The motional dynamics of lens proteins were studied by two 13C nuclear magnetic resonance (NMR) techniques sensitive to molecular motion to define the effect of lens water content on the presence of solid-like protein domains in ocular lenses from bovine (juvenile and adult), human, rat, and chicken eyes. The solid state 13C NMR technique of proton dipolar decoupling was used to study slow (solid-like) motions (correlation time, tau o > or = 10 microseconds), whereas for intermediate (mobile) protein, rotational reorientational motion (tau o range of 1-500 nsec) the 13C off-resonance rotating frame spin-lattice relaxation technique was employed. 13C NMR studies of calf lens cortical and nuclear homogenates indicated a reversible loss of lens protein motional freedom with decreasing water content. Values of 6% and 63% solid-like protein contents were obtained for native cortical and nuclear calf lens homogenates, respectively. At equivalent total protein concentrations cortical and nuclear calf lens homogenates exhibited essentially the same solid-like (motionally restricted) protein content. Lens protein rotational correlation times determined by off-resonance rotating frame spin-lattice relaxation measurements were consistent with lens protein aggregation. The solid-like protein content of the bovine nuclear lens region was observed to increase with age, whereas no significant change was detected for the cortex. Across lens species an inverse correlation between the percentage of solid-like protein content and water content was observed. Very broad 13C NMR resonances, even in the presence of proton dipolar decoupling, were observed for the lens proteins present in the cataractous human lens, indicating the presence of highly aggregated protein species. The occurrence of solid-like protein domains in lens tissue has implications for the interpretation of proton nuclear magnetic resonance dispersion (NMRD) measurements of lens homogenates and for proton magnetization transfer contrast enhanced magnetic resonance imaging of lens. Solid-like protein domains may play a protective role in the maintenance of lens transparency by minimizing enhanced refractive index fluctuations created by protein packing defects resulting from post-translational modification.