The article introduces a bistable inhibitory optoGPCR, *Platyneris dumetilli* ciliary opsin (*PdCO*), which is an efficient and versatile tool for reversible manipulation of synaptic transmission in mammalian neurons. *PdCO* is characterized by its high light sensitivity, bidirectional switchability, and ability to suppress synaptic transmission with high temporal precision in vivo. It exhibits red-shifted activation and a narrow inactivation spectrum, making it suitable for spectral multiplexing with other optogenetic actuators and reporters. The study systematically evaluates multiple bistable opsins and finds that *PdCO* outperforms existing tools in terms of spectral and temporal features. *PdCO* is successfully used to conduct reversible loss-of-function experiments in long-range projections of behaving animals, enabling detailed synapse-specific functional circuit mapping. The biophysical properties of *PdCO* are detailed, including its G-protein specificity and spectral multiplexing capabilities. In vivo applications demonstrate the efficacy of *PdCO* in modulating mouse behavior, such as locomotion and pupil size, and its ability to impact motivated behavior. The study highlights the potential of *PdCO* as a versatile tool for studying projection-specific contributions to behavior.The article introduces a bistable inhibitory optoGPCR, *Platyneris dumetilli* ciliary opsin (*PdCO*), which is an efficient and versatile tool for reversible manipulation of synaptic transmission in mammalian neurons. *PdCO* is characterized by its high light sensitivity, bidirectional switchability, and ability to suppress synaptic transmission with high temporal precision in vivo. It exhibits red-shifted activation and a narrow inactivation spectrum, making it suitable for spectral multiplexing with other optogenetic actuators and reporters. The study systematically evaluates multiple bistable opsins and finds that *PdCO* outperforms existing tools in terms of spectral and temporal features. *PdCO* is successfully used to conduct reversible loss-of-function experiments in long-range projections of behaving animals, enabling detailed synapse-specific functional circuit mapping. The biophysical properties of *PdCO* are detailed, including its G-protein specificity and spectral multiplexing capabilities. In vivo applications demonstrate the efficacy of *PdCO* in modulating mouse behavior, such as locomotion and pupil size, and its ability to impact motivated behavior. The study highlights the potential of *PdCO* as a versatile tool for studying projection-specific contributions to behavior.