Visually Mediated Motor Planning in the Escape Response of Drosophila

Abstract

A key feature of reactive behaviors is the ability to spatially localize a salient stimulus and act accordingly. Such sensory-motor transformations must be particularly fast and well tuned in escape behaviors, in which both the speed and accuracy of the evasive response determine whether an animal successfully avoids predation [1]. We studied the escape behavior of the fruit fly, Drosophila, and found that flies can use visual information to plan a jump directly away from a looming threat. This is surprising, given the architecture of the pathway thought to mediate escape [2, 3]. Using high-speed videography, we found that approximately 200 ms before takeoff, flies begin a series of postural adjustments that determine the direction of their escape. These movements position their center of mass so that leg extension will push them away from the expanding visual stimulus. These preflight movements are not the result of a simple feed-forward motor program because their magnitude and direction depend on the flies' initial postural state. Furthermore, flies plan a takeoff direction even in instances when they choose not to jump. This sophisticated motor program is evidence for a form of rapid, visually mediated motor planning in a genetically accessible model organism.

Preparing for escape: anti-predator posture and fast-start performance in gobies

“…Hindlegs are flexed into a 'cocked' position, which may or may not be followed by an escape jump (Bennet-Clark, 1975;Heitler and Burrows, 1977;Santer et al, 2005). Escape 'preparation' has also been observed in Drosophila flies which, when stimulated, execute postural adjustments so that leg extension will push them away from the stimulus, whether escape will eventually be performed or not (Card and Dickinson, 2008). In these cases, escape preparation is, however, related to either mechanical constraints (locust) or directional advantage (Drosophila), rather than to enhancing locomotor performance as observed here.…”

“…The bending response consists of a slow and subtle movement of the tail and usually occurs within seconds of stimulation. It is therefore hypothesised that this bending response may represent an escape 'preparation' as observed in other animals, although based on very different mechanisms (Bennet-Clark, 1975;Card and Dickinson, 2008). Specifically, here we tested the following main hypotheses: (1) whether escape direction and performance in fish startled using lateral mechanical stimuli were affected by the alerting weak stimulation and the resulting changes in postural curvature, (2) whether escape performance in fish startled using a stimulus from above was affected by the alerting weak stimulation and (3) whether fish observed in the field showed any preference in the direction of escape relative to the postural C-bend.…”

Flying the Fly: Long-range Flight Behavior of Drosophila melanogaster to Attractive Odors

“…Two types of flight initiation are distinguished in the fruit fly, Drosophila melanogaster Meigen (Diptera: Drosophilidae) -a fast escape in response to threatening visual stimuli and a slow voluntary take-off based on the assessment of a stimulus, in reflection of the internal physiological state of the animal (Trimarchi and Schneiderman 1995;Allen et al 2006;Card and Dickinson 2008). Olfactory cues elicit premeditated flights.…”

Optogenetic control of selective neural activity in multiple freely moving Drosophila adults

“…Quantitative analysis of escape behaviors (SI Appendix, Fig. S9A) (31) indicated that these escape behaviors were observed frequently in trained males but rarely in naïve males or control males subjected to either pseudorandom laser irradiation or pseudorandom punishment (Fig. 4A).…”