School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138.
Proc Natl Acad Sci U S A. 2014 Apr 1;111(13):E1182-91. doi: 10.1073/pnas.1323529111. Epub 2014 Mar 17.
Flies and other insects use vision to regulate their groundspeed in flight, enabling them to fly in varying wind conditions. Compared with mechanosensory modalities, however, vision requires a long processing delay (100 ms) that might introduce instability if operated at high gain. Flies also sense air motion with their antennae, but how this is used in flight control is unknown. We manipulated the antennal function of fruit flies by ablating their aristae, forcing them to rely on vision alone to regulate groundspeed. Arista-ablated flies in flight exhibited significantly greater groundspeed variability than intact flies. We then subjected them to a series of controlled impulsive wind gusts delivered by an air piston and experimentally manipulated antennae and visual feedback. The results show that an antenna-mediated response alters wing motion to cause flies to accelerate in the same direction as the gust. This response opposes flying into a headwind, but flies regularly fly upwind. To resolve this discrepancy, we obtained a dynamic model of the fly's velocity regulator by fitting parameters of candidate models to our experimental data. The model suggests that the groundspeed variability of arista-ablated flies is the result of unstable feedback oscillations caused by the delay and high gain of visual feedback. The antenna response drives active damping with a shorter delay (20 ms) to stabilize this regulator, in exchange for increasing the effect of rapid wind disturbances. This provides insight into flies' multimodal sensory feedback architecture and constitutes a previously unknown role for the antennae.
苍蝇和其他昆虫利用视觉来调节飞行中的地速，使它们能够在不同的风况下飞行。然而，与机械感觉模态相比，视觉需要较长的处理延迟（100ms），如果以高增益操作，可能会导致不稳定。苍蝇也用它们的触角感知空气运动，但这种感觉在飞行控制中是如何被利用的还不清楚。我们通过切除果蝇的触角来操纵它们的触角功能，迫使它们仅依靠视觉来调节地速。飞行中的触角切除苍蝇的地速变化明显大于完整苍蝇。然后，我们用空气活塞向它们施加一系列受控的脉冲风，并对触角和视觉反馈进行了实验性操作。结果表明，触角介导的反应改变了翅膀的运动，使苍蝇朝着阵风的方向加速。这种反应与逆风飞行相违背，但苍蝇经常逆风飞行。为了解决这个差异，我们通过将候选模型的参数拟合到我们的实验数据中，获得了苍蝇速度调节器的动态模型。该模型表明，触角切除苍蝇的地速变化是由于视觉反馈的延迟和高增益导致的不稳定反馈振荡造成的。触角反应通过较短的延迟（20ms）驱动主动阻尼，以稳定这个调节器，同时增加对快速风干扰的影响。这为苍蝇的多模态感觉反馈结构提供了深入的了解，并构成了触角以前未知的作用。
