Transfer of Visual Learning Between a Virtual and a Real Environment in Honey Bees: The Role of Active Vision

Alexis Buatois, Clara Flumian, Patrick Schultheiss, Aurore Avarguès-Weber, Martin Giurfa

To study visual learning in honey bees, we developed a virtual reality (VR) system in which the movements of a tethered bee walking stationary on a spherical treadmill update the visual panorama presented in front of it (closed-loop conditions), thus creating an experience of immersion within a virtual environment. In parallel, we developed a small Y-maze with interchangeable end-boxes, which allowed replacing repeatedly a freely walking bee into the starting point of the maze for repeated decision recording. Using conditioning and transfer experiments between the VR setup and the Y-maze, we studied the extent to which movement freedom and active vision are crucial for learning a simple color discrimination. Approximately 57% of the bees learned the visual discrimination in both conditions. Transfer from VR to the maze improved significantly the bees' performances: 75% of bees having chosen the CS+ continued doing so and 100% of bees having chosen the CS- reverted their choice in favor of the CS+. In contrast, no improvement was seen for these two groups of bees during the reciprocal transfer from the Y-maze to VR. In this case, bees exhibited inconsistent choices in the VR setup. The asymmetric transfer between contexts indicates that the information learned in each environment may be different despite the similar learning success. Moreover, it shows that reducing the possibility of active vision and movement freedom in the passage from the maze to the VR impairs the expression of visual learning while increasing them in the reciprocal transfer improves it. Our results underline the active nature of visual processing in bees and allow discussing the developments required for immersive VR experiences in insects.