Rhodopsin is a prototype for the large Family A of G-protein-coupled receptors (GPCRs). These proteins regulate many signaling processes, and more than 35% of human pharmaceuticals are targeted against diseases related to dysfunctions of GPCR pathways. Membrane proteins such as GPCRs are challenging to crystallize for X-ray studies. In addition, their effective molar masses in detergent solutions push the limits for solution NMR spectroscopy. By contrast, solidstate NMR allows both the structure and dynamics of membrane proteins to be investigated in a natural lipid bilayer environment. Here, we describe solid-state ²H NMR methods for investigating structural and dynamical changes of the retinylidene cofactor of the GPCR rhodopsin upon photoillumination. Rhodopsin was regenerated with retinal containing ²H-labeled C5-, C9-, or C13-methyl groups. The receptor was recombined with phospholipid membranes, which were aligned on planar glass slides. The angular dependences of the ²H NMR spectra and the corresponding relaxation rates were measured for rhodopsin in the dark and in the cryo-trapped, preactive Meta-I and active Meta-II states. Analysis of the ²H NMR lineshapes using a static uniaxial distribution yields orientational restraints for the retinylidene conformation when bound to the protein. Solid-state ²H NMR relaxation data provide additional information on the motion of the bound cofactor. The structural and dynamical changes of retinal reveal howits functional groups (methyl groups and the ß-ionone ring) affect rhodopsin light activation, and illustrate the opportunities of solid-state ²H NMR spectroscopy in studying membrane proteins.