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Migratory locusts (Locusta migratoria) emit two key odorants during aggregation: 4-vinylanisole (4VA), which serves as an aggregation pheromone attracting conspecifics to form swarms, and phenylacetonitrile (PAN), which acts as an aposematic signal and a precursor of a defense toxin, deterring conspecifics from cannibalism and protecting against predators. However, how locusts reconcile these two conflicting olfactory signals while aggregating is not yet understood. Our study addresses this by examining the release dynamics of the two signals, their behavioral effects, and the neural mechanisms underlying their perception. 4VA is released earlier and at lower locust densities than PAN, with PAN’s release increasing as aggregation progresses. Although PAN’s emission levels eventually exceed those of 4VA, locusts consistently exhibit a preference for the emitted blend, regardless of variations in proportions and concentrations. Notably, increasing amounts of 4VA added to PAN can counteract PAN’s repellent effects, but this is not the case when PAN is added to 4VA. Mechanistically, we found that antennal neurons responsive to 4VA suppress the activity of neurons responsive to PAN. In the antennal lobe, it is the conduction velocities of projection neurons, rather than other neural properties, that are responsible for the observed behavioral pattern, leading to an overall attractive response. Collectively, our findings imply that insects are capable of harmonizing the effects of two distinct pheromones to optimize both social cohesion and chemical defense. 

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 nonassociative conditioning called ‘latent inhibition’. 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 for latent inhibition to a region of the genome that contains the tyramine receptor geneAmtyr1[We use Amtyr1 to denote the gene and AmTYR1 the receptor throughout the text.]. We then show that disruption ofAmtyr1signaling either pharmacologically or through RNAi qualitatively changes the expression of latent inhibition but has little or slight effects on appetitive conditioning, and these results suggest that AmTYR1 modulates inhibitory processing in the CNS. Electrophysiological recordings from the brain during pharmacological blockade are consistent with a model that AmTYR1 indirectly regulates at inhibitory synapses in the CNS. Our results therefore identify a distinctAmtyr1-based modulatory pathway for this type of nonassociative learning, and we propose a model for howAmtyr1acts as a gain control to modulate 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. Finally, our neural model suggests a mechanism for the broad pleiotropy this gene has on several different behaviors. 

Animals are constantly bombarded with stimuli, which presents a fundamental problem of sorting among pervasive uninformative stimuli and novel, possibly meaningful stimuli. We evaluated novelty detection behaviorally in honey bees as they position their antennae differentially in an air stream carrying familiar or novel odors. We then characterized neuronal responses to familiar and novel odors in the first synaptic integration center in the brain–the antennal lobes. We found that the neurons that exhibited stronger initial responses to the odor that was to be familiarized are the same units that later distinguish familiar and novel odors, independently of chemical identities. These units, including both tentative projection neurons and local neurons, showed a decreased response to the familiar odor but an increased response to the novel odor. Our results suggest that the antennal lobe may represent familiarity or novelty to an odor stimulus in addition to its chemical identity code. Therefore, the mechanisms for novelty detection may be present in early sensory processing, either as a result of local synaptic interaction or via feedback from higher brain centers.