Octopamine and tyramine dynamics predict learning rate phenotypes during associative conditioning in honey bees

Abstract

Biogenic amines are fundamental for physiological homeostasis and behavioral control in both vertebrates and invertebrates. Monoamine neurotransmitters released in target brain regions conjointly regulate adaptive learning and plasticity. However, our understanding of these multi-analyte mechanisms remains nascent, in part due to limitations in measurement technology. Here, during associative conditioning in honey bees, we concurrently tracked sub-second fluctuations in octopamine, tyramine, dopamine, and serotonin in the antennal lobe, where plasticity influences odorant representations. By repeatedly pairing an odorant with subsequent sucrose delivery, we observed individual differences in the conditioned response to odor, which occurred after a variable number of pairings (learners) or not at all (nonlearners). The distinction between learners and non-learners was reflected in neurotransmitter responses across experimental conditions. Remarkably, the speed of learning - the number of pairings prior to a proboscis extension reflex - could be predicted from monoamine opponent signaling (octopamine-tyramine), from both the first presentation of the odorant alone, prior to any pairing with sucrose, and from the first conditioned response to the odorant, coming after a number of sucrose pairings. These results suggest monoamine signaling phenotypes may relate directly to the now widely-reported socially-relevant genetic differences in honey bee learning.