We review recent progress in using numerical models to relate utricular hair bundle and otoconial membrane (OM) structure to the functional requirements imposed by natural behavior in turtles. The head movements section reviews the evolution of experimental attempts to understand vestibular system function with emphasis on turtles, including data showing that accelerations occurring during natural head movements achieve higher magnitudes and frequencies than previously assumed. The structure section reviews quantitative anatomical data documenting topographical variation in the structures underlying macromechanical and micromechanical responses of the turtle utricle to head movement: hair bundles, OM, and bundle-OM coupling. The macromechanics section reviews macromechanical models that incorporate realistic anatomical and mechanical parameters and reveal that the system is significantly underdamped, contrary to previous assumptions. The micromechanics: hair bundle motion and met currents section reviews work based on micromechanical models, which demonstrates that topographical variation in the structure of hair bundles and OM, and their mode of coupling, result in regional specializations for signaling of low frequency (or static) head position and high frequency head accelerations. We conclude that computational models based on empirical data are especially promising for investigating mechanotransduction in this challenging sensorimotor system.