Active anemosensing hypothesis: how flying insects could estimate ambient wind direction through sensory integration and active movement

Abstract

Estimating the direction of ambient fluid flow is a crucial step during chemical plume tracking for flying and swimming animals. How animals accomplish this remains an open area of investigation. Recent calcium imaging with tethered flying Drosophila has shown that flies encode the angular direction of multiple sensory modalities in their central complex: orientation, apparent wind (or airspeed) direction and direction of motion. Here, we describe a general framework for how these three sensory modalities can be integrated over time to provide a continuous estimate of ambient wind direction. After validating our framework using a flying drone, we use simulations to show that ambient wind direction can be most accurately estimated with trajectories characterized by frequent, large magnitude turns. Furthermore, sensory measurements and estimates of their derivatives must be integrated over a period of time that incorporates at least one of these turns. Finally, we discuss approaches that insects might use to simplify the required computations, and present a list of testable predictions. Together, our results suggest that ambient flow estimation may be an important driver underlying the zigzagging manoeuvres characteristic of plume tracking animals’ trajectories.

Wind Gates Olfaction Driven Search States in Free Flight

“…In both laminar wind and still air, immediately after odor onset, flies decelerate and often perform a rapid turn. Both maneuvers are consistent with predictions from recent control theoretic analyses for how insects may estimate properties of wind while in flight 7, 8 . We suggest that flies may use their deceleration and “anemometric” turn as active sensing maneuvers to rapidly gauge properties of their wind environment before initiating a proximal or upwind search routine.…”

“…Additionally, because angular velocity measurements twice propagate the derivatives of tracking noise from flies' x and y position, we found that angular velocity estimates on occasion experience brief highly variable segments along a trajectory. To account for this in our angular velocity analyses, we implemented a Butterworth Filter on the trajectory course direction before first order finite differentiation, all implemented in Python using the PyNumDiff package [Van Breugel et al, 2022].…”

“…Historically, wind orientation in insect flight has been attributed to visual anemotaxis 22,23 : a wind orienting strategy that primarily uses angular measurements of ventral optic flow and the apparent wind direction to guide an insect into the direction of ambient wind. The only stable solution to a control strategy that minimizes the difference between these two angles is to orient upwind 8 .…”

“…Historically, wind orientation in insect flight has been attributed to visual anemotaxis [Kennedy et al, 1940, Kennedy and Marsh, 1974]: a wind orienting strategy that uses angular measurements of ventral optic flow and the apparent wind direction to guide an insect into the direction of ambient wind. The only stable solution to a control strategy that minimizes the difference between these two angles is to orient upwind [van Breugel et al, 2022]. Visual anemotaxis, however, would not allow a fly to distinguish between flying upwind or flying in still air, nor would it explain how a fly can perform a directed saccade into the direction of ambient wind, or maintain a crosswind casting course.…”

Descending control and regulation of spontaneous flight turns inDrosophila

“…Brief bursts of saccades in the same direction may aid local search strategy by allowing the animal to quickly scan the local environment for salient visual and olfactory features (Heisenberg and Wolf, 1984). More recently, it has been suggested that comparing sensory measurements before and after each saccade might enable flies to estimate key parameters that are otherwise not directly measurable, such as the direction and magnitude of the ambient wind (van Breugel et al, 2022). For all these hypotheses, the timing between saccades is critical, and several factors are thought to influence the frequency of the spontaneous turns.…”