Elucidating neural networks underlying behaviors is an essential task of neuroscience. Fruit fly, Drosophila melanogaster, offer significant advantages for this purpose since they exhibit easily quantifiable, robust and genetically traceable behaviors. We previously reported two consistent, context dependent mating behaviors, called longer- and shorter-mating duration (LMD and SMD). LMD is a rival-induced, prolonged mating duration and SMD a sexual experience-mediated shortened mating. We identified specific components of the underlying neural circuits and found that neuropeptide signaling plays a key role in regulating both behaviors.
We identified four SIFamide (SIFa) producing neurons located in the pars intercerebralis, which are critical to induce both behaviors. To identify how SIFamide signaling bridges between two distinct neuronal pathways, we hypothesized that SIFa neurons act as input-specific decision makers in the context of output, which is mating duration. We first screened neurotransmitter (NT) systems to test this theory since NTs are expressed in large but discrete populations of neurons, which allows for large-scale circuit mapping studies of SIFa signaling in the context of mating duration. We also tested sexually dimorphic neuronal populations in the context of SIFa signaling because LMD and SMD are male-specific behaviors.
To test the impact of SIFa signaling on mating duration, NT-GAL4 lines were crossed with UAS-SIFaR-RNAi to knock-down (KD) SIFaR protein expression in GAL4-labeled neurons. To minimize the developmental impact of SIFaR knockdown, crosses are kept at 18°C until adults eclose, then moved to 25°C. We identified that KD of SIFaR in GAD+ (GABAergic) and Tdc2+ (octopaminergic) neurons affects SMD while a SIFaR KD in Cha+ (cholinergic) and DDC+ (dopaminergic/serotonergic) neurons induced a loss of affects both LMD and SMD. These data suggest that SIFaR signaling in GABAergic/octopaminergic neurons is specifically involved with the SMD pathway while signaling in cholinergic and dopaminergic/serotonergic neurons affects both pathways of LMD/SMD. Inactivation of SIFaR+/fru+ neurons (intersectional method) disrupts only LMD not SMD. This data suggests that fru+ neurons are specifically involved with LMD.
All these data suggest that different groups of neurons are targeted by SIFa signaling depending on the social context (input), leading to distinct behavioral outputs. We suggest that SIFaR signaling pathways could be a good model to improve our understating of how neural computations decide different behavioral outputs depending on different input signals. The study of how this decision-making is achieved can provide new models for neuronal computation and a new insight on neural network architecture.