Neuronal ON/OFF Motion Detection Circuits Underlying Looming-Evoked Escape Behavior in Drosophila

Abstract

In Drosophila, early visual processing of motion information segregates in separate ON and OFF pathways. These pathways have been studied in the context of local directional motion detection leading to the encoding of optic flow that provides visual information for flight stabilization. Less is known about their role in detecting impending collision and generating escape behaviors. Looming, the simulated approach of an object at constant speed towards an animal, provides a powerful stimulus eliciting jump escape behaviors in stationary flies. We presented looming stimuli mimicking the approach of either a dark object on a bright background or a light object on a dark background, while inactivating neurons belonging either to the ON- or the OFF-motion detection pathways by expressing the dominant Drosophila temperature-sensitive mutant shibirets in different cells of the ON/OFF pathway. Inactivation of ON, respectively OFF, neurons led to selective decreases in escape behavior to light, resp. dark, looming stimuli. Quantitative analysis showed a nearly perfect splitting of these effects according to the ON/OFF type of the targeted neural populations. Our results suggest that Drosophila ON/OFF motion detection pathways play an important role in controlling jump escape responses according to looming stimulus polarity. They further imply that the biophysical circuits triggering Drosophila jump escape behaviors likely differ substantially from those characterized in other arthropods. SummaryInactivating fly neurons of the ON or OFF directional motion detection pathways during escape behavior selectively reduced jump responses to light and dark looming stimuli, respectively.