吗啡成瘾对海马组合突触可塑性的影响
摘要
物质成瘾主要特征为持续地、失去控制地对成瘾物质的渴求,以及持续的复吸倾向。由于这些特征,物质成瘾的临床治疗显得困难重重。尽管物质成瘾的主要理论各持所见,但均认可与成瘾物质使用相关的环境线索,在触发对成瘾物质的渴求和复吸行为中起了重要作用,类似于条件化环境线索对成瘾记忆的提取。
海马在环境线索相关的学习记忆中起着重要作用。海马突触可塑性,主要是指活动或经验依赖的长时程增强(Long-term potentiation,LTP)和长时程抑制(Long-term depression,LTD),被认为是海马依赖的学习与记忆的细胞分子基础。既往吗啡成瘾对海马突触可塑性影响的研究,常常是以记录单个通路的突触效能改变为基础(例如低频刺激诱导LTD、高频刺激诱导LTP),进而阐明突触可塑性在成瘾行为中的作用及其可能的机制。然而,学习记忆的行为学研究往往采用两种事件的条件化训练来进行,如经典的条件反射是通过条件刺激和非条件刺激来建立联合型学习。在动物实验中运动敏感化是常见的成瘾模型,由于环境线索和成瘾物质使用建立的联合型学习,运动敏感化往往只有在条件化环境中才能有效表达。最近研究进展表明,大鼠海马Schaffer-CA1双通路也存在类似于经典条件反射的联合型学习记忆规律,两个通路之间在一定时间内的协同作用,可在两个通路同时诱导出LTP和LTD,呈现为海马组合突触可塑性,体现了海马突触可塑性可能在学习记忆的编码过程中具有灵活性与稳定性的特点。鉴于条件化环境线索在成瘾记忆提取中的重要作用,我们认为基于双通路条件化作用的海马组合突触可塑性可能在成瘾过程中发挥着重要作用。
本研究采用了活体电生理、行为学、生化等方法,进行了了三方面研究:(1)以海马Schaffer-CA1双通路技术为基础,研究了大鼠Schaffer-CA1组合突触可塑性的分布特点;(2)在此基础上,研究了吗啡成瘾对大鼠Schaffer-CA1双通路组合突触可塑性的影响;(3)研究了吗啡反复戒断对大鼠Schaffer-CA1双通路组合突触可塑性以及大鼠行为敏感化的影响,并采用了免疫印迹法(Western Blotting)测定AMPAR(α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor)的GluR1(Glutamate receptor1)及GluR2/3(Glutamate receptor2/3)亚单位,在一次戒断、三次戒断后在大鼠海马膜蛋白及突触小体的表达。
在第一部分海马组合突触可塑性实验中,我们首次证实了海马突触可塑性在Schaffer-CA1双通路上呈现出四种组合:LTD/LTD,LTP/LTP,LTP/LTD,LTD/LTP。这表明了在信息编码过程中,LTP及LTD可能同时存在,呈现组合可塑性的特点,提供了信息处理过程中的稳定性,避免单一LTP或LTD产生时导致过度兴奋或抑制,同时由于不同突触的不同组合也提供了信息处理的灵活性。因此,推测信息加工可能是各种形式LTD与LTP的组合过程,类似于数字0,1进行组合编码。这种组合编码似乎更加合理,因为它有助于提高记忆编码效率及记忆容量,并有利于突触权重(Synaptic weight)的精确调节。
在第二部分实验中,我们首次将海马Schaffer-CA1双通路技术应用于吗啡成瘾的研究,我们发现慢性吗啡处理易化了LTD(LTD/LTD),伴随着吗啡戒断易化的LTD出现恢复的趋势,在戒断第四天逆转为LTP/LTD。我们认为这反映了突触效能的内稳态性适应(Homeostatic adaptations)过程,有利于吸毒和戒断相关线索建立条件化(Contextual conditioning),形成牢固的物质成瘾记忆。由于LTP/LTD组合可塑性能被NMDAR(N-methyl-D-aspartatereceptor)及D1/D5多巴胺受体阻断剂完全阻断,提示了通过激活多巴胺系统D1/D5受体,调控了谷氨酸系统的突触可塑性,可能是环境线索相关成瘾记忆的分子机制。
第三部分海马组合可塑性实验中,我们首次证实了三次戒断后LTP比一次戒断后的LTP幅值更大,持续更久,并表现为LTP/LTP组合;在行为敏感化实验中发现,三次戒断大鼠的自发活动均多于一次戒断(GluR1及GluR2/3在海马膜蛋白及突触小体表达的数据正在整理中)。结果提示多次戒断可进一步加强条件化环境线索相关的成瘾记忆,增强大鼠的觅药动机。进一步说明了戒断后的存在关键时间窗,促进了条件化环境线索相关成瘾记忆的形成,如能阻断LTP的形成,可能会熄灭环境线索相关联的成瘾记忆,从而减少条件化环境线索诱发的复吸行为。
Drug addiction is characterized by persistent and compulsive drug craving, drug seeking and persistence tendency to relapse, which is the major problem hampering clinical treatment of drug addiction. Ample evidence adds to a growing consensus that drug-associated contextual cues play an important role in triggering drug craving and relapse and the retrieval of addiction memory by conditioned contextual cues may be the underlying mechanism.
Hippocampus is known to be critical for the formation of certain type of memory including contextual cues-associated addiction memory. Hippocampal activity-dependent or experience-dependent synaptic plasticity, including Long-term potentiation (LTP) and Long-term depression (LTD), is believed to be the cellular and molecular mechanism which underlies hippocampus-dependent learning and memory. Hippocampal synaptic plasticity in the studies of morphine addiction is often examined by using one pathway recording technique, in which LTD is induced by low frequency stimulation (LFS) and LTP is induced by high frequency simulation (HFS). The results of those studies suggest that there should be a crosstalk between the potentiation or depression of hippocampal synaptic plasticity and the mechanism of addictive behavior. However behavioral learning, e.g. the classic conditioning, is based on the association between conditioned and unconditioned stimuli and in the experiment of locomotor sensitization to morphine, locomotor sensitization may be expressed sucessfully only in the conditioned context, which is based on unconditioned stimulus (morphine injection) in the conditioned environment (open field). Recent study indicates that hippocampal combinatorial synaptic plasticity can be induced by a similar conditioning procedure that conditioned stimuli between two Schaffer-CA1 pathways within a certain timing window induces LTP and LTD simultaneously, which illustrates the flexibility and stability of hippocampal synaptic plasticity. Since conditioned contextual cues may make critical contribution to relapse, hippocampal combinatorial synaptic plasticity based on conditioning of two pathways should be a candidate mechanism for long-lasting and unforgettable addiction memory.
In the present study, using in vivo electrophysiological, behavioral and biochemical methods, we carried out three sets of experiments. In the first set of experiments, we examined the distribution of hippocampal combinatorial synaptic plasticity in two converging Schaffer-CA1 pathways in rat; in the second set of experiments, we examined the effects of morphine addiction on hippocampal combinatorial synaptic plasticity; in the third set of experiments, we examined the effects of repetitive withdrawal on hippocampal combinatorial synaptic plasticity. We also used immunoblots (Western Blotting) to asses the expression of GluR1 (Glutamate receptor1) and GluR2/3 (Glutamate receptor2/3) subunits of the AMPAR, which is the major receptor responsible for the expression and maintenance of LTP and LTD, in the total membrane fraction and the synaptosome fractions of the hippocampus after one time and third times of morphine withdrawal.
In the first set of experiment, we demonstrated for first time that there are four types of combinatorial synaptic plasticity, i.e. LTD/LTD, LTP/LTD, LTD/LTP and LTP/LTP. The results implicate that LTD and LTP may coexist and concomitantly encode information, which provides the stability of the hippocampal synaptic plasticity and makes contribution to limit the tendency to drive synaptic strength towards potentially epileptogenic level of LTP or minimum value and shows the flexibility of encoding process which may be similar to encoding information by digital 0 and 1. Combinatorial plasticity may encode the information more efficiently and may enhance the capacity for the storage of memory traces compared with encoding process mediated by LTP or LTD independently, which provide the possibility to reset synaptic weight and update synaptic configuration delicately.
In the second set of experiment, we first introduced the dual Schaffer-CA1 pathways experiments to examine hippocampal combinatorial synaptic plasticity after repeated morphine exposure. We observed that repeated morphine exposure facilitated LTD (LTD/LTD), which was gradually restored following morphine withdrawal. However on withdrawal day 4, LTP/LTD was induced. Thus, from drug taking to withdrawal, homeostatic adaptations and contextual conditioning may be the mechanism underlying contextual cues-associated addiction memory. Since LTD or LTP was fully blocked by antagonists to NMDAR and D1/D5 receptors, it seems that morphine may employ dopamine system to modulate glutamatergic LTP and LTD which may be the molecular mechanism of the conditioned contextual cues which can retrieve addiction memory.
In the third set of experiments, we demonstrated for first time that LTP after three times of withdrawal was enhanced as compared with that after one time of withdrawal and combinatorial plasticity was remarkable LTP/LTP as compared with LTP/LTD after one time of withdrawal. Consistent with this result, locomotor activity after three times of withdrawal was largely increased as compared with that after one time of withdrawal. The data of the expression of GluR1 and GluR2/3 are in preparation. Our findings suggest that the more times of withdrawal, the more possibilities of combinatorial plasticity would be LTP/LTP that may be responsible for stronger contextual cues-associated addiction memory and drug-seeking behavior. These results reveal that acute withdrawal may be critical in the formation of contextual cues-associated addiction memory and effective block of hippocampal LTP induction may contribute to the extinction of contextual cues-associated addiction memory and thereby decrease the tendency to relapse evoked by conditioned contextual cues.
海马在环境线索相关的学习记忆中起着重要作用。海马突触可塑性,主要是指活动或经验依赖的长时程增强(Long-term potentiation,LTP)和长时程抑制(Long-term depression,LTD),被认为是海马依赖的学习与记忆的细胞分子基础。既往吗啡成瘾对海马突触可塑性影响的研究,常常是以记录单个通路的突触效能改变为基础(例如低频刺激诱导LTD、高频刺激诱导LTP),进而阐明突触可塑性在成瘾行为中的作用及其可能的机制。然而,学习记忆的行为学研究往往采用两种事件的条件化训练来进行,如经典的条件反射是通过条件刺激和非条件刺激来建立联合型学习。在动物实验中运动敏感化是常见的成瘾模型,由于环境线索和成瘾物质使用建立的联合型学习,运动敏感化往往只有在条件化环境中才能有效表达。最近研究进展表明,大鼠海马Schaffer-CA1双通路也存在类似于经典条件反射的联合型学习记忆规律,两个通路之间在一定时间内的协同作用,可在两个通路同时诱导出LTP和LTD,呈现为海马组合突触可塑性,体现了海马突触可塑性可能在学习记忆的编码过程中具有灵活性与稳定性的特点。鉴于条件化环境线索在成瘾记忆提取中的重要作用,我们认为基于双通路条件化作用的海马组合突触可塑性可能在成瘾过程中发挥着重要作用。
本研究采用了活体电生理、行为学、生化等方法,进行了了三方面研究:(1)以海马Schaffer-CA1双通路技术为基础,研究了大鼠Schaffer-CA1组合突触可塑性的分布特点;(2)在此基础上,研究了吗啡成瘾对大鼠Schaffer-CA1双通路组合突触可塑性的影响;(3)研究了吗啡反复戒断对大鼠Schaffer-CA1双通路组合突触可塑性以及大鼠行为敏感化的影响,并采用了免疫印迹法(Western Blotting)测定AMPAR(α-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor)的GluR1(Glutamate receptor1)及GluR2/3(Glutamate receptor2/3)亚单位,在一次戒断、三次戒断后在大鼠海马膜蛋白及突触小体的表达。
在第一部分海马组合突触可塑性实验中,我们首次证实了海马突触可塑性在Schaffer-CA1双通路上呈现出四种组合:LTD/LTD,LTP/LTP,LTP/LTD,LTD/LTP。这表明了在信息编码过程中,LTP及LTD可能同时存在,呈现组合可塑性的特点,提供了信息处理过程中的稳定性,避免单一LTP或LTD产生时导致过度兴奋或抑制,同时由于不同突触的不同组合也提供了信息处理的灵活性。因此,推测信息加工可能是各种形式LTD与LTP的组合过程,类似于数字0,1进行组合编码。这种组合编码似乎更加合理,因为它有助于提高记忆编码效率及记忆容量,并有利于突触权重(Synaptic weight)的精确调节。
在第二部分实验中,我们首次将海马Schaffer-CA1双通路技术应用于吗啡成瘾的研究,我们发现慢性吗啡处理易化了LTD(LTD/LTD),伴随着吗啡戒断易化的LTD出现恢复的趋势,在戒断第四天逆转为LTP/LTD。我们认为这反映了突触效能的内稳态性适应(Homeostatic adaptations)过程,有利于吸毒和戒断相关线索建立条件化(Contextual conditioning),形成牢固的物质成瘾记忆。由于LTP/LTD组合可塑性能被NMDAR(N-methyl-D-aspartatereceptor)及D1/D5多巴胺受体阻断剂完全阻断,提示了通过激活多巴胺系统D1/D5受体,调控了谷氨酸系统的突触可塑性,可能是环境线索相关成瘾记忆的分子机制。
第三部分海马组合可塑性实验中,我们首次证实了三次戒断后LTP比一次戒断后的LTP幅值更大,持续更久,并表现为LTP/LTP组合;在行为敏感化实验中发现,三次戒断大鼠的自发活动均多于一次戒断(GluR1及GluR2/3在海马膜蛋白及突触小体表达的数据正在整理中)。结果提示多次戒断可进一步加强条件化环境线索相关的成瘾记忆,增强大鼠的觅药动机。进一步说明了戒断后的存在关键时间窗,促进了条件化环境线索相关成瘾记忆的形成,如能阻断LTP的形成,可能会熄灭环境线索相关联的成瘾记忆,从而减少条件化环境线索诱发的复吸行为。
Drug addiction is characterized by persistent and compulsive drug craving, drug seeking and persistence tendency to relapse, which is the major problem hampering clinical treatment of drug addiction. Ample evidence adds to a growing consensus that drug-associated contextual cues play an important role in triggering drug craving and relapse and the retrieval of addiction memory by conditioned contextual cues may be the underlying mechanism.
Hippocampus is known to be critical for the formation of certain type of memory including contextual cues-associated addiction memory. Hippocampal activity-dependent or experience-dependent synaptic plasticity, including Long-term potentiation (LTP) and Long-term depression (LTD), is believed to be the cellular and molecular mechanism which underlies hippocampus-dependent learning and memory. Hippocampal synaptic plasticity in the studies of morphine addiction is often examined by using one pathway recording technique, in which LTD is induced by low frequency stimulation (LFS) and LTP is induced by high frequency simulation (HFS). The results of those studies suggest that there should be a crosstalk between the potentiation or depression of hippocampal synaptic plasticity and the mechanism of addictive behavior. However behavioral learning, e.g. the classic conditioning, is based on the association between conditioned and unconditioned stimuli and in the experiment of locomotor sensitization to morphine, locomotor sensitization may be expressed sucessfully only in the conditioned context, which is based on unconditioned stimulus (morphine injection) in the conditioned environment (open field). Recent study indicates that hippocampal combinatorial synaptic plasticity can be induced by a similar conditioning procedure that conditioned stimuli between two Schaffer-CA1 pathways within a certain timing window induces LTP and LTD simultaneously, which illustrates the flexibility and stability of hippocampal synaptic plasticity. Since conditioned contextual cues may make critical contribution to relapse, hippocampal combinatorial synaptic plasticity based on conditioning of two pathways should be a candidate mechanism for long-lasting and unforgettable addiction memory.
In the present study, using in vivo electrophysiological, behavioral and biochemical methods, we carried out three sets of experiments. In the first set of experiments, we examined the distribution of hippocampal combinatorial synaptic plasticity in two converging Schaffer-CA1 pathways in rat; in the second set of experiments, we examined the effects of morphine addiction on hippocampal combinatorial synaptic plasticity; in the third set of experiments, we examined the effects of repetitive withdrawal on hippocampal combinatorial synaptic plasticity. We also used immunoblots (Western Blotting) to asses the expression of GluR1 (Glutamate receptor1) and GluR2/3 (Glutamate receptor2/3) subunits of the AMPAR, which is the major receptor responsible for the expression and maintenance of LTP and LTD, in the total membrane fraction and the synaptosome fractions of the hippocampus after one time and third times of morphine withdrawal.
In the first set of experiment, we demonstrated for first time that there are four types of combinatorial synaptic plasticity, i.e. LTD/LTD, LTP/LTD, LTD/LTP and LTP/LTP. The results implicate that LTD and LTP may coexist and concomitantly encode information, which provides the stability of the hippocampal synaptic plasticity and makes contribution to limit the tendency to drive synaptic strength towards potentially epileptogenic level of LTP or minimum value and shows the flexibility of encoding process which may be similar to encoding information by digital 0 and 1. Combinatorial plasticity may encode the information more efficiently and may enhance the capacity for the storage of memory traces compared with encoding process mediated by LTP or LTD independently, which provide the possibility to reset synaptic weight and update synaptic configuration delicately.
In the second set of experiment, we first introduced the dual Schaffer-CA1 pathways experiments to examine hippocampal combinatorial synaptic plasticity after repeated morphine exposure. We observed that repeated morphine exposure facilitated LTD (LTD/LTD), which was gradually restored following morphine withdrawal. However on withdrawal day 4, LTP/LTD was induced. Thus, from drug taking to withdrawal, homeostatic adaptations and contextual conditioning may be the mechanism underlying contextual cues-associated addiction memory. Since LTD or LTP was fully blocked by antagonists to NMDAR and D1/D5 receptors, it seems that morphine may employ dopamine system to modulate glutamatergic LTP and LTD which may be the molecular mechanism of the conditioned contextual cues which can retrieve addiction memory.
In the third set of experiments, we demonstrated for first time that LTP after three times of withdrawal was enhanced as compared with that after one time of withdrawal and combinatorial plasticity was remarkable LTP/LTP as compared with LTP/LTD after one time of withdrawal. Consistent with this result, locomotor activity after three times of withdrawal was largely increased as compared with that after one time of withdrawal. The data of the expression of GluR1 and GluR2/3 are in preparation. Our findings suggest that the more times of withdrawal, the more possibilities of combinatorial plasticity would be LTP/LTP that may be responsible for stronger contextual cues-associated addiction memory and drug-seeking behavior. These results reveal that acute withdrawal may be critical in the formation of contextual cues-associated addiction memory and effective block of hippocampal LTP induction may contribute to the extinction of contextual cues-associated addiction memory and thereby decrease the tendency to relapse evoked by conditioned contextual cues.
引文
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