On the adaptive behavior of head-fixed flies navigating in two-dimensional, visual virtual reality

Abstract

A navigating animal’s sensory experience is shaped not just by its surroundings, but by its movements within them, which in turn are influenced by its past experiences. Studying the intertwined roles of sensation, experience and directed action in navigation has been made easier by the development of virtual reality (VR) environments for head-fixed animals, which allow for quantitative measurements of behavior in well-controlled sensory conditions. VR has long featured in studies of Drosophila melanogaster, but these experiments have typically relied on one-dimensional (1D) VR, effectively allowing the fly to change only its heading in a visual scene, and not its position. Here we explore how flies navigate in a two-dimensional (2D) visual VR environment that more closely resembles their experience during free behavior. We show that flies’ interaction with landmarks in 2D environments cannot be automatically derived from their behavior in simpler 1D environments. Using a novel paradigm, we then demonstrate that flies in 2D VR adapt their behavior in a visual environment in response to optogenetically delivered appetitive and aversive stimuli. Much like free-walking flies after encounters with food, head-fixed flies respond to optogenetic activation of sugar-sensing neurons by initiating a local search behavior. Finally, by pairing optogenetic activation of heat-sensing cells to the flies’ presence near visual landmarks of specific shapes, we elicit selective learned avoidance of landmarks associated with aversive “virtual heat”. These head-fixed paradigms set the stage for an interrogation of fly brain circuitry underlying flexible navigation in complex visual environments.

Virtual reality for animal navigation with camera-based optical flow tracking

“…For testing the setup for fly behavior, we used a simple VR with a single bright stripe of 10 degree width and 45 degree height projected onto a two-part screen similar to [7] of 9 mm height and 2 times 18 mm width made out of black paper. The fly’s head was fixed to its thorax with UV glue, and the wings were glued to the tethering pin using UV glue to encourage walking behavior [17].…”

“…A schematic of the setup is shown in Figure 1. Two digital micromirror devices (DMD, DLP LightCrafter 6500 by Texas Instruments) were used for projecting the VR onto an angled screen from two sides [8, 7]. The projectors are FullHD digital micromirror devices with HDMI and DisplayPort interfaces allowing them to display images the same way as standard monitors.…”

“…Here, we combine the flexibility of optical flow-based tracking with the advantages of using a high-resolution camera. The developed system tracks optical flow of rotational ball movement at 500 Hz using a single camera and is integrated with an open source virtual reality environment and two projectors [7] with a refresh rate of 120 Hz [8] and overall latency of 30 ± 8 ms – from detecting ball movement to projecting the updated virtual reality image. This is achieved using off-the-shelf hardware components and open source software.…”