Misfolded species of the 140-residue protein a-synuclein (alpha S) are implicated in the demise of dopaminergic neurons, resulting in fatal neurodegenaration. The intrinsically unstructured protein binds curved synaptic vesicle membranes in helical conformations but misfolds into amyloid fibrils via beta-sheet interactions. Breaks in helical alpha S conformation may offer a pathway to transition from helical to sheet conformation. Here, we explore the evolution of broken alpha S helix conformations formed in complex with SDS and SLAS micelles by molecular dynamics simulations. The population distribution of experimentally observed alpha S conformations is related to the spatial concentration of intrinsic micelle shape perturbations: For the success of micelle induced alpha S folding, we posit the length of the first helical segment formed, which controls micelle ellipticity, to be a key determinant. The degree of micelle curvature relates to the arrangement and segmental motions of helical secondary structure elements. A criterion for assessing the reproduction of such intermediate time scale protein dynamics is introduced by comparing the sampling of experimental and simulated spin label distributions. Finally, at the sites of breaks in the elongated, marginally stable alpha S helix, vulnerability to forming a transient, intramolecular beta-sheet is identified. Upon subsequent; intermolecular beta-sheet pairing, pathological alpha S amyloid formation from initial helical conformation is thus achievable.