Octopamine neuron dependent aggression requires dVGLUT from dual-transmitting neurons

Neuromodulators such as monoamines are often expressed in neurons that also release at least one fast-acting neurotransmitter. The release of a combination of transmitters provides both “classical” and “modulatory” signals that could produce diverse and/or complementary effects in associated circuits. Here, we establish that the majority of Drosophila octopamine (OA) neurons are also glutamatergic and identify the individual contributions of each neurotransmitter on sex-specific behaviors. Males without OA display low levels of aggression and high levels of inter-male courtship. Males deficient for dVGLUT solely in OA-glutamate neurons (OGNs) also exhibit a reduction in aggression, but without a concurrent increase in inter-male courtship. Within OGNs, a portion of VMAT and dVGLUT puncta differ in localization suggesting spatial differences in OA signaling. Our findings establish a previously undetermined role for dVGLUT in OA neurons and suggests that glutamate uncouples aggression from OA-dependent courtship-related behavior. These results indicate that dual neurotransmission can increase the efficacy of individual neurotransmitters while maintaining unique functions within a multi-functional social behavior neuronal network.

神经调质（Neuromodulators），如单胺类物质，通常在同时释放至少一种快速作用神经递质（fast-acting neurotransmitter）的神经元中表达。递质联合释放可同时产生"经典"与"调节性"信号，进而在相关神经环路中引发多样化或互补性效应。本研究证实，绝大多数果蝇章鱼胺（octopamine, OA）能神经元同时为谷氨酸能（glutamatergic）神经元，并明确了两种递质各自对性别特异性行为的独立调控作用。缺失章鱼胺的雄性果蝇表现出攻击行为水平低下，而雄性间求偶行为（inter-male courtship）水平升高。仅在章鱼胺-谷氨酸能神经元（OGNs）中敲除果蝇囊泡谷氨酸转运蛋白（dVGLUT）的雄性果蝇，同样表现出攻击行为减弱，但并未伴随雄性间求偶行为的升高。在章鱼胺-谷氨酸能神经元内，部分囊泡单胺转运蛋白（VMAT）与dVGLUT的点状结构存在分布差异，提示章鱼胺信号传导存在空间特异性。本研究明确了dVGLUT在章鱼胺能神经元中此前未被发现的功能，并证实谷氨酸可将攻击行为与依赖章鱼胺的求偶相关行为解偶联。上述结果表明，双重递质传递（dual neurotransmission）可在多功能社交行为神经元环路中维持各递质独特功能的同时，提升单个递质的作用效能。