Prior studies of the human translational vestibulo-ocular reflex (tVOR) report that eye rotations amount to less than 60% of those required to keep the eyes pointed at a stationary visual target, unlike the angular VOR (aVOR) which is optimized to maintain stable gaze. Our first goal was to determine if the performance of the tVOR improves when head translations are combined with head rotations in ambient lighting. A second goal was to measure tVOR during vertical head translations (bob), which has not received systematic study. We measured tVOR alone and in combination with the aVOR in 20 normal human subjects, aged 25-72 years, as they sat on a moving platform that bobbed at 2.0 Hz while rotating horizontally (yaw) at 1.0 Hz. When subjects viewed a visual target at 2 m, median "compensation gain" (eye rotational velocity/required eye rotational velocity to maintain foveal target fixation) was 0.52 during pure bob and 0.59 during combined bob-yaw; during viewing of a near target at approximately 17 cm, compensation gain was 0.58 for pure bob and 0.60 for combined bob-yaw. Mean phase lag of eye-in-head velocity for the tVOR was approximately 19 degrees with respect to the ideal compensatory response, irrespective of whether translation was accompanied by rotation. Thus, the tVOR changed only slightly during translation-rotation versus pure translation, and our subjects' ocular rotations remained at about 60% of those required to point the eyes at the target. Comparison of response during binocular or monocular viewing, and ambient or reduced illumination, indicated that relative image motion between the target and background was an important determinant of tVOR behavior. We postulate that tVOR evolved not to stabilize the image of the target on the fovea, but rather to minimize retinal image motion between objects lying in different planes, in order to optimize motion parallax information.