The polypeptide backbone of gramicidin lines the channel lumen, which maintains a single file string of water molecules and the occasional cation. Whether or not local motions of the backbone are important for facilitating cation transport has been the subject of debate. Here it is demonstrated that motions of the backbone occur on the same time scale as cation translation through this transmembrane channel. To characterize the frequency of the local motions, field-dependent 15N T1 relaxation times were interpreted in light of an independently determined motional model that defines the motions as occurring about the C alpha-C alpha axis. To overdamp these local motions, several models that involve extensive correlations of the molecular motions were considered. One of these schemes for correlated motions suggests a unidirectional reaction path that would minimize the time necessary for the cation to pass through the low-dielectric center of the bilayer.