小鼠前额叶皮层GABA环路的发育及其分子机制研究
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摘要
前额叶皮层(prefrontal cortex, PFC)是中枢神经系统主要负责多种高级认知功能如工作记忆的一个重要脑区。小清蛋白阳性的快尖峰放电(fast-spiking, FS)中间神经元在这些功能的执行过程中扮演着重要角色。FS中间神经元占新皮层所有中间神经元的40-50%,其中绝大部分是篮状细胞(～90%)；这类中间神经元在皮层有复杂的网络联系：它们既投射到锥体细胞(pyramidal neurons, PN)也接受PN的兴奋性输入,从而形成一个交互的局部兴奋-抑制环路(FS-PN);并且这些神经元彼此之间通过广泛的电、化学突触联系形成一个相对独立的网络(FS-FS)。此外,FS中间神经元还接受丘脑-皮层中继神经元的输入,也与皮层内其它中间神经元形成突触联系。尽管PFC的GABA环路,特别是由FS中间神经元参与形成的微环路的结构与功能异常与多种发育相关的神经精神类疾病如精神分裂症关联紧密；然而,目前尚无报道对由PFC的FS中间神经元参与形成的微环路在出生后的发育进行系统研究。
皮层GABA环路在发育过程中受到多种因素的调控,包括生长因子如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清楚。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。但是,NRG1-ErbB4信号通路在PFC的FS中间神经元特别是由篮状细胞参与形成的微环路发育过程中的作用却鲜有报道。
因此,本研究结合分子遗传学、生化以及电生理等手段,试图回答两个问题：第一,PFC的FS中间神经元在正常发育过程中的微环路构建,我们重点关注FS-PN和FS-FS两个微环路；第二,敲除中间神经元上的ErbB4受体后,由FS中间神经元特别是篮状细胞参与形成的微环路的发育是否受影响。我们发现：1)FS中间神经元微环路在出生后第二周初步建立起来,而环路重塑却一直持续到青春期；2)在胚胎期敲除ErbB4受体,由FS篮状细胞所形成的抑制性突触的发育并没有受到明显影响,但是活性依赖性的突触传递功能明显减弱；3)敲除ErbB4不影响FS-FS之间电突触的发育；4)敲除ErbB4虽不影响PN-FS的兴奋性突触的早期发育,但其成熟受阻。根据上述实验结果,我们提出如下模型：敲除ErbB4后导致FS篮状细胞的兴奋性突触输入减少,同时,由FS篮状细胞所介导的活性依赖性抑制性突触传递功能也减弱了,二者共同促成为了由FS篮状细胞所介导的抑制功能的降低；通过稳态机制,锥体细胞下调兴奋性突触的表达,以维持皮层兴奋-抑制功能之间的相对平衡；这种平衡可能在某些发育关键期如青春期受到破坏而最终导致精神分裂症的发生。
The prefrontal cortex (PFC) is responsible for higher cognitive functions such as working memory, during which parvalbumin-positive fast-spiking (FS) interneurons play an essential role. FS interneurons account for40-50%of all interneurons in the neocortex, a large majority of which are basket cells; these neurons form several microcircuits in the PFC:first, they are connected with pyramidal neurons (PN) through chemical synapses (FS-PN); second, they are interconnected via chemical and electrical synapses (FS-FS). In addition, FS interneurons also receive synaptic inputs from thalamo-cortical relay neurons, and project to and receive inputs from somatostatin-expressing interneurons. Despite the putative relevance of FS interneurons for neurodevelopmental disease processes such as schizophrenia in humans, to the best of our knowledge, little effort has been exerted to study when and how FS interneurons develop their networks in the PFC.
The development of GABA circuitry is regulated by many factors. Among them are neurotrophins like BDNF and FGF. Neuregulin1(NRG1), a member of the growth factor family, functions in a number of developmental processes 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. Recent studies show that ErbB4is expressed predominantly in interneurons, specifically, in FS interneurons. However, it is largely unknown what roles NRG1-ErbB4signals play during the development of FS interneuronal microcircuits, particularly that mediated by basket cells in the PFC.
Here, with the use of a combination of research disciplines including molecular genetics, biochemistry, and electrophysiology, we demonstrate that in the mouse PFC, FS interneurons were poorly developed in terms of the membrane and network properties during the first postnatal week, both of which exhibited an abrupt maturation during the second postnatal week. The development of FS interneuronal microcircuits persisted throughout early adulthood. NRG1-ErbB4signaling was dispensable for the development of GABAergic synapses and gap junctions formed by FS basket interneurons in vivo. However, activity-dependent GABAergic FS-PN transmissions were disrupted without erbb4. While NRG1-ErbB4signaling was not required for the early development of glutamatergic synapses on FS basket interneurons, it was essential for the maturation of these synapses. Based on these observations, we speculate the following model:NRG1-ErbB4signaling is required for the development of glutamatergic synapses, but not GABAergic synapses. Knock-out of ErbB4leads to hypo-glutamatergic transmissions on FS basket interneurons and reduced activity-dependent GABAergic FS-PN transmissions, thus reducing inhibition mediated by FS basket interneurons. To maintain the appropriate excitation/inhibition (E/I) balance, PN neurons then homeostatically reduce the glutamatergic excitatory synapses. The disruption of E/I balance during adolescence may underlie the etiology of neuropsychiatric disorders like schizophrenia.
皮层GABA环路在发育过程中受到多种因素的调控,包括生长因子如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清楚。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。但是,NRG1-ErbB4信号通路在PFC的FS中间神经元特别是由篮状细胞参与形成的微环路发育过程中的作用却鲜有报道。
因此,本研究结合分子遗传学、生化以及电生理等手段,试图回答两个问题：第一,PFC的FS中间神经元在正常发育过程中的微环路构建,我们重点关注FS-PN和FS-FS两个微环路；第二,敲除中间神经元上的ErbB4受体后,由FS中间神经元特别是篮状细胞参与形成的微环路的发育是否受影响。我们发现：1)FS中间神经元微环路在出生后第二周初步建立起来,而环路重塑却一直持续到青春期；2)在胚胎期敲除ErbB4受体,由FS篮状细胞所形成的抑制性突触的发育并没有受到明显影响,但是活性依赖性的突触传递功能明显减弱；3)敲除ErbB4不影响FS-FS之间电突触的发育；4)敲除ErbB4虽不影响PN-FS的兴奋性突触的早期发育,但其成熟受阻。根据上述实验结果,我们提出如下模型：敲除ErbB4后导致FS篮状细胞的兴奋性突触输入减少,同时,由FS篮状细胞所介导的活性依赖性抑制性突触传递功能也减弱了,二者共同促成为了由FS篮状细胞所介导的抑制功能的降低；通过稳态机制,锥体细胞下调兴奋性突触的表达,以维持皮层兴奋-抑制功能之间的相对平衡；这种平衡可能在某些发育关键期如青春期受到破坏而最终导致精神分裂症的发生。
The prefrontal cortex (PFC) is responsible for higher cognitive functions such as working memory, during which parvalbumin-positive fast-spiking (FS) interneurons play an essential role. FS interneurons account for40-50%of all interneurons in the neocortex, a large majority of which are basket cells; these neurons form several microcircuits in the PFC:first, they are connected with pyramidal neurons (PN) through chemical synapses (FS-PN); second, they are interconnected via chemical and electrical synapses (FS-FS). In addition, FS interneurons also receive synaptic inputs from thalamo-cortical relay neurons, and project to and receive inputs from somatostatin-expressing interneurons. Despite the putative relevance of FS interneurons for neurodevelopmental disease processes such as schizophrenia in humans, to the best of our knowledge, little effort has been exerted to study when and how FS interneurons develop their networks in the PFC.
The development of GABA circuitry is regulated by many factors. Among them are neurotrophins like BDNF and FGF. Neuregulin1(NRG1), a member of the growth factor family, functions in a number of developmental processes 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. Recent studies show that ErbB4is expressed predominantly in interneurons, specifically, in FS interneurons. However, it is largely unknown what roles NRG1-ErbB4signals play during the development of FS interneuronal microcircuits, particularly that mediated by basket cells in the PFC.
Here, with the use of a combination of research disciplines including molecular genetics, biochemistry, and electrophysiology, we demonstrate that in the mouse PFC, FS interneurons were poorly developed in terms of the membrane and network properties during the first postnatal week, both of which exhibited an abrupt maturation during the second postnatal week. The development of FS interneuronal microcircuits persisted throughout early adulthood. NRG1-ErbB4signaling was dispensable for the development of GABAergic synapses and gap junctions formed by FS basket interneurons in vivo. However, activity-dependent GABAergic FS-PN transmissions were disrupted without erbb4. While NRG1-ErbB4signaling was not required for the early development of glutamatergic synapses on FS basket interneurons, it was essential for the maturation of these synapses. Based on these observations, we speculate the following model:NRG1-ErbB4signaling is required for the development of glutamatergic synapses, but not GABAergic synapses. Knock-out of ErbB4leads to hypo-glutamatergic transmissions on FS basket interneurons and reduced activity-dependent GABAergic FS-PN transmissions, thus reducing inhibition mediated by FS basket interneurons. To maintain the appropriate excitation/inhibition (E/I) balance, PN neurons then homeostatically reduce the glutamatergic excitatory synapses. The disruption of E/I balance during adolescence may underlie the etiology of neuropsychiatric disorders like schizophrenia.
引文
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