<p>The functioning of brain networks can be broadly categorized as an interplay of two main contributors, namely the neurological processes dictating the local dynamics and the patterns of anatomical connections that enable the interactions between the various local processes, resulting in a global emergent behavior. Using Brain Network Modeling (BNM) we describe the constraints of the anatomical structure upon the resting state dynamics of the human brain. We identify a low-dimensional representation of the brain states, the Resting State Manifold (RSM), and leveraging network degeneracy and its relationship to structural properties, we identify dynamic patterns supported by the RSM. Noise driven dynamics of the BNM are used to explore the manifold and validate the contours of degeneracy. We demonstrate that the patterns of degeneracy regulate the dynamics of the broader system in the presence of external and/or internal perturbations, revealing the productive relationship between emergent network processes and their constituent network entities.</p>