We report on progress toward improving NMR relaxation analysis in proteins in terms of the slowly relaxing local structure (SRLS) approach by developing a method that combines SRLS with molecular dynamics (MD) simulations. N-15-H bonds from the Rho GTPase binding domain of plexin-B1 are used as test case. We focus on the locally restricting/ordering potential of mean force (POMF), u(theta,phi), at the N-H site (theta and phi specify the orientation of the N-H bond in the protein). In SRLS, u(theta,phi) is expanded in the basis set of the real linear combinations of the Wigner rotation matrix elements with M = 0, D-L,D-vertical bar K vertical bar(theta,phi). Because of limited data sensitivity, only the lowest (L = 2) terms are preserved; this potential function is denoted by u((SRLS)). In MD, the force-field-parametrized POMF is the potential, u((MD)), defined in terms of the probability distribution, P-eq((MD)) proportional to exp(-u((MD))). P-eq((MD)), and subsequently u((MD)), can be derived from the MD trajectory as histograms. One might contemplate utilizing u((MD)) instead of u((SRLS)); however, histograms cannot be used in SRLS analyses. Here, we approximate u(theta,phi) in terms of linear combinations of the D-L,D-vertical bar K vertical bar functions with L = 1-4 and appropriate symmetry, denoted by u((DLK)), and optimize the latter (via P-eq) against u((MD)). This yields for every N-H bond an analytical ordering potential, u((DLK-BEST)), which exceeds u((SRLS)) considerably in accuracy. u((DLK-BEST)) can be used fixed in SRLS data fitting, thereby enabling the determination of additional parameters. This yields a substantially improved picture of structural dynamics, which is a significant benefit. The primary achievement of this work is to have employed for the first time MD data to derive a suitable (in terms of composition and symmetry) approximation to the SRLS POMF.