The biogenic amine octopamine (OA, invertebrate counterpart of noradrenaline) plays critical roles in the regulation of olfactory behavior. Historically, OA has been thought to mediate appetitive but not aversive learning in honeybees, fruit flies (Drosophila), and crickets. However, this viewpoint has recently been challenged because OA activity through a β-adrenergic-like receptor drives both appetitive and aversive learning. Here, we explored the roles of OA neurons in olfactory learning and memory retrieval in Bactrocera dorsalis. We trained flies to associate an orange odor with a sucrose reward or to associate methyl eugenol, a male lure, with N,N-diethyl-3-methyl benzoyl amide (DEET) punishment. We then treated flies with OA receptor antagonists before appetitive or aversive conditioning and a memory retention test. Injection of OA receptor antagonist mianserin or epinastine into the abdomen of flies led to impaired of appetitive learning and memory retention with a sucrose reward, while aversive learning and memory retention with DEET punishment remained intact. Our results suggest that the OA signaling participates in appetitive but not aversive learning and memory retrieval in B. dorsalis through OA receptors.
Learning and memory are the most characterized advanced neurological activities of insects, which can associate information with food. Our previous studies on Bactrocera dorsalis have shown that this fly can learn to evaluate the nutritional value of sugar rewards, although whether all metabolizable sugars are equally rewarding to flies is still unclear. To address this question, we used three sweet and metabolizable sugars – sucrose, fructose and glucose – as rewards for conditioning. The flies showed differences in learning and memory in response to the three sugar rewards. The level of learning performance in sucrose-rewarded flies was higher than that in fructose-rewarded and glucose-rewarded flies, and, strikingly, only sucrose and glucose stimulation led to the formation of robust 24-h memory. Furthermore, the unequal rewarding of three sugars was observed in two distinct processes of memory formation: preingestive and postingestive processes. When flies received the positive tastes (preingestive signal) by touching their tarsi and proboscis (mouthparts) to three sugars, they showed differences in learning for the three sugar rewards. The formation of a robust 24-h memory was dependent on the postingestive signal triggered by feeding on a sugar. A deficit of 24-h memory was observed only in fructose-feeding flies no matter what sugar was used to stimulate the tarsi. Taken together, our results suggest that three sweet and metabolizable sugars unequally rewarded B. dorsalis, which might be a strategy for flies to discriminate the nature of sugars.
Studies on insects have contributed significantly to a better understanding of learning and memory, which is a necessary cognitive capability for all animals. Although the formation of memory has been studied in some model insects, more evidence is required to clarify the characteristics of memory formation, especially long‐term memory (LTM), which is important for reliably storing information. Here, we explored this question by examining Bactrocera dorsalis, an agricultural pest with excellent learning abilities. Using the classical conditioning paradigm of the olfactory proboscis extension reflex (PER), we found that paired conditioning with multiple trials (>3) spaced with an intertrial interval (≥10 min) resulted in stable memory that lasted for at least 3 d. Furthermore, even a single conditioning trial was sufficient for the formation of a 2‐d memory. With the injection of protein inhibitors, protein‐synthesis‐dependent memory was confirmed to start 4 h after training, and its dependence on translation and transcription differed. Moreover, the results revealed that the dependence of memory on protein translation exhibited a time‐window effect (4–6 h). Our findings provide an integrated view of LTM in insects, suggesting common mechanisms in LTM formation that play a key role in the biological basis of memory.
To adapt to the environment, it is important for insects to learn and evaluate food quality to avoid toxins in food. Currently, attractants are widely used for pest control, as they are environmentally friendly pesticides. Learning to associate an attractive odor with a toxin in food may influence insect behaviour in response to the attractant, thus affecting its application. In this study, we found that Bactrocera dorsalis, a serious pest of fruits and vegetables, can learn to associate a male lure compound, methyl eugenol (ME), with a sucrose solution contaminated with N,N‐diethyl‐3‐methyl benzoyl amide (DEET), a common insect repellent and decrease its proboscis extension response (PER) elicited by ME. Learning with DEET depends on its concentration, and flies exhibited significant aversive memory formation when high concentrations were used. Aversive‐DEET memory formed with 0.6% DEET persisted for at least 24 hr. We also found that aversive memory formed during training could be transferred to a behavioural response in an operant context.
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