小鼠前额叶皮层和丘脑网状核γ-氨基丁酸能神经环路的调控及其机制
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摘要
在中枢神经系统中,丫-氨基丁酸(γ-aminobutyric acid, GABA)能神经环路起着重要的调控作用。GABA能神经元中parvalbumin (PV)蛋白阳性的快速放电(fast-spiking, FS)神经元占皮层所有中间神经元的40-50%。这类神经元形成复杂的网络联系：它们既投射到锥体细胞,也投射到其他类型的中间神经元,并且这些神经元彼此之间也通过广泛的电、化学突触相联系,从而形成一个交互的GABA能抑制性神经环路。此外,皮层下的GABA能神经元还接受其他如胆碱能或多巴胺能等神经元的输入,这些都能调控GABA能神经环路的功能,从而影响大脑的许多高级认知活动。
前额叶皮层(prefrontal cortex, PFC)是中枢神经系统中主要负责多种高级认知功能如决策、学习和工作记忆的一个重要脑区。许多因素可以调控皮层的GABA能神经环路,包括神经营养因子如BDNF和FGF等。神经调节素1(Neuregulin1, NRG1)作为神经营养因子大家族的一个成员,在中枢神经系统,主要通过与酪氨酸蛋白激酶受体ErbB4结合并激活一系列胞内信号通路来发挥功能。近些年,nrgl和erbb4作为精神分裂症的两大易感基因而备受重视,但是,NRG1-ErbB4信号通路通过哪些途径参与精神分裂症的发生目前仍不很清楚。在很多脑区,特别是前额叶皮层,神经元同步化活动的减弱和精神分裂症的核心症状直接相关。近期研究显示,ErbB4主要在中间神经元,特别是FS中间神经元上表达。NRG1作用于海马的FS中间神经元,可以影响海马锥体细胞同步化的丫波振荡。但是,NRG1-ErbB4信号通路在PFC神经元的同步化活动中的作用目前尚无报道。
丘脑网状核(thalamic reticular nucleus, TRN)是联系皮层和丘脑的一个核团,其中大部分是GABA能PV神经元。TRN接受谷氨酸能、胆碱能和多巴胺能等多种输入,其中胆碱能输入主要来自脑干,对睡眠的调节有重要作用。虽然有少数研究从形态学的证据支持基底大细胞核(nucleus basalis of Meynert, nbM)和TRN有联系,但缺乏从nbM的胆碱能神经元到TRN的PV神经元具备突触传递的直接证据,并且这种来自基底前脑的胆碱能投射对TRN的GABA能神经环路的调控有何重要功能仍不清楚。
因此,本研究结合电生理、分子遗传学、免疫组化、光遗传学以及行为学等手段,试图回答两个问题：第一,PFC的FS中间神经元在正常和敲除中间神经元上的ErbB4受体后,NRG1对各种神经元同步化活动的影响；第二,nbM的胆碱能神经元是否具备到TRN的PV神经元直接的突触传递,这种投射参与何种大脑的高级认知功能。我们发现：1)NRG1不仅可以增强前额叶皮层锥体神经元的同步性活动,对同种FS-FS或不同种FS-LTS (low-threshold-spiking,低阈值放电)中间神经元的同步化也都有增强作用；2)NRG1是通过抑制性突触而不是通过电突触对神经元的同步化起作用的；3)中间神经元上的ErbB4介导了NRG1的这种作用；4)在活体中,NRG1可以增强海人酸诱导的同步化的丫波振荡,而在前脑的中间神经元中敲除ErbB4,可以使NRG1的上述作用消失；5)nbM的胆碱能神经元到TRN的PV神经元具有直接的突触传递；6)其中兴奋性电流由突触后的α7尼古丁受体(α7nAChRs)介导,而抑制性电流由突触后的M1型毒蕈碱受体(M1mAChRs)介导；7)而且这种兴奋性突触传递可以增强TRN的PV神经元的谷氨酸能突触可塑性；8)Ap可以损伤这种兴奋性电流及可塑性；9)nbM到TRN的胆碱能投射参与了大脑记忆巩固的过程。根据上述实验结果,我们认为前额叶皮层GABA能神经环路的调控可以影响大脑的同步化活动,而丘脑网状核的GABA能神经元的调控,参与了记忆巩固等高级认知功能。因此,这些GABA能神经环路的功能异常,可能和许多神经精神疾病的发生密切相关。
The y-aminobutyric acid (GABA)-ergic circuits play an important role in the mouse central nervous system. Parvalbumin (PV) positive fast-spiking (FS) neurons account for40-50%of all GABAergic interneurons in the neocortex. These neurons form several microcircuits in the PFC: first, they are connected with pyramidal neurons or other types of inteneurons through chemical synapses; second, they are interconnected via chemical and electrical synapses (FS-FS). In addition, subcortical PV neurons also receive synaptic input from cholinergic neurons. All these projections are involved in many higher cognitive functions by regulating the GABAergic circuit in the central nervous system.
The prefrontal cortex (PFC) is responsible for higher cognitive functions such as decision, learning and working memory. The GABA circuit is regulated by many factors. Among them are neurotrophins like BDNF and FGF. Neuregulin1(NRG1), a member of the growth factor family, functions mainly through binding with the tyrosine kinase-type receptor ErbB4in the central nervous system. Both nrgl and erbb4are susceptibility genes for schizophrenia, yet their precise roles in schizophrenia are largely unknown. Reduced synchronization in several cortical regions, especially in the PFC, is associated with the core symptoms of schizophrenia. Recent studies show that NRG1may affect the hippocampal oscillations through ErbB4expressed on FS interneurons. However, the role of NRG1/ErbB4signaling in the synchronization of neurons in the PFC is unclear.
The thalamic reticular nucleus (TRN) is located between the thalamus and the cortex and composed entirely of GABAergic neurons, of which most are PV neurons. TRN mainly receives cholinergic projections from the brainstem which has an important role in sleep regulation. A few morphologic studies suggested that TRN maybe receive fibers from cholinergic neurons of the nucleus basalis of Meynert (nbM). However, direct evidence linking the nbM cholinergic neurons to TRN PV interneurons is lacking, and the function of this circuit is unknown.
Here, with the use of multiple approaches including electrophysiology, immunohistochemistry, optogenetics, we demonstrate that in the mouse PFC, NRG1enhanced the synchrony of the two major kinds of neurons through inhibitory synapses in the local network and increased the power of kainate-induced gamma oscillations in vivo. Furthermore, this effect was mediated by ErbB4receptors. While in the TRN, optical activation of nbM cholinergic neurons provided direct excitatory and inhibitory synaptic transmission to PV neurons via α7nicotinic acetylcholine receptors (α7nAChRs) and M1muscarinic acetylcholine receptors (Ml mAChRs), respectively. And the excitatory cholinergic transmission could regulate glutamatergic synaptic plasticity in these neurons. Both the excitatory transmission and the plasticity could be disrupted by Aβ exposure. Moreover, this functional cholinergic transmission from the nbM to the TRN was involved in memory consolidation. Therefore, abnormality of the neural GABAergic circuits may be related to the pathology of many higher cognitive disorders and likely causes many kinds of neuropsychiatric diseases such as schizophrenia.
前额叶皮层(prefrontal cortex, PFC)是中枢神经系统中主要负责多种高级认知功能如决策、学习和工作记忆的一个重要脑区。许多因素可以调控皮层的GABA能神经环路,包括神经营养因子如BDNF和FGF等。神经调节素1(Neuregulin1, NRG1)作为神经营养因子大家族的一个成员,在中枢神经系统,主要通过与酪氨酸蛋白激酶受体ErbB4结合并激活一系列胞内信号通路来发挥功能。近些年,nrgl和erbb4作为精神分裂症的两大易感基因而备受重视,但是,NRG1-ErbB4信号通路通过哪些途径参与精神分裂症的发生目前仍不很清楚。在很多脑区,特别是前额叶皮层,神经元同步化活动的减弱和精神分裂症的核心症状直接相关。近期研究显示,ErbB4主要在中间神经元,特别是FS中间神经元上表达。NRG1作用于海马的FS中间神经元,可以影响海马锥体细胞同步化的丫波振荡。但是,NRG1-ErbB4信号通路在PFC神经元的同步化活动中的作用目前尚无报道。
丘脑网状核(thalamic reticular nucleus, TRN)是联系皮层和丘脑的一个核团,其中大部分是GABA能PV神经元。TRN接受谷氨酸能、胆碱能和多巴胺能等多种输入,其中胆碱能输入主要来自脑干,对睡眠的调节有重要作用。虽然有少数研究从形态学的证据支持基底大细胞核(nucleus basalis of Meynert, nbM)和TRN有联系,但缺乏从nbM的胆碱能神经元到TRN的PV神经元具备突触传递的直接证据,并且这种来自基底前脑的胆碱能投射对TRN的GABA能神经环路的调控有何重要功能仍不清楚。
因此,本研究结合电生理、分子遗传学、免疫组化、光遗传学以及行为学等手段,试图回答两个问题：第一,PFC的FS中间神经元在正常和敲除中间神经元上的ErbB4受体后,NRG1对各种神经元同步化活动的影响；第二,nbM的胆碱能神经元是否具备到TRN的PV神经元直接的突触传递,这种投射参与何种大脑的高级认知功能。我们发现：1)NRG1不仅可以增强前额叶皮层锥体神经元的同步性活动,对同种FS-FS或不同种FS-LTS (low-threshold-spiking,低阈值放电)中间神经元的同步化也都有增强作用；2)NRG1是通过抑制性突触而不是通过电突触对神经元的同步化起作用的；3)中间神经元上的ErbB4介导了NRG1的这种作用；4)在活体中,NRG1可以增强海人酸诱导的同步化的丫波振荡,而在前脑的中间神经元中敲除ErbB4,可以使NRG1的上述作用消失；5)nbM的胆碱能神经元到TRN的PV神经元具有直接的突触传递；6)其中兴奋性电流由突触后的α7尼古丁受体(α7nAChRs)介导,而抑制性电流由突触后的M1型毒蕈碱受体(M1mAChRs)介导；7)而且这种兴奋性突触传递可以增强TRN的PV神经元的谷氨酸能突触可塑性；8)Ap可以损伤这种兴奋性电流及可塑性；9)nbM到TRN的胆碱能投射参与了大脑记忆巩固的过程。根据上述实验结果,我们认为前额叶皮层GABA能神经环路的调控可以影响大脑的同步化活动,而丘脑网状核的GABA能神经元的调控,参与了记忆巩固等高级认知功能。因此,这些GABA能神经环路的功能异常,可能和许多神经精神疾病的发生密切相关。
The y-aminobutyric acid (GABA)-ergic circuits play an important role in the mouse central nervous system. Parvalbumin (PV) positive fast-spiking (FS) neurons account for40-50%of all GABAergic interneurons in the neocortex. These neurons form several microcircuits in the PFC: first, they are connected with pyramidal neurons or other types of inteneurons through chemical synapses; second, they are interconnected via chemical and electrical synapses (FS-FS). In addition, subcortical PV neurons also receive synaptic input from cholinergic neurons. All these projections are involved in many higher cognitive functions by regulating the GABAergic circuit in the central nervous system.
The prefrontal cortex (PFC) is responsible for higher cognitive functions such as decision, learning and working memory. The GABA circuit is regulated by many factors. Among them are neurotrophins like BDNF and FGF. Neuregulin1(NRG1), a member of the growth factor family, functions mainly through binding with the tyrosine kinase-type receptor ErbB4in the central nervous system. Both nrgl and erbb4are susceptibility genes for schizophrenia, yet their precise roles in schizophrenia are largely unknown. Reduced synchronization in several cortical regions, especially in the PFC, is associated with the core symptoms of schizophrenia. Recent studies show that NRG1may affect the hippocampal oscillations through ErbB4expressed on FS interneurons. However, the role of NRG1/ErbB4signaling in the synchronization of neurons in the PFC is unclear.
The thalamic reticular nucleus (TRN) is located between the thalamus and the cortex and composed entirely of GABAergic neurons, of which most are PV neurons. TRN mainly receives cholinergic projections from the brainstem which has an important role in sleep regulation. A few morphologic studies suggested that TRN maybe receive fibers from cholinergic neurons of the nucleus basalis of Meynert (nbM). However, direct evidence linking the nbM cholinergic neurons to TRN PV interneurons is lacking, and the function of this circuit is unknown.
Here, with the use of multiple approaches including electrophysiology, immunohistochemistry, optogenetics, we demonstrate that in the mouse PFC, NRG1enhanced the synchrony of the two major kinds of neurons through inhibitory synapses in the local network and increased the power of kainate-induced gamma oscillations in vivo. Furthermore, this effect was mediated by ErbB4receptors. While in the TRN, optical activation of nbM cholinergic neurons provided direct excitatory and inhibitory synaptic transmission to PV neurons via α7nicotinic acetylcholine receptors (α7nAChRs) and M1muscarinic acetylcholine receptors (Ml mAChRs), respectively. And the excitatory cholinergic transmission could regulate glutamatergic synaptic plasticity in these neurons. Both the excitatory transmission and the plasticity could be disrupted by Aβ exposure. Moreover, this functional cholinergic transmission from the nbM to the TRN was involved in memory consolidation. Therefore, abnormality of the neural GABAergic circuits may be related to the pathology of many higher cognitive disorders and likely causes many kinds of neuropsychiatric diseases such as schizophrenia.
引文
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