Odour boosts visual object approach in flies.

Karen Y Cheng,Mark A Frye

doi:10.1098/rsbl.2020.0770

Abstract

Multisensory integration is synergistic—input from one sensory modality might modulate the behavioural response to another. Work in flies has shown that a small visual object presented in the periphery elicits innate aversive steering responses in flight, likely representing an approaching threat. Object aversion is switched to approach when paired with a plume of food odour. The ‘open-loop’ design of prior work facilitated the observation of changing valence. How does odour influence visual object responses when an animal has naturally active control over its visual experience? In this study, we use closed-loop feedback conditions, in which a fly's steering effort is coupled to the angular velocity of the visual stimulus, to confirm that flies steer toward or ‘fixate’ a long vertical stripe on the visual midline. They tend either to steer away from or ‘antifixate’ a small object or to disengage active visual control, which manifests as uncontrolled object ‘spinning’ within this experimental paradigm. Adding a plume of apple cider vinegar decreases the probability of both antifixation and spinning, while increasing the probability of frontal fixation for objects of any size, including a normally typically aversive small object.

Highlights

In flight, flies approach the vertically elongated edges of landscape features such as plant stalks, whereas they avoid threats posed by small moving objects [1,2,3]
Under so-called ‘open-loop’ experimental conditions, in which the wing kinematics of a tethered fly are recorded in response to imposed visual stimuli but the animal cannot control its visual experience, flies steer towards a tall object projected into the visual periphery and away from a small object in the same location for seconds [1,2,4], an artificially elongated time frame
The steering effort, proxied as the difference between left and right wingbeat amplitudes, ΔWBA [10], was negatively coupled to the angular velocity of the visual stimulus such that when the fly steered in one direction, the visual stimulus moved in the opposite direction to ‘virtually’

Summary

Introduction

Flies approach the vertically elongated edges of landscape features such as plant stalks, whereas they avoid threats posed by small moving objects [1,2,3]. This simple algorithm, based only on vertical object size, reduces the computational resources required for the brain to quickly make a crucial behavioural decision [1]. When provided with virtual ‘closed-loop’ feedback, in which the fly’s steering effort controls the visual stimulus [1,5], persistent approach towards a bar manifests as centring the object on the visual midline. Under closed-loop control, object aversion manifests either as spinning, in which a fly seems to forego active control and instead steers constantly in one direction, or as antifixation, in which a fly actively avoids the stimulus, keeping it centred in the rear field of view [1]

Methods

Results

Conclusion