One-to-one innervation of vocal muscles allows precise control of birdsong.

One-to-one innervation of vocal muscles allows precise control of birdsong.
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DOI:
10.1016/j.cub.2021.05.008
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发表时间:
2021-07-26
期刊:
Current biology : CB
影响因子:
--
通讯作者:
Elemans CPH
Elemans CPH
中科院分区:
其他
文献类型:
--
作者:
Adam I;Maxwell A;Rößler H;Hansen EB;Vellema M;Brewer J;Elemans CPH

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任何动物行为的运动控制分辨率都限于激活肌肉时可用的最小力阶,这是由运动单位(MU)的数量和大小分布以及肌肉比力设定的。鸟鸣是一个很好的模型系统,用于理解复杂精细运动技能的获得和维持,但令人惊讶的是,我们对控制鸣管的运动池是如何组织的以及MU招募如何驱动声音输出的变化知之甚少。在这里,我们开发了一个实验范例,以测量MU大小分布的细胞内钙离子浓度在活的完整的空洞肌肉的横截面的时空成像。我们结合这些测量与肌肉应力和体外鸣管制备,以确定控制分辨率的基本频率(fo),一个关键的声乐参数,在斑胸草雀。我们发现,舌骨肌的MU非常小,其中40 - 50%支配≤ 3,13 - 17%支配单个肌纤维。结合骨骼脊椎动物肌肉已知的最低比应力(5 mN/mm 2),主要控制肌肉的小力步长提供了每MU 50 mHz至7.3 Hz步长的控制。我们发现,歌曲系统具有最高的运动控制分辨率可能在脊椎动物的神经系统,并建议这是由于强大的选择上的声音输出的精细分级。此外,我们建议,高分辨率的电机控制是一个关键的功能,有助于辐射鸣禽,允许多样化的歌曲和物种的声乐空间扩展。亚当等人发现斑胸草雀的发声运动池有非常小的运动单位,其中13-17%的运动神经元支配单一的舌肌纤维。加上非常低的肌肉应力,这种高分辨率的运动控制允许对声音输出进行精细控制,包括亚赫兹音高控制,从而扩大声音空间。
The motor control resolution of any animal behavior is limited to the minimal force step available when activating muscles, which is set by the number and size distribution of motor units (MUs) and muscle specific force. Birdsong is an excellent model system for understanding acquisition and maintenance of complex fine motor skills, but we know surprisingly little how the motor pool controlling the syrinx is organized and how MU recruitment drives changes in vocal output. Here we developed an experimental paradigm to measure MU size distribution using spatiotemporal imaging of intracellular calcium concentration in cross-sections of living intact syrinx muscles. We combined these measurements with muscle stress and an in vitro syrinx preparation to determine the control resolution of fundamental frequency (fo), a key vocal parameter, in zebra finches. We show that syringeal muscles have extremely small MUs, with 40 – 50 % innervating ≤ 3, and 13 – 17% innervating a single muscle fiber. Combined with the lowest specific stress (5 mN/mm2) known to skeletal vertebrate muscle, small force steps by the major fo controlling muscle provide control of 50 mHz to 7.3 Hz steps per MU. We show that the song system has the highest motor control resolution possible in the vertebrate nervous system and suggest this evolved due to strong selection on fine gradation of vocal output. Furthermore, we propose that high-resolution motor control was a key feature contributing to the radiation of songbirds that allowed diversification of song and speciation by vocal space expansion. Adam et al. show that the zebra finch vocal motor pool has extremely small motor units, with 13–17% of motor neurons innervating single syringeal muscle fibers. Together with very low muscle stress, this high-resolution motor control allows for fine control of vocal output, including sub-Hz pitch control, leading to vocal space expansion.
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