Behavioral Role of the Reciprocal Inhibition between a Pair of Mauthner Cells during Fast Escapes in Zebrafish

Behavioral Role of the Reciprocal Inhibition between a Pair of Mauthner Cells during Fast Escapes in Zebrafish
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DOI:
10.1523/jneurosci.1964-18.2018
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发表时间:
2019-02
期刊:
The Journal of Neuroscience
影响因子:
--
通讯作者:
Takashi Shimazaki;M. Tanimoto;Y. Oda;S. Higashijima
Takashi Shimazaki;M. Tanimoto;Y. Oda;S. Higashijima
中科院分区:
其他
文献类型:
--
作者:
Takashi Shimazaki;M. Tanimoto;Y. Oda;S. Higashijima

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在脊椎动物的许多行为中,中枢神经系统在左右两侧产生不对称的活动,从而产生不对称的身体运动。对于CNS的不对称激活,认为左右侧之间的相互抑制起关键作用。然而,中枢神经系统的复杂性使得很难在单个细胞水平上识别相互抑制回路以及每个神经元对不对称活动的贡献。利用斑马鱼幼体,我们通过研究一对Mauthner(M)细胞之间的相互抑制回路来研究这个问题,Mauthner(M)细胞是触发快速逃逸的巨大网状脊髓神经元。先前的研究表明,一类兴奋性神经元,称为颅中继神经元,参与M细胞之间的相互抑制通路。使用转基因鱼,其中两个颅中继神经元(Ta 1和Ta 2)表达GFP,我们表明,Ta 1和Ta 2构成的途径的主要部分。在Ta 1/Ta 2被激光烧蚀的幼虫中,相互IPSPs的幅度下降到不到三分之一。钙成像和电生理记录表明,在Ta 1/Ta 2消融的幼虫中,声/振动刺激时双侧M细胞激活的发生概率大大增加。行为实验表明,Ta 1/Ta 2消融导致在声音/振动诱发的逃逸过程中身体弯曲较浅,这与观察结果一致,即双侧M细胞激活的发生率增加会损害逃逸性能。我们的研究揭示了M细胞系统中相互抑制回路的主要组成部分及其行为重要性。显著性声明CNS左右侧之间的相互抑制被认为是动物产生不对称运动的必要条件。然而,很难在单个细胞水平上识别电路及其在行为中的作用。在这里,我们解决这个问题,通过检查的相互抑制回路的后脑Mauthner(M)细胞系统在斑马鱼幼虫。我们确定,两个配对的中间神经元之间的配对M细胞的相互抑制中发挥了关键作用,相互抑制防止双边发射的M细胞,因此是必要的全身弯曲在M细胞启动的逃生。此外,我们讨论了合作的多种相互抑制工作在后脑和脊髓,以确保高性能的逃生。
During many behaviors in vertebrates, the CNS generates asymmetric activities between the left and right sides to produce asymmetric body movements. For asymmetrical activations of the CNS, reciprocal inhibition between the left and right sides is believed to play a key role. However, the complexity of the CNS makes it difficult to identify the reciprocal inhibition circuits at the level of individual cells and the contribution of each neuron to the asymmetric activity. Using larval zebrafish, we examined this issue by investigating reciprocal inhibition circuits between a pair of Mauthner (M) cells, giant reticulospinal neurons that trigger fast escapes. Previous studies have shown that a class of excitatory neurons, called cranial relay neurons, is involved in the reciprocal inhibition pathway between the M cells. Using transgenic fish, in which two of the cranial relay neurons (Ta1 and Ta2) expressed GFP, we showed that Ta1 and Ta2 constitute major parts of the pathway. In larvae in which Ta1/Ta2 were laser-ablated, the amplitude of the reciprocal IPSPs dropped to less than one-third. Calcium imaging and electrophysiological recording showed that the occurrence probability of bilateral M-cell activation upon sound/vibration stimuli was greatly increased in the Ta1/Ta2-ablated larvae. Behavioral experiments revealed that the Ta1/Ta2 ablation resulted in shallower body bends during sound/vibration-evoked escapes, which is consistent with the observation that increased occurrence of bilateral M-cell activation impaired escape performance. Our study revealed major components of the reciprocal inhibition circuits in the M cell system and the behavioral importance of the circuits. SIGNIFICANCE STATEMENT Reciprocal inhibition between the left and right side of the CNS is considered imperative for producing asymmetric movements in animals. It has been difficult, however, to identify the circuits at the individual cell level and their role in behavior. Here, we address this problem by examining the reciprocal inhibition circuits of the hindbrain Mauthner (M) cell system in larval zebrafish. We determined that two paired interneurons play a critical role in the reciprocal inhibition between the paired M cells and that the reciprocal inhibition prevents bilateral firing of the M cells and is thus necessary for the full body bend during M cell-initiated escape. Further, we discussed the cooperation of multiple reciprocal inhibitions working in the hindbrain and spinal cord to ensure high-performance escapes.