G-protein coupled receptors (GPCRs) are the largest family of membrane signaling proteins. They respond to a wide-array of stimuli and contain a seven transmembrane domain that couples to heterotrimeric G-proteins. These pathways play roles in controlling second messenger levels and regulating other signaling proteins, such as ion channels and kinases. Due to their importance in many diseases, GPCRs are the most explored drug targets in biology. Despite this, the specific biochemical, physiological, and behavioral roles of many GPCRs are not well-understood and make this field ripe for the application of new tools for high-precision probing. We have developed an approach to elucidate the function of a GPCR by chemically re-engineering it to be sensitive to light. The class C glutamate-gated GPCR, mGluR2, which couples to the Gi/o pathway, was derivatized with photoswitchable ligands to generate both light-agonized (LimGluR2) and light-antagonized (“LimGluR2-block”) receptors. The bistable, azobenzene photoswitch enables activation by a light pulse to be sustained for long periods in the dark before being switched off by a longer wavelength light pulse. LimGluR2 deactivates quickly and supports multiple reproducible rounds of on/off switching with superior fidelity and speed compared to Rhodopsin. We have extended optical control to a variety of mGluRs with distinct G-protein coupling profiles. These designed receptors provide excellent tools for the dissection of the specific roles of different mGluRs in physiological functions, such as induction of synaptic plasticity, with high spatiotemporal precision. Furthermore, the high level of control afforded by tethered agonists allows for the probing of coupling of ligand-binding to receptor activation with single-subunit control. Along with single-molecule fluorescence experiments, we have used optical control via LimGluRs to probe the mechanisms of assembly and cooperative activation in the class C GPCRs.