SignificanceHere we used a visual blue opsin to induce asymmetric signaling in a cell. The opsin recruited endogenous G proteins and allowed immune cell migration to be optically steered with directional precision. Using this approach, cellular and molecular response dynamics were quantitated to facilitate computational modeling of migration. We identified an ultrasensitive switch-like signaling response that explains how immune cells filter background fluctuations in signals and respond decisively to persistent stimuli. This approach can be widely applied to understand G-protein–coupled receptor-stimulated signaling network control of other cell behaviors and potentially to control cell movements in whole animals.