Higher-order discrimination learning by honey bees in a virtual environment

Abstract

Non-elemental learning constitutes a cognitive challenge because, contrary to elemental learning forms, it does not rely on simple associations, as events to be learned are usually ambiguous in terms of reinforcement outcome. Negative patterning constitutes a paradigmatic case of non-elemental learning, as subjects have to learn that single elements A and B are reinforced while their conjunctive representation AB is not reinforced (A+, B+ vs. AB-). Solving this problem requires treating the compound AB as being different from the linear sum of its components in order to overcome stimulus ambiguity (A+/A- and B+/B-). The honey bee is the only insect capable of mastering negative patterning as shown by numerous studies restricted mainly to the olfactory domain. Here we studied the capacity of bees to solve a negative patterning discrimination in the visual domain and used to this end a virtual reality (VR) environment in which a tethered bee walking stationary on a treadmill faces visual stimuli projected on a semicircular screen. Stimuli are updated by the bees movements, thus creating an immersive environment. Bees were trained to discriminate single-colored gratings rewarded with sucrose solution (blue, green; A+, B+) from a non-rewarded composite grating (blue-green, AB-). Bees learned this discrimination in the VR environment and inhibited to this end linear processing of the composite grating, which otherwise is treated as the sum of its components. Our results show for the first time mastering of a non-linear visual discrimination in a VR environment by honey bees, thus highlighting the value of VR for the study of cognition in insects.