Lipid bilayers form the core of functional membrane platforms such as cellular plasma membranes. Their dynamics are inherently related to a wide range of physical and biological processes and thus have become the subject of both experimental measurements and theoretical investigations. Nuclear magnetic resonance (NMR) in particular, is able to probe a hierarchy of lipid motions by measuring the power spectrum of thermally excited molecular fluctuations. From this spectrum of molecular noise emerge both average conformational parameters such as chain order, SCD, and dynamical descriptors such as the relaxation rate, R1, of carbon-hydrogen (or deuterium) bond fluctuations. Interestingly, these experimental observables exhibit specific functional relationships including an SCD-R1 square-law dependence, and an R1 inverse square-root frequency law. Different theories explain these functional forms, but the convoluted nature of the NMR data complicates further decoupling of the signal and testing of underlying models. Here we use atomistic molecular dynamics (MD) simulations to investigate the underpinnings of the experimental results. We calculated SCD and R1 for a series of experimentally studied bilayers composed of unsaturated or saturated lipids with different cholesterol content and at different hydration levels. The simulation results show the same functional dependencies as those observed with NMR and reveal unprecedented details of the relevant molecular mechanisms. Following a recently developed paradigm, we use the slope of the SCD-R1 square-law dependence from the simulations to calculate the bilayer bending rigidity modulus kC and explore its underlying parameter space. Comparison to kC values obtained from MD splay fluctuations and neutron spin-echo measurements allows for a closer look at the complementary applications of the techniques. Our results provide novel and clarifying insights into the nature of experimentally accessible molecular motions and their biophysical implications.