The translational linear vestibulo-ocular reflex compensates most accurately for high frequencies of head translation, with response magnitude decreasing with declining stimulus frequency. However, studies of the perception of translation typically report robust responses even at low frequencies or during prolonged motion. This inconsistency may reflect the incorporation of non-directional sensory information associated with the vibration and noise that typically accompany translation, into motion perception. We investigated the perception of passive translation in humans while dissociating non-directional cues from actual head motion. In a Cue-Dissociation experiment, inter-aural (IA) motion was generated using either a linear sled whose mechanics generated noise and vibration cues that were correlated with the motion profile, or a multiaxis technique that dissociated these cues from actual motion. In a Trajectory-Shift experiment, IA motion was interrupted by a sudden change in direction (±30° diagonal) which produced a change in linear acceleration while maintaining sled speed, and therefore mechanical (non-directional) cues. During multi-axis Cue-Dissociation trials subjects reported erroneous translation perceptions that strongly reflected the pattern of non-directional cues, as opposed to nearly veridical percepts when motion and non-directional cues coincided. During Trajectory-Shift trials, subjects' percepts were initially accurate, but erroneous following the direction change. Results suggest that non-directional cues strongly influence the perception of linear motion, while the utility of cues directly related to translational acceleration is limited. One key implication is that "path integration" likely involves complex mechanisms that depend upon non-directional and contextual self-motion cues in support of limited and transient otolith-dependent acceleration input.