Active Sensing in Bees Through Antennal Movements Is Independent of Odor Molecule

When sampling odors, many insects are moving their antennae in a complex but repeatable fashion. Previous studies with bees have tracked antennal movements in only two dimensions, with a low sampling rate and with relatively few odorants. A detailed characterization of the multimodal antennal movement patterns as function of olfactory stimuli is thus wanted. The aim of this study is to test for a relationship between the scanning movements and the properties of the odor molecule. We tracked several key locations on the antennae of bumblebees at high frequency and in three dimensions while stimulating the insect with puffs of 11 common odorants released in a low-speed continuous flow. Water and paraffin were used as negative controls. Movement analysis was done with the neural network Deeplabcut. Bees use a stereotypical oscillating motion of their antennae when smelling odors, similar across all bees, independently of the identity of the odors and hence their diffusivity and vapor pressure. The variability in the movement amplitude among odors is as large as between individuals. The main type of oscillation at low frequencies and large amplitude is triggered by the presence of an odor and is in line with previous work, as is the speed of movement. The second oscillation mode at higher frequencies and smaller amplitudes is constantly present. Antennae are quickly deployed when a stimulus is perceived, decorrelate their movement trajectories rapidly, and oscillate vertically with a large amplitude and laterally with a smaller one. The cone of airspace thus sampled was identified through the 3D understanding of the motion patterns. The amplitude and speed of antennal scanning movements seem to be function of the internal state of the animal, rather than determined by the odorant. Still, bees display an active olfactory sampling strategy. First, they deploy their antennae when perceiving an odor. Second, fast vertical scanning movements further increase the odorant capture rate. Finally, lateral movements might enhance the likelihood to locate the source of odor, similarly to the lateral scanning movement of insects at odor plume boundaries.