A simple behaviour provides accuracy and flexibility in odour plume tracking—the robotic control of sensory-motor coupling in silkmoths

Abstract

Odour plume tracking is an essential behaviour for animal survival. A fundamental strategy for this is moving upstream and then across-stream. Male silkmoths, Bombyx mori, display this strategy as a pre-programmed sequential behaviour. They walk forward (surge) in response to the female sex pheromone and perform a zigzagging “mating dance”. Though pre-programmed, the surge direction is modulated by the bilateral olfactory input and optic flow. However, the nature of interaction between these two sensory modalities and contribution of the resultant motor command to localizing an odour source are still unknown. We evaluated the ability of the silkmoth to localize the odour source under conditions of disturbed sensory-motor coupling, using a silkmoth-driven mobile robot. The significance of the bilateral olfaction of the moth was confirmed by inverting the robot's olfactory input that is acquired using two flexible air-suction tubes and delivered to the antennae of the moth, or its motor output. Inversion of the motor output induced consecutive circling, which was inhibited by covering the visual field of the moth. This suggests that the corollary discharge from the motor command and the reafference of self-generated optic flow generates compensatory signals to guide the surge accurately. Additionally, after inverting the olfactory input, the robot successfully tracked the odour plume by using a combination of behaviours. These results indicate that accurate guidance of the reflexive surge by integrating bilateral olfactory and visual information with innate pre-programmed behaviours increases the flexibility to track an odour plume even under disturbed circumstances.