G-protein coupled receptors (GPCRs), including the mu-opioid receptor, interact with G-proteins and other proteins via their intracellular face as required for signal transduction. However, characterization of the structure of the intracellular face of. GPCRs is complicated by the experimental methods used for structural characterization. In the present study we undertook a series of long-time molecular dynamics (MD) simulations, ranging from 1 to 5 mu s, on the mu-opioid receptor in both the dimeric and monomeric states. Results show intracellular loop 2 (ICL2) to sample an equilibrium between coiled and helical states. Intracellular loop 3 (ICL3) samples a wider range of conformations. Previously unobserved beta-sheet structures were primarily sampled in the simulations initiated from the inactive dimer conformation. In contrast, helical structures were sampled in simulations initiated from the active, monomer conformation. Notably, in the dimeric form of the receptor, both intramolecular and intermolecular beta-sheet structures were sampled, with the latter occurring between the two monomers. These results indicate that the sampling of beta-sheet structures can maintain the ICL3 in an inactive conformation that contributes to stabilization of the dimeric form of the receptor via interchain beta-sheet structures.