Tyramine and its AmTYR1 receptor modulate attention in honey bees (Apis mellifera)

Abstract

Animals must learn to ignore stimuli that are irrelevant to survival and attend to ones that enhance survival. When a stimulus regularly fails to be associated with an important consequence, subsequent excitatory learning about that stimulus can be delayed, which is a form of non-associative conditioning called latent inhibi-tion. Honey bees show latent inhibition toward an odor they have experienced without association with food reinforcement. Moreover, individual honey bees from the same colony differ in the degree to which they show latent inhibition, and these individual differences have a genetic basis. To investigate the mechanisms that underly individual differences in latent inhibition, we selected two honey bee lines for high and low latent inhibition, respectively. We crossed those lines and mapped a Quantitative Trait Locus (QTL) for latent inhibition to a region of the genome that contains the tyramine receptor gene Amtyr1 . We then show that disruption of Amtyr1 signaling either pharmacologically or through RNAi increases expression of latent inhibition but has little effect on appetitive conditioning, and these results suggest that AmTYR1 modulates inhibitory processing in the CNS. Electrophysio-logical recordings from the brain during pharmacological blockade are consistent with a model that AmTYR1 regulates inhibition, such that without a functional AmTYR1 protein inhibition becomes strong and suppresses sensory responses that drive Hebbian plasticity underlying latent inhibition. Finally, sequencing Amtyr1 and its up and downstream genomic region for high and low line workers suggested that individual differences might arise from variation in transcriptional control rather than structural changes in the coding region. Our results therefore identify a distinct modulatory pathway for this type of non-associative learning, and we propose a model for how it modulates Hebbian plasticity at defined synapses in the CNS. We have shown elsewhere how this modulation also underlies potentially adaptive intracolonial learning differences among individuals that benefit colony survival.