated the increased REM sleep but also alleviated depressive-like behaviors in a depression mouse ***,our results demonstrated that REM sleep-active LHb neurons selectively promoted REM sleep,and a potentiation of these neurons contributed to depression-associated sleep disturbance.

关键词： lateral habenula REM sleep depression

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The Medial Prefrontal Cortex Modulates Activity in the Nucleus Accumbens and lateral habenula to Maintain Wakefulness During Task Performance in Mice

The Medial Prefrontal Cortex Modulates Activity in the Nucle...

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中国睡眠研究会第16届全国学术年会暨湖北科学技术学术年会

作者： Chengwei Liu Weimin Qu Zhili Huang Department of Pharmacology School of Basic Medical Sciences State Key Laboratory of Medical Neurobiology and MOE Frontiers Center for Brain Science institutes of Brain Science Fudan University

Beyond the natural rhythm of working at sunrise and resting at sunset,individuals can sustain wakefulness and counteract sleep when working overtime or pursuing *** specific context of arousal regulation may be topdown mediated by the medial prefrontal cortex(mPFC),but the neural circuitry mechanisms remain *** a lever-pressing task of reinforcement learning,we found that mice maintain wakefulness during the task state,independent of immediate *** photometry recording showed that increased activity of mPFC,nucleus accumbens(NAc),and lateral habenula(LHb) neurons during the *** optogenetic manipulations revealed that mPFC neuron terminals projecting to the NAc or LHb were critical for the transition from non-rapid eye movement(NREM) sleep to wakefulness in *** interventions showed that the mPFC-NAcD1R and mPFC-LHbVglut2 pathways are crucial for arousal regulation during the task ***,our study revealed top-down arousal regulation circuits based on reward motivation.

关键词： lateral habenula medial prefrontal cortex motivation of reward nucleus accumbens task state wakefulness

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Lycium barbarum polysaccharide-glycoprotein preventative treatment ameliorates aversive stimuli-induced depression

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Neural Regeneration Research 2021年第3期16卷 543-549页

作者： Yun-Wei Fu Yan-Fang Peng Xiao-Dan Huang Yan Yang Lu Huang Yue Xi Zheng-Fang Hu Song Lin Kwok-Fai So Chao-Ran Ren Guangdong-Hongkong-Macao Institute of CNS Regeneration Ministry of Education CNS Regeneration Collaborative Joint LaboratoryJinan UniversityGuangzhouGuangdong ProvinceChina Aier Eye Institute ChangshaHunan ProvinceChina Department of Physiology School of MedicineJinan UniversityGuangzhouGuangdong ProvinceChina Bioland Laboratory(Guangzhou Regenerative Medicine and Health Guangdong Laboratory) GuangzhouGuangdong ProvinceChina Center for Brain Science and Brain-Inspired Intelligence Guangdong-Hong Kong-Macao Greater Bay AreaGuangzhouGuangdong ProvinceChina Co-innovation Center of Neuroregeneration Nantong UniversityNantongJiangsu ProvinceChina Department of Ophthalmology and State Key Laboratory of Brain and Cognitive Sciences The University of Hong KongHong Kong Special Administrative RegionChina

Previous studies have shown that Lycium barbarum polysaccharide,the main active component of Lycium barbarum,exhibits antiinflammatory and antioxidant effects in treating neurological ***,the therapeutic action of Lycium barbarum polysaccharide on depression has not been *** this investigation,we established mouse models of depression using aversive stimuli including exposure to fox urine,air puff and foot shock and physical ***,we administered 5 mg/kg per day Lycium barbarum polysaccharide-glycoprotein to each mouse intragastrically for the 28 *** results showed that long-term exposure to aversive stimuli significantly enhanced depressive-like behavior evaluated by the sucrose preference test and the forced swimming test and increased anxietylike behaviors evaluated using the open field *** addition,aversive stimuli-induced depressed mice exhibited aberrant neuronal activity in the lateral ***,concurrent Lycium barbarum polysaccharide-glycoprotein treatment significantly reduced these *** findings suggest that Lycium barbarum polysaccharide-glycoprotein is a potential preventative intervention for depression and may act by preventing aberrant neuronal activity and microglial activation in the lateral *** study was approved by the Jinan University Institutional Animal Care and Use Committee(approval No.20170301003)on March 1,2017.

关键词： aversive stimuli behaviors depression immune response inflammation lateral habenula Lycium barbarum polysaccharide mice microglia neuron

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