Active sensing movements by antennae enhance neural processing and plasticity for odour processing in the CNS in the honey bee Apis mellifera

Abstract

Animals frequently move their sensory organs relative to dynamic environmental stimuli to maximize information acquisition, a behaviour known as active sensing. Recent studies show that insects adjust antennal movements according to the temporal structure and salience of olfactory signals, suggesting that antennae participate in active sensing. However, how these movements affect central olfactory processing remains unclear. To address this question, we trained honey bee foragers using a proboscis extension response (PER) protocol in which one odour (CS+) was paired with sucrose and another (CS-) with salt water. This training produces distinct antennal movements toward the two odours. Bees were subsequently tested with a series of concentrations of both CS+ and CS- odours. Antennae were either fixed or allowed to move freely during training and testing, while ectrophysiological recordings were made from the antennae and from the antennal lobes. Peripheral antennal responses across odour concentrations were not affected by whether the antennae were fixed or free. In contrast, antennal lobe projection neurons and local interneurons showed learning-related increases in responses to the CS+ odour, consistent with previous studies, and these increases were stronger in bees with freely moving antennae. Neural responses were also more variable, particularly at lower odour concentrations, when antennae could move, suggesting that response variability may contribute to plasticity. These results support the hypothesis that active antennal movements influence central processing of odour representations. Future studies comparing restrained bees with freely walking bees will help clarify the natural behavioural contexts in which antennal movements enhance olfactory sensing.