Motor cortex analogue neurons in songbirds utilize Kv3 subunits to generate ultranarrow spikes

Complex motor skills in vertebrates require specialized upper motor neurons with precise action potential (AP) firing. To examine how diverse populations of upper motor neurons subserve distinct functions and the specific repertoire of ion channels involved, we conducted a thorough study of the excitability of upper motor neurons controlling somatic motor function in the zebra finch. We found that robustus arcopallialis projection neurons (RAPNs), key command neurons for song production, exhibit ultranarrow spikes and higher firing rates compared to neurons controlling non-vocal somatic motor functions (AId neurons). Pharmacological and molecular data indicate that this striking difference is associated with the higher expression in RAPNs of high threshold, fast-activating voltage-gated Kv3 channels likely containing Kv3.1 subunits. The spike waveform and Kv3.1 expression in RAPNs mirror properties of Betz cells, specialized upper motor neurons involved in fine digit control in humans and other primates but absent in rodents. Our study thus provides evidence that songbirds and primates have convergently evolved the use of Kv3.1 to ensure precise, rapid AP firing in upper motor neurons controlling fast and complex motor skills.

脊椎动物的复杂运动技能需要具备精准动作电位（action potential, AP）发放能力的特化上级运动神经元。为探究不同类群的上级运动神经元如何介导特异性功能，以及其所涉及的离子通道特异性组成，我们针对斑胸草雀中调控躯体运动功能的上级运动神经元的兴奋性开展了全面研究。我们发现，作为鸣曲产生关键命令神经元的弓状核投射神经元（robustus arcopallialis projection neurons, RAPNs），相较于调控非发声躯体运动功能的AId神经元，具有超窄锋电位与更高的放电频率。药理学与分子生物学数据表明，这种显著差异与RAPNs中高阈值、快速激活的电压门控Kv3通道（大概率含有Kv3.1亚基）的高表达密切相关。RAPNs的锋电位波形与Kv3.1表达特征，与人类及其他灵长类动物中负责精细手指操控的特化上级运动神经元——贝茨细胞（Betz cells）的特性高度吻合，而这类神经元在啮齿类动物中并不存在。综上，本研究提供证据表明，鸣禽与灵长类动物通过趋同演化，均利用Kv3.1通道保障调控快速复杂运动技能的上级运动神经元实现精准、快速的动作电位发放。