Highlights d LPLC2 and LC4 are the primary direct visual inputs to the giant fiber (GF) d The GF sums LPLC2 and LC4 input to drive escape from looming d LPLC2-GF input encodes looming size, whereas LC4-GF input encodes looming speed d A model summing looming size and speed optical variables reproduces GF responses

An approaching predator and self-motion towards an object can generate similar looming patterns on the retina, but these situations demand different rapid responses. How central circuits flexibly process visual cues to activate appropriate, fast motor pathways remains unclear. Here, we identify two descending neuron (DN) types that control landing and contribute to visuomotor flexibility in Drosophila . For each, silencing impairs visually-evoked landing, activation drives landing, and spike rate determines leg extension amplitude. Critically, visual responses of both DNs are severely attenuated during non-flight periods, effectively decoupling visual stimuli from the landing motor pathway when landing is inappropriate. The flight-dependence mechanism differs between DN types. Octopamine exposure mimics flight effects in one, whereas the other likely receives neuronal feedback from flight motor circuits. Thus, this sensorimotor flexibility arises from distinct mechanisms for gating action-specific descending pathways, such that sensory and motor networks are coupled or decoupled according to the behavioral state.

SummaryBackgroundLimb movements are generally driven by active muscular contractions working with and against passive forces arising in muscles and other structures. In relatively heavy limbs, the effects of gravity and inertia predominate, whereas in lighter limbs, passive forces intrinsic to the limb are of greater consequence. The roles of passive forces generated by muscles and tendons are well understood, but there has been little recognition that forces originating within joints themselves may also be important, and less still that these joint forces may be adapted through evolution to complement active muscle forces acting at the same joint.ResultsWe examined the roles of passive joint forces in insect legs with different arrangements of antagonist muscles. We first show that passive forces modify actively generated movements of a joint across its working range, and that they can be sufficiently strong to generate completely passive movements that are faster than active movements observed in natural behaviors. We further demonstrate that some of these forces originate within the joint itself. In legs of different species adapted to different uses (walking, jumping), these passive joint forces complement the balance of strength of the antagonist muscles acting on the joint. We show that passive joint forces are stronger where they assist the weaker of two antagonist muscles.ConclusionsIn limbs where the dictates of a key behavior produce asymmetry in muscle forces, passive joint forces can be coadapted to provide the balance needed for the effective generation of other behaviors.