A rapid and bidirectional reporter of neural activity reveals neural correlates of social behaviors in Drosophila

Neural activity is modulated over different timescales encompassing sub-seconds to days reflecting changes in external environment, internal state, and behavior. Using Drosophila as a model, we have developed a rapid and bidirectional reporter that provides a robust cellular readout of recent neural activity. This reporter utilizes nuclear vs cytoplasmic distribution of CREB-regulated transcriptional coactivator, CRTC. Subcellular distribution of GFP-tagged CRTC (CRTC::GFP) bidirectionally changes on the order of minutes and reflects both increases and decreases in neural activity. We establish an automated machine-learning-based routine for efficient quantification of reporter signal. Using this reporter, we demonstrate acute mating- evoked activation of peptidergic neurons. We further investigate the functional role of the master courtship regulator gene, fruitless, and show that fruitless is necessary to ensure activation of male arousal neurons by female cues. Together, our results establish CRTC::GFP as a bidirectional reporter of recent neural activity suitable for examining neural correlates in behavioral contexts.