Octopaminergic neurons function in appetitive but not aversive olfactory learning and memory in Bactrocera dorsalis

Abstract

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.

The modulatory effects of biogenic amines on male mating performance in Bactrocera dorsalis

“…To prevent mating, we separated male and female flies on the third day post emergence and placed male and female flies into separate chambers ( Markow, 1985 ). Each chamber (30 cm × 30 cm × 30 cm) consisted of 500 same-sex flies, and those males without contact with females since the third day post emergence are considered “virginal ♂” ( Yu et al, 2022 ). Males that have mated only once with females since emergence are considered as “mated ♂“, and were used for subsequent experiments within 24 h post mating.…”

“…3-Hydroxytyramine hydrochloride, octopamine hydrochloride, tyramine hydrochloride, serotonin hydrochloride, chlorpromazine hydrochloride, epinastine hydrochloride, and yohimbine hydrochloride were purchased from Macklin (Shanghai, China) and dissolved in RNase-Free Deionized water (DEPC water) at concentrations of 0.5 μg/μl and 0.05 μg/μl, respectively (concentration selection was followed by previous study) ( Lenschow et al, 2018 ; Li et al, 2020 ; Yu et al, 2022 ). Male flies (13th day post emergence) were injected with 0.4 µL of chemicals at a concentration of 0.5 μg/μl or 0.05 μg/μl, respectively.…”

“…, 2019 ). Previous studies have shown that biogenic amines play important roles in pupation, immune regulation, olfactory learning, and gut bacterial community homeostasis in B. dor s alis ( Chen et al, 2018 ; Yu et al, 2022 ; Zeng et al, 2022 ). However, their roles in regulation of courtship and mating behavior in B. dor s alis remain elusive.…”

“…This species causes a substantial loss of cultivated crops throughout most of Asia and damages more than 250 host fruits and vegetables worldwide (Zeng et al, 2018;Liu et al, 2019). Previous studies have shown that biogenic amines play important roles in pupation, immune regulation, olfactory learning, and gut bacterial community homeostasis in B. dorsalis (Chen et al, 2018;Yu et al, 2022;Zeng et al, 2022). However, their roles in regulation of courtship and mating behavior in B. dorsalis remain elusive.…”

Formation characteristics of long‐term memory in Bactrocera dorsalis

“…Postinjection, flies were placed in small cages with access to 1.0 mol/L sucrose ad libitum. This method induces minimal damage and stress, compared with brain injections, and has been successfully used in B. dorsalis (Yu et al, 2022).…”