The pore-lining helix (PLH) bundles are central to the function of all ion channels, as their conformational rearrangements dictate channel gating. Here, we explore all plausible oligomeric arrangements of the PLH bundles within homomeric ion channels by building models using generic restraints. In particular, the distance between two neighboring PLHs was bounded both below and above in order to avoid steric clash and allow proper packing. The resulting models provide a theoretical representation of the accessible space for oligomeric arrangements. While the represented space is confined, it encompasses nearly all the ion channel PLH bundles for which the structures are currently known. For a multitude of channels, gating models suggested by paths within the confined accessible space are in qualitative agreement with those established in previous structural and computational studies.