Mills Kevin M, Cowan Noah J, Suver Marie P
Department of Biological Sciences, Vanderbilt University, Nashville, TN.
Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD.
bioRxiv. 2025 Jun 24:2025.06.20.660728. doi: 10.1101/2025.06.20.660728.
To support robust behaviors in highly variable environments, animals rely on active sampling of their sensory surroundings. Here, we use tethered, flying and a multisensory behavioral apparatus simulating forward flight to determine how visual and mechanosensory information are integrated and control active movements of an important multimodal sensory organ, the antennae. We found that flies perform active antennal movements in response to varying airflow, and that the direction of these movements changes depending on the visual environment. Next, we found that antennal movements are amplified in the presence of visual motion, but only when the fly was flying. Through mechanical and optogenetic manipulation of mechanosensory input, we found that mechanosensory feedback is vital to antennal positioning at flight onset. Additionally, we observed unexpected changes in wingbeat frequency when the antenna was mechanically stabilized, suggesting that multiple antennal mechanosensors contribute to flight regulation. Finally, we show that integration of mechanosensory and visual cues for controlling antennal motion follows in a "winner-takes-all" paradigm dependent on the stimulus frequency, mirroring visuo-mechanosensory guided behaviors in other species. Together, these results reveal novel behavioral gating of sensory information and expand our understanding of the efferent control of active sensing.
为了在高度多变的环境中支持强健的行为,动物依赖于对其感官环境进行主动采样。在这里,我们使用系留飞行和一种模拟向前飞行的多感官行为装置,来确定视觉和机械感觉信息是如何整合的,以及如何控制一个重要的多模态感觉器官——触角的主动运动。我们发现,果蝇会根据变化的气流进行主动的触角运动,并且这些运动的方向会根据视觉环境而改变。接下来,我们发现,在有视觉运动的情况下,触角运动会被放大,但只有当果蝇飞行时才会如此。通过对机械感觉输入进行机械和光遗传学操作,我们发现机械感觉反馈对于飞行开始时触角的定位至关重要。此外,当触角被机械稳定时,我们观察到翅膀拍动频率出现了意想不到的变化,这表明多个触角机械传感器有助于飞行调节。最后,我们表明,用于控制触角运动的机械感觉和视觉线索的整合遵循一种取决于刺激频率的“赢家通吃”模式,这与其他物种中视觉-机械感觉引导的行为相似。总之,这些结果揭示了感觉信息的新型行为门控,并扩展了我们对主动感知的传出控制的理解。