In vivo studies have demonstrated that the superior colliculus (SC) integrates sensory information and plays a role in controlling orienting motor output. However, how the complex microcircuitry within the SC, as documented by slice studies, subserves these functions is unclear. Optogenetics affords the potential to examine, in behaving animals, the functional roles of specific neuron types that comprise heterogeneous nuclei. As a first step toward understanding how SC microcircuitry underlies motor output, we applied optogenetics to mice performing an odor discrimination task in which sensory decisions are reported by either a leftward or rightward SC-dependent orienting movement. We unilaterally expressed either channelrhodopsin-2 or halorhodopsin in the SC and delivered light in order to excite or inhibit motor-related SC activity as the movement was planned. We found that manipulating SC activity predictably affected the direction of the selected movement in a manner that depended on the difficulty of the odor discrimination. This study demonstrates that the SC plays a similar role in directional orienting movements in mice as it does in other species, and provides a framework for future investigations into how specific SC cell types contribute to motor control.