A Descending Neuron Correlated with the Rapid Steering Maneuvers of Flying Drosophila

Abstract

Summary To navigate through the world, animals must stabilize their path against disturbances and change direction to avoid obstacles and to search for resources [1,2]. Locomotion is thus guided by sensory cues, but also depends on intrinsic processes, such as motivation and physiological state. Flies, for example, turn with the direction of large-field rotatory motion, an optomotor reflex that is thought to help them fly straight [3-5]. Occasionally, however, they execute fast turns, called body saccades, either spontaneously or in response to patterns of visual motion such as expansion [6-8]. These turns can be measured in tethered flying Drosophila [3,4,9], which facilitates the study of underlying neural mechanisms. Whereas there is evidence for an efference copy input to visual interneurons during saccades [10], the circuits that control spontaneous and visually elicited saccades are not well known. Using 2-photon calcium imaging and electrophysiological recordings in tethered flying Drosophila, we have identified a descending neuron whose activity is correlated with both spontaneous and visually elicited turns during tethered flight. The cell's activity in open- and closed-loop experiments suggests that it does not underlie slower compensatory responses to horizontal motion, but rather controls rapid changes in flight path. The activity of this neuron can explain some of the behavioral variability observed in response to visual motion and appears sufficient for eliciting turns when artificially activated. This work provides an entry point into studying the circuits underlying the control of rapid steering maneuvers in the fly brain.

Multisensory Control of Orientation in Tethered Flying Drosophila

“…Across stimulus intensities and spatial configurations, we found that turn dynamics reflected both mechanosensory and visual input; antennal stabilization experiments argue that these signals are integrated within the brain. Although integration of both modalities was visible in nearly every stimulus configuration we tested, unexpected turns also occurred in many of our experiments, suggesting that the integrative process on which we have focused must coexist with mechanisms to generate stochastic turns [7,29,30]. …”

Drosophila Spatiotemporally Integrates Visual Signals to Control Saccades

“…One recent study has identified descending neurons whose activity correlates with spontaneous saccades [19]. At present it is unknown what neural center could provide the trigger for bar-fixation saccades.…”

“…Once a saccade is triggered, visual motion appears to play no role in modulating its dynamics [17, 18], suggesting that they are ballistic, all-or-none events. In tethered flight, flies generate saccades in the absence of any visual motion, suggesting that endogenous processes may also evoke saccades [10, 19]. …”

Abolishment of Spontaneous Flight Turns in Visually Responsive Drosophila

“…NP0212 > Shi ts flies at 34°C continued to make some sharp turns during optomotor stimuli (see NP0212 > Shi ts example trace in Figure 4C). Such turns, whose rate seems to be increased by optomotor stimuli and which have been noted previously [3, 29, 45], represent a potentially different class of flight maneuver from those blocked in NP0212 > Shi ts flies.…”