Neuromuscular basis of Drosophila larval rolling escape behavior.
Neuromuscular basis of Drosophila larval rolling escape behavior.
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果蝇幼虫滚动逃生行为的神经肌肉基础。
DOI：
10.1073/pnas.2303641120
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发表时间：
2023-12-19
影响因子：
11.1
通讯作者：
Zarin, Aref A.
中科院分区：
文献类型：
--
作者：
Cooney, Patricia C.;Huang, Yuhan;Li, Wenze;Perera, Dulanjana M.;Hormigo, Richard;Tabachnik, Tanya;Godage, Isuru S.;Hillman, Elizabeth M. C.;Grueber, Wesley B.;Zarin, Aref A.
关键词：
为了逃避危险的刺激，动物会执行与正常运动完全不同的逃避行为。果蝇幼虫的滚逃行为包括c型弯曲和滚逃。然而，导致滚动的肌肉收缩模式却知之甚少。我们发现，在最初的身体弯曲之后，肌肉在幼虫进入弯曲处时以圆周波的形式收缩，保持单向滚动，类似于在表面上滚动的圆柱体。我们研究了滚动运动回路的结构，抑制不同的运动神经元来确定哪些肌肉是滚动所必需的，并提出了滚动产生的电路和生物力学模型。我们的发现为运动回路如何产生不同的运动行为提供了见解。当受到危险或有害刺激的威胁时，动物会采取各种形式的快速逃离行为。在果蝇幼虫中，一种逃脱反应包括c形弯曲和横向滚动，然后是快速向前爬行。促进幼虫逃脱的感觉回路已被广泛描述；然而，运动程序背后的滚动是未知的。在这里，我们描述了滚动逃跑行为的神经肌肉基础。我们使用高速、体积、扫描共聚焦平面激发（SCAPE）显微镜来成像幼虫滚动过程中的肌肉活动。与向前和向后爬行时从一个节段到另一个节段的连续蠕动肌肉收缩不同，在弯曲和滚动逃跑行为中肌肉活动呈周向进展。我们认为，幼虫周围肌肉收缩的进展导致体重和地面支撑力之间的短暂错位，这产生了一个扭矩，诱导稳定的身体旋转。因此，连续的周期轻微的不对准，然后是被动的对准旋转导致连续滚动运动。支持我们的生物力学模型，我们发现，破坏肌肉群的活动，进行圆周收缩进展导致滚动缺陷。我们使用EM连接组数据来识别可以驱动滚动行为的前运动到运动连接模式，并执行神经沉默方法来证明一组谷氨酸能前运动神经元在滚动中的关键作用。我们的数据揭示了全身肌肉活动模式和执行滚动逃逸反应的假定的运动前电路组织。
To escape from dangerous stimuli, animals execute escape behaviors that are fundamentally different from normal locomotion. The rolling escape behavior of Drosophila larvae consists of C-shaped bending and rolling. However, the muscle contraction patterns that lead to rolling are poorly understood. We find that following the initial body bending, muscles contract in a circumferential wave around the larva as they enter the bend, maintaining unidirectional rolling that resembles a cylinder rolling on a surface. We study the structure of motor circuits for rolling, inhibit different motor neurons to determine which muscles are essential for rolling, and propose circuit and biomechanical models for roll generation. Our findings provide insights into how motor circuits produce diverse motor behaviors. When threatened by dangerous or harmful stimuli, animals engage in diverse forms of rapid escape behaviors. In Drosophila larvae, one type of escape response involves C-shaped bending and lateral rolling followed by rapid forward crawling. The sensory circuitry that promotes larval escape has been extensively characterized; however, the motor programs underlying rolling are unknown. Here, we characterize the neuromuscular basis of rolling escape behavior. We used high-speed, volumetric, Swept Confocally Aligned Planar Excitation (SCAPE) microscopy to image muscle activity during larval rolling. Unlike sequential peristaltic muscle contractions that progress from segment to segment during forward and backward crawling, muscle activity progresses circumferentially during bending and rolling escape behavior. We propose that progression of muscular contraction around the larva’s circumference results in a transient misalignment between weight and the ground support forces, which generates a torque that induces stabilizing body rotation. Therefore, successive cycles of slight misalignment followed by reactive aligning rotation lead to continuous rolling motion. Supporting our biomechanical model, we found that disrupting the activity of muscle groups undergoing circumferential contraction progression leads to rolling defects. We use EM connectome data to identify premotor to motor connectivity patterns that could drive rolling behavior and perform neural silencing approaches to demonstrate the crucial role of a group of glutamatergic premotor neurons in rolling. Our data reveal body-wide muscle activity patterns and putative premotor circuit organization for execution of the rolling escape response.
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影响因子：
9.8
作者：
Donnelly JL;Clark CM;Leifer AM;Pirri JK;Haburcak M;Francis MM;Samuel AD;Alkema MJ
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影响因子：
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影响因子：
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作者：
Fotowat, Haleh;Harrison, Reid R.;Gabbiani, Fabrizio
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