Abstract
Honey bees exhibit remarkable visual learning capacities, which can be studied using virtual reality (VR) landscapes in laboratory conditions. Existing VR environments for bees are imperfect as they provide either open-loop conditions or 2D displays. Here we achieved a true 3D environment in which walking bees learned to discriminate a rewarded from a punished virtual stimulus based on color differences. We included ventral or frontal background cues, which were also subjected to 3D updating based on the bee movements. We thus studied if and how the presence of such motion cues affected visual discrimination in our VR landscape. Our results showed that the presence of frontal, and to a lesser extent, of ventral background motion cues impaired the bees’ performance. Whenever these cues were suppressed, color discrimination learning became possible. We analyzed the specific contribution of foreground and background cues and discussed the role of attentional interference and differences in stimulus salience in the VR environment to account for these results. Overall, we show how background and target cues may interact at the perceptual level and influence associative learning in bees. In addition, we identify issues that may affect decision-making in VR landscapes, which require specific control by experimenters.
Highlights
Honey bees exhibit remarkable visual learning capacities, which can be studied using virtual reality (VR) landscapes in laboratory conditions
The model that best fitted the data included an interaction between the red intensity and the bees’ choice (Choice*Intensity: χ2 = 65.48, df: 4, p < 0.001)
We pooled the data of the four tests and represented for each intensity the percentage of bees within each category (Red, No Stimulus and No choice category (Choice); Fig. 3)
Summary
Honey bees exhibit remarkable visual learning capacities, which can be studied using virtual reality (VR) landscapes in laboratory conditions. A predecessor of current VR systems is the flight simulator conceived for the fruit fly Drosophila melanogaster In this setup, which was first used to study how optical properties of compound eyes influence optomotor reactions[3], a tethered fly flies stationary in the middle of a cylindrical arena and experiences surrounding visual stimuli that can be updated by the fly’s movements. VR setups in which a tethered animal makes decision based on visual cues represent a suitable solution to overcome these limitations as they provide access both to behavioral output and to the nervous system of a behaving bee with restricted m obility[27,28] This perspective is supported by recent developments allowing to record from specific neurons in the brain of walking bees[16,27,29,30,31]. The development of VR environments requires considerable work in order to adapt visual displays to the subjective perception of an insect and determine optimal parameters for immersive sensations from an insect’s perspective
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