Understanding the mechanisms of protein folding requires knowledge of both the energy landscape and the structural dynamics of a protein. We report a neutron-scattering study of the nanosecond and picosecond dynamics of native and the denatured alpha-lactalbumin. The quasielastic scattering intensity shows that there are alpha-helical structure and tertiary-like side-chain interactions fluctuating on sub-nanosecond time-scales under extremely denaturing conditions and even in the absence of disulfide bonds. Based on the length-scale dependence of the decay rate of the measured correlation functions, the nanosecond dynamics of the native and the variously denatured proteins have three dynamic regimes. When 0.05<Q<0.5 A(-1) (where the scattering vector, Q, is inversely proportional to the length-scale), the decay rate, Gamma, shows a power law relationship, Gamma proportional to Q(2.42+/-0.08), that is analogous to the dynamic behavior of a random coil. However, when 0.5<Q<1.0 A(-1), the decay rate exhibits a Gamma proportional to Q(1.0+/-0.2) relationship. The effective diffusion constant of the protein decreases with increasing Q, a striking dynamic behavior that is not found in any chain-like macromolecule. We suggest that this unusual dynamics is due to the presence of a strongly attractive force and collective conformational fluctuations in both the native and the denatured states of the protein. Above Q>1.0 A(-1) is a regime that displays the local dynamic behavior of individual residues, Gamma proportional to Q(1.8+/-0.3). The picosecond time-scale dynamics shows that the potential barrier to side-chain proton jump motion is reduced in the molten globule and in the denatured proteins when compared to that of the native protein. Our results provide a dynamic view of the native-like topology established in the early stages of protein folding. Copyright 2001 Academic Press.