National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India.
Elife. 2022 Jun 27;11:e78410. doi: 10.7554/eLife.78410.
During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated via visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, albeit at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization primarily at low frequencies of body roll. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements at high frequencies of body roll.
在飞行机动过程中，昆虫会做出代偿性头部运动，这对于稳定视网膜上的视野、减少运动模糊和支持视觉自运动估计至关重要。在双翅目昆虫中，这种头部运动是通过它们的复眼提供的视觉反馈来介导的，复眼可以检测到视网膜滑移，以及它们的平衡棒——感知身体旋转角速度的改装后翅——提供的快速机械感觉反馈。由于非双翅目昆虫没有平衡棒，所以尚不清楚关于身体旋转的机械感觉反馈是否在它们的头部稳定反应中发挥作用。不同的非双翅目昆虫已知依赖视觉和触角机械感觉反馈来进行飞行控制。例如，在鹰蛾中，减少触角机械感觉反馈会严重影响它们控制飞行的能力。同样，当自由飞行的蛾的头部运动受到限制时，它们的飞行能力也会受到严重损害。昆虫飞行中的代偿性头部运动和多模态反馈的作用提出了一个有趣的问题：在缺乏平衡棒的昆虫中，头部稳定需要哪些感觉线索？在这里，我们表明在夜间的鹰蛾中，代偿性头部运动是由视觉和触角机械感觉反馈的结合介导的。我们让被束缚的蛾在不同的照明条件下进行开环体滚旋转，并测量它们在有或没有触角机械感觉反馈的情况下保持头部角度的能力。我们的研究表明，在较低频率的滚动运动中，头部稳定主要是由视觉反馈介导的，而在较高频率的滚动中则需要触角机械感觉反馈。这些发现与以下假设一致，即头部角度的控制是由一个整合视觉和触角机械感觉反馈的多模态反馈回路介导的，尽管存在不同的延迟。在足够的光照水平下，视觉反馈足以在体滚的低频下主要用于头部稳定。然而，在黑暗条件下，触角机械感觉反馈对于控制体滚高频下的头部运动至关重要。
