Octopamine (OA) and Dopamine (DA) are biological amines commonly found in insects and are involved in regulating learning and memory behaviors. OA and DA regulate insect physiological processes by binding specifically to their corresponding receptors, Octopamine receptors (OARs) and Dopamine receptors (DARs), respectively. The purpose of this study was to explore the differential regulatory effects of OA and DA on olfactory learning and memory retrieval in Bactrocera dorsalis through pharmacological intervention. The results showed that the injection of two OAR antagonists, phentolamine and yohimbine, significantly reduced reward-based olfactory learning of B. dorsalis but did not affect punishment-based olfactory learning. The effects of these antagonists were influenced by both injection concentration and time. In contrast, the injection of two DAR antagonists, SCH23390 and spiperone, significantly reduced punishment-based olfactory learning but had no effect on reward-based olfactory learning. The effects of these DAR antagonists were primarily influenced by injection concentration. In memory retrieval experiments, the injection of OAR antagonists significantly impaired the retrieval of reward-based memories but did not affect punishment-based memories. The effect of phentolamine was dependent on injection time, while the effect of yohimbine was dependent on injection concentration. On the other hand, the injection of DAR antagonists impaired the retrieval of both reward and punishment memories. Specifically, SCH23390 mainly reduced the retrieval of punishment-based olfactory memories, while spiperone primarily reduced the retrieval of reward-based olfactory memories. These results indicate that OA and DA play distinct roles in regulating olfactory learning and memory retrieval in B. dorsalis. The findings provide a theoretical foundation for developing behavior regulators targeting insect learning processes.

To ensure the reliability of learned information, most insects require multiple intervals of experience before storing the information as long-term memory (LTM), and this requirement has been validated in insects from the behavioral to the molecular level. Recent studies have shown that some insects can form LTM after one-trial experience, although the mechanisms underlying one-trial LTM formation are not well understood. Therefore, understanding the mechanisms underlying rapid learning and subsequent preference formation in insects is crucial. Here we show that the agricultural pest Bactrocera dorsalis can rapidly form LTM, which is dependent on protein synthesis, and that the formation of LTM requires high energy support at the cost of reduced survival. Furthermore, based on a liquid chromatography-mass spectrometry (LC-MS) metabolomics approach, we found that LTM-related processes are sequentially coupled to two processes for energy generation, the TCA cycle and oxidative phosphorylation. This was further confirmed by blocking these energy generation processes. Our results provide a theoretical basis for the development of behavioral modulators in oriental fruit flies that target energy generation metabolites, as well as a new perspective on the rapid formation of LTM in insects.