AMPA受体运输在杏仁外侧核NMDA受体依赖性的突触可塑性调节中的作用
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摘要
学习与记忆是动物和人赖以生存不可缺少的重要脑功能。学习是指获得外界信息的过程,记忆是将获得的信息储存和读出的神经过程。众多研究显示,中枢神经系统内的突触可塑性与学习记忆密切相关,是学习记忆的神经基础之一。中枢神经系统的突触可塑性调节主要有两种模式:长时程增强(long termpotentiation;LTP)和长时程减弱(long term depression;LTD)。一般认为,在研究较为彻底的海马CA1部位,NMDA受体激活后导致的突触后AMPA受体的运输(分泌与内吞)是LTP和LTD诱导表达的主要机制。
近期研究发现LTP和LTD现象也存在于丘脑-杏仁外侧核通路,被认为对和恐惧情绪反应有关的学习与记忆的突触可塑性调节过程有重要作用。但其具体的内在机制目前尚不清楚。因此本课题在杏仁核部位对作为脑内突触可塑性模式的LTP和LTD的神经和细胞分子机制及其与学习记忆的相关性进行了深入系统的研究。第一部分研究了不同模式电刺激丘脑-杏仁外侧核传入纤维通路所诱导的长时程增强(LTP)和长时程减弱(LTD)现象,并观察了不同NMDA受体亚基在诱导中的作用;第二部分研究了突触后AMPA受体的运输是否参与杏仁外侧核部位LTP和LTD的诱导表达。
一、NMDA受体在杏仁外侧核突触可塑性调节中的作用
本部分研究中,用经典的电刺激方法在大鼠脑薄片的丘脑-杏仁外侧核传入通路诱导LTP和LTD,在杏仁外侧核区记录兴奋性突触后电流EPSC。为了进一步确定大鼠杏仁外侧核区LTP/LTD与NMDA受体之间的关系,在电刺激诱导LTP/LTD前,用脑薄片灌流液内给药的方法进行不同的竞争性NMDA受体拮抗剂的预处理,并观察此种拮抗剂是否影响了LTP/LTD的诱导,以确定LTP/LTD诱导发生的受体依赖性过程。
杏仁外侧核(LA)直接接受来自丘脑和皮层的输入,而杏仁核中的神经可塑性调节主要发生在丘脑-LA通路,因此大量关于恐惧记忆形成的细胞和分子机制的研究都集中在这一环路上。在本实验中,高频电刺激(HFS:串长:100;频率:100 Hz;连续刺激3次,串间隔20s)和配对高频电刺激(pairing:串长:200;频率:2Hz;突触后膜电压钳制在-5 mv)丘脑-杏仁外侧核传入纤维通路,均能在杏仁外侧核锥体神经元诱导出稳定的LTP,主要表现为兴奋性突触后电流(EPSC)幅度的增加,并可稳定的维持40-60分钟以上。而低频电刺激(LFS:串长:900;频率:1 Hz)和配对低频电刺激(pairing:串长:480;频率:1 Hz;突触后膜电压钳制在-50 mv)丘脑-杏仁外侧核传入纤维通路,则均能在杏仁外侧核部位诱导出稳定的LTD,主要表现为兴奋性突触后电流(EPSC)幅度的减小,并可稳定的维持40-60分钟以上。
谷氨酸受体(glutamate receptor,GluR)是中枢神经系统内主要的兴奋性神经递质受体。其中,NMDA受体在突触可塑性调节中发挥的重要作用近年愈来愈被重视。本实验将NMDA受体抑制剂D-APV(50uM)加入杏仁核脑薄片的灌流液,预处理20-30分钟后以与对照组相同参数的电刺激分别诱导LTP和LTD,则LTP和LTD现象均不能被诱导发生;用NR2A亚基抑制剂NVP-AAM077(0.4uM)预处理脑薄片,则LTP的诱导被阻断,LTD可正常发生;而用NR2B亚基抑制剂Ro25-6981(3uM)和Ifenprodil(10uM)预处理脑薄片,则LTP可被正常诱导,但LTD的诱导被阻断。以上结果提示杏仁外侧核部位的突触可塑性调节主要为NMDA受体依赖性的突触过程,不同亚基组成的NMDA受体在决定大鼠杏仁核部位突触可塑性的极性方面具有重要作用。
二、AMPA受体的运输参与杏仁外侧核的突触可塑性调节过程
本部分实验采用脑片电生理方法观察丘脑-杏仁外侧核传入通路上LTP诱导表达过程中与膜融合有关的囊泡内受体分泌过程,以及AMPA受体的调节性内吞过程与LTD之间的特异性联系。并使用表面蛋白生物素分析方法(SurfaceBiotinylation Assay)在杏仁外侧核脑薄片上测定AMPA受体的细胞表面表达量,以观察AMPA受体的运输是否参与杏仁外侧核部位LTP和LTD的诱导表达。
中枢神经系统的兴奋性突触传递主要由谷氨酸受体:AMPA受体和NMDA受体介导。而突触传递效率的改变主要取决于突触前膜的神经递质释放量和聚集在突触后膜的相应受体数目。目前认为对突触后膜上的AMPA受体数目进行调控是导致突触可塑性发生的有效途径。在突触后部位利用神经毒素TeTx(含200nM TeTx的细胞内液充灌记录微电极)阻断VAMP蛋白介导的囊泡受体的分泌过程,则LTP的表达被抑制;同样,在突触后部位利用干扰肽GluR2_(3Y)(含100μg/mlGluR2_(3Y)的细胞内液充灌记录微电极)特异性阻断AMPA受体的内吞过程,则LTD的表达被阻断。利用表面蛋白生物素分析、免疫沉淀和免疫印迹等方法测定在杏仁外侧核部位有效诱导LTP或LTD前后,神经元细胞表面上AMPA受体的表达。发现在高频电刺激诱导LTP后,细胞膜表面的AMPA受体表达增加,主要表现为GluR1亚单位表达明显增多;低频电刺激诱导LTD后,细胞膜表面的AMPA受体表达减少,主要表现为细胞膜表面GluR2亚单位的表达显著减少。细胞膜上AMPA受体的数量在诱导LTP/LTD后短时间内发生了显著性变化。提示诱导LTP后可以促进AMPA受体由胞内迁移至细胞膜表面(插膜),而诱导LTD后则可以促进AMPA受体从细胞膜表面移入到胞内(内化)。
本研究证实长时程增强(LTP)和长时程减弱(LTD)现象存在于丘脑-杏仁外侧核通路,它们的诱导发生均需要NMDA受体的参与。含有NR2A亚基的NMDA受体的激活导致LTP的形成,含有NR2B亚基的NMDA受体的激活导致LTD的形成,说明不同亚基组成的NMDA受体在决定大鼠杏仁核部位突触可塑性的极性方面具有重要作用。而杏仁外侧核部位这种NMDA受体依赖性的突触可塑性调节过程需要AMPA受体运输的参与。膜融合依赖性的AMPA受体分泌过程参与LTP的诱导表达,有效诱导LTP后伴随神经元细胞表面AMPA受体的表达增加;而AMPA受体调节性内吞过程参与LTD的诱导表达,有效诱导LTD后伴随神经元表面AMPA受体表达的减少。以上结果表明由NMDA受体介导的AMPA受体的插膜和内吞过程分别是杏仁体外侧核LTP、LTD发生的机制之一,对突触后膜上的AMPA受体数目进行调控是进行突触可塑性改变的有效途径,本研究为阐明杏仁外侧核部位突触可塑性的变化过程提供了可能的分子机制。
Learning and memory are important computational strategies of the brain. They are generally believed to result from changes in synaptic efficacy induced by afferent activity. Long-term potentiation (LTP) and long-term depression (LTD), the two most well characterized forms of synaptic plasticity, are thought to be important for learning and memory in behaving animals. Stimulated exocytosis and endocytosis of postsynaptic alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid subtype of glutamate receptors (AMPARs) have been proposed as primary mechanisms for the expression of hippocampal CA1 long-term potentiation (LTP) and long-term depression (LTD), respectively.
In recent years, LTP and LTD are considered as two forms of synaptic plasticity that underlie the memory storage at sensory input synapses to the lateral amygdala (LA) during fear conditioning. However, the detailed underlying mechanisms especially the role of AMPAR trafficking in the expression of either LTP or LTD in this structure is still unknown. In the present study, we first observe the expression of LTP and LTD at thalamic input synapses induced by two different protocols in vitro and the effect of N-methy-D-aspartate receptors (NMDARs) blocked during LTP and LTD, to study the candidate mechanism for learning and memory during fear conditioning. Then we observe weather the induction protocols of LTP and LTD could increased or decreased the surface expression of AMPARs, thus NMDAR mediated AMPAR traffickings are responsible for the expression of LTP and LTD in the LA.
1. NMDA receptors contribute to Long-term potentiation and long-term depression in the lateral amygdala
Both LTP and LTD can also be induced in the lateral amygdala (LA), a critical structure involved in fear conditioning. Here we show that, using standard LTP or LTD stimulation protocols, N-methy-D-aspartate receptor (NMDAR)-dependent LTP and LTD can be reliably induced at the synapses of the auditory thalamic inputs to the LA in brain slices. High frequency stimulation (HFS: 3 episodes of 100 pulses at 100 Hz) could induce stable LTP, which could last for 40-60 min after the induction in fresh brain slices. While pairing protocol (200 pulses at 2Hz while depolarizing the cell to -5mv ) can induced more robust LTP in the LA. Stable and persistent LTD can be induced by low frequency stimulation (LFS: 900 pulses at 1 Hz) and paired protocol (delivering 480 pulses at 1Hz while holding potential was at -50 mv). Activation of NMDA receptors (NMDARs) is required for LTP and LTD of excitatory synaptic transmission at lateral amygdala synapses. Bath application of D-APV (50μM) during the recording can blocked the induction of LTP and LTD. Selectively blocking NMDARs that contain the NR2B subunit by the NR2B subunit-selective antagonist ifenprodil (3μM) or Ro25-6981 (0.5μM) can abolish the induction of LTD but not LTP. In contrast, preferential inhibition of NR2A-containing NMDARs by NVP-AAM077 (0.4μM) prevents the induction of LTP without affecting the induction of LTD.
2. AMPA receptor trafficking is required for NMDA-dependent synaptic plasticity in the lateral amygdala
It is generally agreed that postsynaptic changes in the number of surface AMPA receptors play an important role in synaptic plasticity. NMDAR mediated AMPAR trafficking is at least one of the mechanisms for the expression of LTP and LTD. Here we show that the expression of the bidirectional synaptic plasticity in the LA was also mediated by the trafficking of postsynaptic AMPARs. Postsynaptic application of a light chain of Clostridium tetanus neurotoxin (TeTx) which selectively cleaves vesicle-associated membrane proteins (VAMP) eliminated the expression of LTP, while postsynaptic application of a GluR2-derived interfering peptide which selectively blocks the stimulated clathrin-dependent regulated AMPAR endocytosis prevented the induction of LTD. The level of AMPAR subunits in the LA was examined following HFS or LFS stimulation by surface biotinylation assay, a quantification of the average density of individual band obtained by western blots. Biotinylation data also showed that the induction protocols of LTP or LTD respectively increased or decreased the surface expression of AMPARs.
Results of the present study showed the induction of LTP and LTD at the synapses of the auditory thalamic inputs to the LA in brain slices were dependent upon NMDARs. Distinct NMDARs of different subunit composition have critical roles in determining the polarity of synaptic plasticity in lateral amygdala synapses of adult rats. The activation of NR2A-containing NMDARs leads to LTP formation, while the activation of NR2B-containing NMDARs produces LTD. The membrane fusion-dependent exocytosis plays an important role in the LTP expression and regulated AMPAR endocytosis is required for the NMDAR-dependent LTD. A rapid increase of AMPAR surface expression is responsible for the rise of transmission efficacy during LTP, while a rapid endocytotic-dependent decrease in the number of surface AMPARs accounts for LTD expression. This regulated change in the trafficking of postsynaptic AMPA receptors may serve as a common mechanism for synaptic strength alteration during synaptic plasticity in the central nerve system. The results of present study strongly suggest that NMDAR mediated AMPAR trafficking is at least one of the mechanisms for the expression of LTP and LTD in the LA.
近期研究发现LTP和LTD现象也存在于丘脑-杏仁外侧核通路,被认为对和恐惧情绪反应有关的学习与记忆的突触可塑性调节过程有重要作用。但其具体的内在机制目前尚不清楚。因此本课题在杏仁核部位对作为脑内突触可塑性模式的LTP和LTD的神经和细胞分子机制及其与学习记忆的相关性进行了深入系统的研究。第一部分研究了不同模式电刺激丘脑-杏仁外侧核传入纤维通路所诱导的长时程增强(LTP)和长时程减弱(LTD)现象,并观察了不同NMDA受体亚基在诱导中的作用;第二部分研究了突触后AMPA受体的运输是否参与杏仁外侧核部位LTP和LTD的诱导表达。
一、NMDA受体在杏仁外侧核突触可塑性调节中的作用
本部分研究中,用经典的电刺激方法在大鼠脑薄片的丘脑-杏仁外侧核传入通路诱导LTP和LTD,在杏仁外侧核区记录兴奋性突触后电流EPSC。为了进一步确定大鼠杏仁外侧核区LTP/LTD与NMDA受体之间的关系,在电刺激诱导LTP/LTD前,用脑薄片灌流液内给药的方法进行不同的竞争性NMDA受体拮抗剂的预处理,并观察此种拮抗剂是否影响了LTP/LTD的诱导,以确定LTP/LTD诱导发生的受体依赖性过程。
杏仁外侧核(LA)直接接受来自丘脑和皮层的输入,而杏仁核中的神经可塑性调节主要发生在丘脑-LA通路,因此大量关于恐惧记忆形成的细胞和分子机制的研究都集中在这一环路上。在本实验中,高频电刺激(HFS:串长:100;频率:100 Hz;连续刺激3次,串间隔20s)和配对高频电刺激(pairing:串长:200;频率:2Hz;突触后膜电压钳制在-5 mv)丘脑-杏仁外侧核传入纤维通路,均能在杏仁外侧核锥体神经元诱导出稳定的LTP,主要表现为兴奋性突触后电流(EPSC)幅度的增加,并可稳定的维持40-60分钟以上。而低频电刺激(LFS:串长:900;频率:1 Hz)和配对低频电刺激(pairing:串长:480;频率:1 Hz;突触后膜电压钳制在-50 mv)丘脑-杏仁外侧核传入纤维通路,则均能在杏仁外侧核部位诱导出稳定的LTD,主要表现为兴奋性突触后电流(EPSC)幅度的减小,并可稳定的维持40-60分钟以上。
谷氨酸受体(glutamate receptor,GluR)是中枢神经系统内主要的兴奋性神经递质受体。其中,NMDA受体在突触可塑性调节中发挥的重要作用近年愈来愈被重视。本实验将NMDA受体抑制剂D-APV(50uM)加入杏仁核脑薄片的灌流液,预处理20-30分钟后以与对照组相同参数的电刺激分别诱导LTP和LTD,则LTP和LTD现象均不能被诱导发生;用NR2A亚基抑制剂NVP-AAM077(0.4uM)预处理脑薄片,则LTP的诱导被阻断,LTD可正常发生;而用NR2B亚基抑制剂Ro25-6981(3uM)和Ifenprodil(10uM)预处理脑薄片,则LTP可被正常诱导,但LTD的诱导被阻断。以上结果提示杏仁外侧核部位的突触可塑性调节主要为NMDA受体依赖性的突触过程,不同亚基组成的NMDA受体在决定大鼠杏仁核部位突触可塑性的极性方面具有重要作用。
二、AMPA受体的运输参与杏仁外侧核的突触可塑性调节过程
本部分实验采用脑片电生理方法观察丘脑-杏仁外侧核传入通路上LTP诱导表达过程中与膜融合有关的囊泡内受体分泌过程,以及AMPA受体的调节性内吞过程与LTD之间的特异性联系。并使用表面蛋白生物素分析方法(SurfaceBiotinylation Assay)在杏仁外侧核脑薄片上测定AMPA受体的细胞表面表达量,以观察AMPA受体的运输是否参与杏仁外侧核部位LTP和LTD的诱导表达。
中枢神经系统的兴奋性突触传递主要由谷氨酸受体:AMPA受体和NMDA受体介导。而突触传递效率的改变主要取决于突触前膜的神经递质释放量和聚集在突触后膜的相应受体数目。目前认为对突触后膜上的AMPA受体数目进行调控是导致突触可塑性发生的有效途径。在突触后部位利用神经毒素TeTx(含200nM TeTx的细胞内液充灌记录微电极)阻断VAMP蛋白介导的囊泡受体的分泌过程,则LTP的表达被抑制;同样,在突触后部位利用干扰肽GluR2_(3Y)(含100μg/mlGluR2_(3Y)的细胞内液充灌记录微电极)特异性阻断AMPA受体的内吞过程,则LTD的表达被阻断。利用表面蛋白生物素分析、免疫沉淀和免疫印迹等方法测定在杏仁外侧核部位有效诱导LTP或LTD前后,神经元细胞表面上AMPA受体的表达。发现在高频电刺激诱导LTP后,细胞膜表面的AMPA受体表达增加,主要表现为GluR1亚单位表达明显增多;低频电刺激诱导LTD后,细胞膜表面的AMPA受体表达减少,主要表现为细胞膜表面GluR2亚单位的表达显著减少。细胞膜上AMPA受体的数量在诱导LTP/LTD后短时间内发生了显著性变化。提示诱导LTP后可以促进AMPA受体由胞内迁移至细胞膜表面(插膜),而诱导LTD后则可以促进AMPA受体从细胞膜表面移入到胞内(内化)。
本研究证实长时程增强(LTP)和长时程减弱(LTD)现象存在于丘脑-杏仁外侧核通路,它们的诱导发生均需要NMDA受体的参与。含有NR2A亚基的NMDA受体的激活导致LTP的形成,含有NR2B亚基的NMDA受体的激活导致LTD的形成,说明不同亚基组成的NMDA受体在决定大鼠杏仁核部位突触可塑性的极性方面具有重要作用。而杏仁外侧核部位这种NMDA受体依赖性的突触可塑性调节过程需要AMPA受体运输的参与。膜融合依赖性的AMPA受体分泌过程参与LTP的诱导表达,有效诱导LTP后伴随神经元细胞表面AMPA受体的表达增加;而AMPA受体调节性内吞过程参与LTD的诱导表达,有效诱导LTD后伴随神经元表面AMPA受体表达的减少。以上结果表明由NMDA受体介导的AMPA受体的插膜和内吞过程分别是杏仁体外侧核LTP、LTD发生的机制之一,对突触后膜上的AMPA受体数目进行调控是进行突触可塑性改变的有效途径,本研究为阐明杏仁外侧核部位突触可塑性的变化过程提供了可能的分子机制。
Learning and memory are important computational strategies of the brain. They are generally believed to result from changes in synaptic efficacy induced by afferent activity. Long-term potentiation (LTP) and long-term depression (LTD), the two most well characterized forms of synaptic plasticity, are thought to be important for learning and memory in behaving animals. Stimulated exocytosis and endocytosis of postsynaptic alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid subtype of glutamate receptors (AMPARs) have been proposed as primary mechanisms for the expression of hippocampal CA1 long-term potentiation (LTP) and long-term depression (LTD), respectively.
In recent years, LTP and LTD are considered as two forms of synaptic plasticity that underlie the memory storage at sensory input synapses to the lateral amygdala (LA) during fear conditioning. However, the detailed underlying mechanisms especially the role of AMPAR trafficking in the expression of either LTP or LTD in this structure is still unknown. In the present study, we first observe the expression of LTP and LTD at thalamic input synapses induced by two different protocols in vitro and the effect of N-methy-D-aspartate receptors (NMDARs) blocked during LTP and LTD, to study the candidate mechanism for learning and memory during fear conditioning. Then we observe weather the induction protocols of LTP and LTD could increased or decreased the surface expression of AMPARs, thus NMDAR mediated AMPAR traffickings are responsible for the expression of LTP and LTD in the LA.
1. NMDA receptors contribute to Long-term potentiation and long-term depression in the lateral amygdala
Both LTP and LTD can also be induced in the lateral amygdala (LA), a critical structure involved in fear conditioning. Here we show that, using standard LTP or LTD stimulation protocols, N-methy-D-aspartate receptor (NMDAR)-dependent LTP and LTD can be reliably induced at the synapses of the auditory thalamic inputs to the LA in brain slices. High frequency stimulation (HFS: 3 episodes of 100 pulses at 100 Hz) could induce stable LTP, which could last for 40-60 min after the induction in fresh brain slices. While pairing protocol (200 pulses at 2Hz while depolarizing the cell to -5mv ) can induced more robust LTP in the LA. Stable and persistent LTD can be induced by low frequency stimulation (LFS: 900 pulses at 1 Hz) and paired protocol (delivering 480 pulses at 1Hz while holding potential was at -50 mv). Activation of NMDA receptors (NMDARs) is required for LTP and LTD of excitatory synaptic transmission at lateral amygdala synapses. Bath application of D-APV (50μM) during the recording can blocked the induction of LTP and LTD. Selectively blocking NMDARs that contain the NR2B subunit by the NR2B subunit-selective antagonist ifenprodil (3μM) or Ro25-6981 (0.5μM) can abolish the induction of LTD but not LTP. In contrast, preferential inhibition of NR2A-containing NMDARs by NVP-AAM077 (0.4μM) prevents the induction of LTP without affecting the induction of LTD.
2. AMPA receptor trafficking is required for NMDA-dependent synaptic plasticity in the lateral amygdala
It is generally agreed that postsynaptic changes in the number of surface AMPA receptors play an important role in synaptic plasticity. NMDAR mediated AMPAR trafficking is at least one of the mechanisms for the expression of LTP and LTD. Here we show that the expression of the bidirectional synaptic plasticity in the LA was also mediated by the trafficking of postsynaptic AMPARs. Postsynaptic application of a light chain of Clostridium tetanus neurotoxin (TeTx) which selectively cleaves vesicle-associated membrane proteins (VAMP) eliminated the expression of LTP, while postsynaptic application of a GluR2-derived interfering peptide which selectively blocks the stimulated clathrin-dependent regulated AMPAR endocytosis prevented the induction of LTD. The level of AMPAR subunits in the LA was examined following HFS or LFS stimulation by surface biotinylation assay, a quantification of the average density of individual band obtained by western blots. Biotinylation data also showed that the induction protocols of LTP or LTD respectively increased or decreased the surface expression of AMPARs.
Results of the present study showed the induction of LTP and LTD at the synapses of the auditory thalamic inputs to the LA in brain slices were dependent upon NMDARs. Distinct NMDARs of different subunit composition have critical roles in determining the polarity of synaptic plasticity in lateral amygdala synapses of adult rats. The activation of NR2A-containing NMDARs leads to LTP formation, while the activation of NR2B-containing NMDARs produces LTD. The membrane fusion-dependent exocytosis plays an important role in the LTP expression and regulated AMPAR endocytosis is required for the NMDAR-dependent LTD. A rapid increase of AMPAR surface expression is responsible for the rise of transmission efficacy during LTP, while a rapid endocytotic-dependent decrease in the number of surface AMPARs accounts for LTD expression. This regulated change in the trafficking of postsynaptic AMPA receptors may serve as a common mechanism for synaptic strength alteration during synaptic plasticity in the central nerve system. The results of present study strongly suggest that NMDAR mediated AMPAR trafficking is at least one of the mechanisms for the expression of LTP and LTD in the LA.
引文
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