Current Biology
Volume 31, Issue 18, 27 September 2021, Pages 4009-4024.e3
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Article
Mechanisms of punctuated vision in fly flight

https://doi.org/10.1016/j.cub.2021.06.080Get rights and content
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Highlights

  • Flies (Drosophila) perform stereotyped head saccades to reset gaze

  • Head-reset saccades leverage the neck’s elasticity to rapidly accelerate

  • Head movements are gated by behavioral state and influence wing-reset saccades

  • Neck proprioceptive feedback is the primary trigger of head-reset saccades

Summary

To guide locomotion, animals control gaze via movements of their eyes, head, and/or body, but how the nervous system controls gaze during complex motor tasks remains elusive. In many animals, shifts in gaze consist of periods of smooth movement punctuated by rapid eye saccades. Notably, eye movements are constrained by anatomical limits, which requires resetting eye position. By studying tethered, flying fruit flies (Drosophila), we show that flies perform stereotyped head saccades to reset gaze, analogous to optokinetic nystagmus in primates. Head-reset saccades interrupted head smooth movement for as little as 50 ms—representing less than 5% of the total flight time—thereby enabling punctuated gaze stabilization. By revealing the passive mechanics of the neck joint, we show that head-reset saccades leverage the neck’s natural elastic recoil, enabling mechanically assisted redirection of gaze. The consistent head orientation at saccade initiation, the influence of the head’s angular position on saccade rate, the decrease in wing saccade frequency in head-fixed flies, and the decrease in head-reset saccade rate in flies with their head range of motion restricted together implicate proprioception as the primary trigger of head-reset saccades. Wing-reset saccades were influenced by head orientation, establishing a causal link between neck sensory signals and the execution of body saccades. Head-reset saccades were abolished when flies switched to a landing state, demonstrating that head movements are gated by behavioral state. We propose a control architecture for active vision systems with limits in sensor range of motion.

Keywords

active vision
Drosophila
saccade
gaze stabilization
flight control
optokinetic nystagmus
neck mechanics
eye movement

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