Mechanisms Underlying the Recruitment of Inhibitory Interneurons in Fictive Swimming in Developing Xenopus laevis Tadpoles.
Mechanisms Underlying the Recruitment of Inhibitory Interneurons in Fictive Swimming in Developing Xenopus laevis Tadpoles.
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DOI：
10.1523/jneurosci.0520-22.2022
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发表时间：
2023-02-22
影响因子：
5.3
通讯作者：
Li, Wen-Chang
中科院分区：
文献类型：
--
作者：
Ferrario, Andrea;Saccomanno, Valentina;Zhang, Hong-Yan;Borisyuk, Roman;Li, Wen-Chang
发育中的脊髓回路产生有模式的运动输出，而许多具有高膜电阻的神经元仍在成熟。在性别不明的幼蛙蝌蚪的脊髓中，我们发现带有连合和同侧上升轴突的抑制性中间神经元在游泳时的放电可靠性与其细胞膜阻力呈负相关。进一步的分析表明，具有较高电阻的神经元具有外向整流特性，放电阈值较低，并且电流注入引起的放电延迟很小。这些神经元在游泳过程中收到的输入突触电流，无论是复合的、单一的电流幅度，还是单一的突触电流数量，都是根据它们的膜电阻来衡量的，但它们自己的突触输出与它们的突触后伙伴的膜电阻相关。对神经元、树突和轴突的长度及其在游泳和细胞输入阻力中的活动的分析并未显示出明确的相关模式。将这些电学和突触特性结合到计算机游泳模型中可以产生强健的游泳节奏，而随机输入的突触强度会导致游泳节奏的崩溃，加上抑制性中间神经元中不那么同步的尖峰放电。我们的结论是，这些发育中的中间神经元在游泳中的招募可以通过细胞输入阻力来预测，但顺序与Henneman的大小原理所描述的基于运动强度的招募方案相反。在精细运动控制出现之前，这种招募/整合顺序的发展是渐进的，可能随着神经元获得成熟的电和突触属性，其中输入突触强度与细胞输入阻力的调节起着关键作用。意义陈述关于中间神经元如何被招募来参与神经系统发育中的回路功能的机制很少被研究。在2-d龄的青蛙蝌蚪脊髓中，我们发现游泳中抑制性中间神经元的招募与细胞输入阻力呈负相关，与Henneman的大小原理所描述的基于运动强度的招募顺序相反。进一步的分析表明，神经元在游泳过程中接收到的突触输入的幅度与细胞输入阻力呈负相关。随机化/颠倒模型中输入突触强度和膜阻力之间的关系打破了游泳节奏。因此，这些中间神经元的招募或整合取决于几个电和突触特性的获得，包括输入突触强度随细胞输入阻力的变化。
Developing spinal circuits generate patterned motor outputs while many neurons with high membrane resistances are still maturing. In the spinal cord of hatchling frog tadpoles of unknown sex, we found that the firing reliability in swimming of inhibitory interneurons with commissural and ipsilateral ascending axons was negatively correlated with their cellular membrane resistance. Further analyses showed that neurons with higher resistances had outward rectifying properties, low firing thresholds, and little delay in firing evoked by current injections. Input synaptic currents these neurons received during swimming, either compound, unitary current amplitudes, or unitary synaptic current numbers, were scaled with their membrane resistances, but their own synaptic outputs were correlated with membrane resistances of their postsynaptic partners. Analyses of neuronal dendritic and axonal lengths and their activities in swimming and cellular input resistances did not reveal a clear correlation pattern. Incorporating these electrical and synaptic properties into a computer swimming model produced robust swimming rhythms, whereas randomizing input synaptic strengths led to the breakdown of swimming rhythms, coupled with less synchronized spiking in the inhibitory interneurons. We conclude that the recruitment of these developing interneurons in swimming can be predicted by cellular input resistances, but the order is opposite to the motor-strength-based recruitment scheme depicted by Henneman’s size principle. This form of recruitment/integration order in development before the emergence of refined motor control is progressive potentially with neuronal acquisition of mature electrical and synaptic properties, among which the scaling of input synaptic strengths with cellular input resistance plays a critical role. SIGNIFICANCE STATEMENT The mechanisms on how interneurons are recruited to participate in circuit function in developing neuronal systems are rarely investigated. In 2-d-old frog tadpole spinal cord, we found the recruitment of inhibitory interneurons in swimming is inversely correlated with cellular input resistances, opposite to the motor-strength-based recruitment order depicted by Henneman’s size principle. Further analyses showed the amplitude of synaptic inputs that neurons received during swimming was inversely correlated with cellular input resistances. Randomizing/reversing the relation between input synaptic strengths and membrane resistances in modeling broke down swimming rhythms. Therefore, the recruitment or integration of these interneurons is conditional on the acquisition of several electrical and synaptic properties including the scaling of input synaptic strengths with cellular input resistances.
影响因子：
4.3
作者：
Hull MJ;Soffe SR;Willshaw DJ;Roberts A
通讯作者：
Roberts A
影响因子：
3.7
作者：
Borisyuk R;Al Azad AK;Conte D;Roberts A;Soffe SR
通讯作者：
Soffe SR