Dataset Information

Aversive gustatory learning and perception in honey bees.

ABSTRACT: Taste perception allows discriminating edible from non-edible items and is crucial for survival. In the honey bee, the gustatory sense has remained largely unexplored, as tastants have been traditionally used as reinforcements rather than as stimuli to be learned and discriminated. Here we provide the first characterization of antennal gustatory perception in this insect using a novel conditioning protocol in which tastants are dissociated from their traditional food-reinforcement role to be learned as predictors of punishment. We found that bees have a limited gustatory repertoire via their antennae: they discriminate between broad gustatory modalities but not within modalities, and are unable to differentiate bitter substances from water. Coupling gustatory conditioning with blockade of aminergic pathways in the bee brain revealed that these pathways are not restricted to encode reinforcements but may also encode conditioned stimuli. Our results reveal unknown aspects of honey bee gustation, and bring new elements for comparative analyses of gustatory perception in animals.

SUBMITTER: Guiraud M

PROVIDER: S-EPMC5778057 | biostudies-literature | 2018 Jan

REPOSITORIES: biostudies-literature

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Aversive gustatory learning and perception in honey bees.

Guiraud Marie M Hotier Lucie L Giurfa Martin M de Brito Sanchez María Gabriela MG

Scientific reports 20180122 1

Taste perception allows discriminating edible from non-edible items and is crucial for survival. In the honey bee, the gustatory sense has remained largely unexplored, as tastants have been traditionally used as reinforcements rather than as stimuli to be learned and discriminated. Here we provide the first characterization of antennal gustatory perception in this insect using a novel conditioning protocol in which tastants are dissociated from their traditional food-reinforcement role to be lea ...[more]

PMID: 29358592

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Project description:Honey bees (Apis mellifera) provide a system for studying social and food-related behavior. A caste of workers performs age-related tasks: young bees (nurses) usually feed the brood and other adult bees inside the nest, while older bees (foragers) forage outside for pollen, a protein/lipid source, or nectar, a carbohydrate source. The workers' transition from nursing to foraging and their foraging preferences correlate with differences in gustatory perception, metabolic gene expression, and endocrine physiology including the endocrine factors vitellogenin (Vg) and juvenile hormone (JH). However, the understanding of connections among social behavior, energy metabolism, and endocrine factors is incomplete. We used RNA interference (RNAi) to perturb the gene network of Vg and JH to learn more about these connections through effects on gustation, gene transcripts, and physiology. The RNAi perturbation was achieved by single and double knockdown of the genes ultraspiracle (usp) and vg, which encode a putative JH receptor and Vg, respectively. The double knockdown enhanced gustatory perception and elevated hemolymph glucose, trehalose, and JH. We also observed transcriptional responses in insulin like peptide 1 (ilp1), the adipokinetic hormone receptor (AKHR), and cGMP-dependent protein kinase (PKG, or "foraging gene" Amfor). Our study demonstrates that the Vg-JH regulatory module controls changes in carbohydrate metabolism, but not lipid metabolism, when worker bees shift from nursing to foraging. The module is also placed upstream of ilp1, AKHR, and PKG for the first time. As insulin, adipokinetic hormone (AKH), and PKG pathways influence metabolism and gustation in many animals, we propose that honey bees have conserved pathways in carbohydrate metabolism and conserved connections between energy metabolism and gustatory perception. Thus, perhaps the bee can make general contributions to the understanding of food-related behavior and metabolic disorders.

Project description:Honeybees have remarkable learning abilities given their small brains, and have thus been established as a powerful model organism for the study of learning and memory. Most of our current knowledge is based on appetitive paradigms, in which a previously neutral stimulus (e.g., a visual, olfactory, or tactile stimulus) is paired with a reward. Here, we present a novel apparatus, the yAPIS, for aversive training of walking honey bees. This system consists in three arms of equal length and at 120° from each other. Within each arm, colored lights (λ = 375, 465 or 520 nm) or odors (here limonene or linalool) can be delivered to provide conditioned stimuli (CS). A metal grid placed on the floor and roof delivers the punishment in the form of mild electric shocks (unconditioned stimulus, US). Our training protocol followed a fully classical procedure, in which the bee was exposed sequentially to a CS paired with shocks (CS+) and to another CS not punished (CS-). Learning performance was measured during a second phase, which took advantage of the Y-shape of the apparatus and of real-time tracking to present the bee with a choice situation, e.g., between the CS+ and the CS-. Bees reliably chose the CS- over the CS+ after only a few training trials with either colors or odors, and retained this memory for at least a day, except for the shorter wavelength (λ = 375 nm) that produced mixed results. This behavior was largely the result of the bees avoiding the CS+, as no evidence was found for attraction to the CS-. Interestingly, trained bees initially placed in the CS+ spontaneously escaped to a CS- arm if given the opportunity, even though they could never do so during the training. Finally, honey bees trained with compound stimuli (color + odor) later avoided either components of the CS+. Thus, the yAPIS is a fast, versatile and high-throughput way to train honey bees in aversive paradigms. It also opens the door for controlled laboratory experiments investigating bimodal integration and learning, a field that remains in its infancy.

Project description:BackgroundSpray adjuvants are often applied to crops in conjunction with agricultural pesticides in order to boost the efficacy of the active ingredient(s). The adjuvants themselves are largely assumed to be biologically inert and are therefore subject to minimal scrutiny and toxicological testing by regulatory agencies. Honey bees are exposed to a wide array of pesticides as they conduct normal foraging operations, meaning that they are likely exposed to spray adjuvants as well. It was previously unknown whether these agrochemicals have any deleterious effects on honey bee behavior.Methodology/principal findingsAn improved, automated version of the proboscis extension reflex (PER) assay with a high degree of trial-to-trial reproducibility was used to measure the olfactory learning ability of honey bees treated orally with sublethal doses of the most widely used spray adjuvants on almonds in the Central Valley of California. Three different adjuvant classes (nonionic surfactants, crop oil concentrates, and organosilicone surfactants) were investigated in this study. Learning was impaired after ingestion of 20 µg organosilicone surfactant, indicating harmful effects on honey bees caused by agrochemicals previously believed to be innocuous. Organosilicones were more active than the nonionic adjuvants, while the crop oil concentrates were inactive. Ingestion was required for the tested adjuvant to have an effect on learning, as exposure via antennal contact only induced no level of impairment.Conclusions/significanceA decrease in percent conditioned response after ingestion of organosilicone surfactants has been demonstrated here for the first time. Olfactory learning is important for foraging honey bees because it allows them to exploit the most productive floral resources in an area at any given time. Impairment of this learning ability may have serious implications for foraging efficiency at the colony level, as well as potentially many social interactions. Organosilicone spray adjuvants may therefore contribute to the ongoing global decline in honey bee health.

Dataset Information

Aversive gustatory learning and perception in honey bees.

Publications

Aversive gustatory learning and perception in honey bees.

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