Misalignment of a covered eye reveals frontoparallel smooth pursuit is driven by multiple signals

Smooth pursuit research assumes a unitary command rotates both eyes for conjugate and vergence movements (Hering’s Law). Recent work challenged the unitary vergence command when an occluded eye rotated asynchronously with the target during vergence pursuit (Chandna et al., 2021), suggesting independent ocular control. Here we similarly occlude an eye to test if independent control drives conjugate pursuit. Neurotypical observers (N = 10) fixated, then pursued a dot (0.4 deg) moving on a tangent screen horizontally, either sinusoidally, or with random direction reversals (peak target velocity 25 or 5 deg/s). An infrared occluder permitted binocular recording with an EyeLink+ (1000 Hz) under monocular viewing. During binocular viewing, both eyes pursued the target accurately. During monocular fixation before pursuit, the occluded eye’s rotational position was displaced slightly either outward or inward, consistent with “phoria”, a clinical ocular misalignment that also occurs in neurotypicals. During monocular pursuit the occluded eye’s displacement persisted. Despite misalignment, both eyes matched the target’s velocity during monocular pursuit, evidence for a unitary conjugate command. The results suggest that independent controllers maintain ocular alignment during pursuit while a unitary motor command drives it.