Threat gates visual aversion via theta activity in Tachykinergic neurons

Animals must adapt sensory responses to an ever-changing environment for survival. Such sensory modulation is especially critical in a threatening situation, in which animals often promote aversive responses to, among others, visual stimuli. Recently, threatened Drosophila has been shown to exhibit a defensive internal state. Whether and how threatened Drosophila promotes visual aversion, however, remains elusive. Here we report that mechanical threats to Drosophila transiently gate aversion from an otherwise neutral visual object. We further identified the neuropeptide tachykinin, and a single cluster of neurons expressing it (“Tk-GAL4(2) ∩ Vglut neurons”), that are responsible for gating visual aversion. Calcium imaging analysis revealed that mechanical threats are encoded in Tk-GAL4(2) ∩ Vglut neurons as elevated activity. Remarkably, we also discovered that a visual object is encoded in Tk-GAL4(2) ∩ Vglut neurons as θ oscillation, which is causally linked to visual aversion. Our data reveal how a single cluster of neurons adapt organismal sensory response to a threatening situation through a neuropeptide and a combination of rate/temporal coding schemes.