Department of Biology, University of Miami, Coral Gables, Florida 33143.
Neuroscience Program, University of Miami School of Medicine, Miami, Florida 33136.
J Neurosci. 2021 Apr 21;41(16):3635-3650. doi: 10.1523/JNEUROSCI.2150-20.2021. Epub 2021 Mar 9.
Successful execution of behavior requires coordinated activity and communication between multiple cell types. Studies using the relatively simple neural circuits of invertebrates have helped to uncover how conserved molecular and cellular signaling events shape animal behavior. To understand the mechanisms underlying neural circuit activity and behavior, we have been studying a simple circuit that drives egg-laying behavior in the nematode worm Here we show that the sex-specific, ventral C (VC) motor neurons are important for vulval muscle contractility and egg laying in response to serotonin. Ca imaging experiments show the VCs are active during times of vulval muscle contraction and vulval opening, and optogenetic stimulation of the VCs promotes vulval muscle Ca activity. Blocking VC neurotransmission inhibits egg laying in response to serotonin and increases the failure rate of egg-laying attempts, indicating that VC signaling facilitates full vulval muscle contraction and opening of the vulva for efficient egg laying. We also find the VCs are mechanically activated in response to vulval opening. Optogenetic stimulation of the vulval muscles is sufficient to drive VC Ca activity and requires muscle contractility, showing the presynaptic VCs and the postsynaptic vulval muscles can mutually excite each other. Together, our results demonstrate that the VC neurons facilitate efficient execution of egg-laying behavior by coordinating postsynaptic muscle contractility in response to serotonin and mechanosensory feedback. Many animal motor behaviors are modulated by the neurotransmitters, serotonin and ACh. Such motor circuits also respond to mechanosensory feedback, but how neurotransmitters and mechanoreceptors work together to coordinate behavior is not well understood. We address these questions using the egg-laying circuit in where we can manipulate presynaptic neuron and postsynaptic muscle activity in behaving animals while recording circuit responses through Ca imaging. We find that the cholinergic VC motoneurons are important for proper vulval muscle contractility and egg laying in response to serotonin. Muscle contraction also activates the VCs, forming a positive feedback loop that promotes full contraction for egg release. In all, mechanosensory feedback provides a parallel form of modulation that shapes circuit responses to neurotransmitters.
成功执行行为需要多个细胞类型的协调活动和通信。使用相对简单的无脊椎动物神经回路的研究有助于揭示保守的分子和细胞信号事件如何塑造动物行为。为了了解神经回路活动和行为的机制，我们一直在研究一个简单的回路，该回路驱动线虫中的产卵行为。在这里，我们表明，性特异的腹侧 C（VC）运动神经元对于对血清素作出反应的阴道肌肉收缩和产卵是重要的。Ca 成像实验表明，VC 在阴道肌肉收缩和阴道开口期间活跃，并且 VC 的光遗传学刺激促进阴道肌肉 Ca 活性。阻断 VC 神经传递会抑制对血清素的产卵，并增加产卵尝试的失败率，表明 VC 信号促进充分的阴道肌肉收缩和阴道开口，以有效地产卵。我们还发现 VC 对阴道开口有机械激活。阴道肌肉的光遗传学刺激足以驱动 VC Ca 活性，并且需要肌肉收缩性，表明突触前 VC 和突触后阴道肌肉可以相互兴奋。总之，我们的结果表明，VC 神经元通过协调对血清素的突触后肌肉收缩性和机械感觉反馈来促进有效的产卵行为执行。许多动物运动行为受到神经递质血清素和 ACh 的调节。这种运动回路也对机械感觉反馈作出反应，但是神经递质和机械感受器如何协同工作以协调行为尚不清楚。我们使用 中的产卵回路来解决这些问题，在该回路中，我们可以在行为动物中操纵突触前神经元和突触后肌肉活动，同时通过 Ca 成像记录回路响应。我们发现，胆碱能 VC 运动神经元对于对血清素作出反应的适当阴道肌肉收缩性和产卵是重要的。肌肉收缩也会激活 VC，形成一个正反馈回路，促进完全收缩以释放卵子。总的来说，机械感觉反馈提供了一种平行的调制形式，塑造了对神经递质的回路响应。
