Cross-modal predictive oculomotor control: visually acquired prediction transfers to vestibular-driven eye movements

Predictive motor control enables animals to compensate for sensorimotor delays and perform timely movements in dynamic environments. Although event timing prediction has been widely investigated in visually and auditorily evoked behaviours, its presence in the vestibular-motor system remains unclear. Moreover the extent to which predictive learning generalizes across sensory modalities is poorly understood. Recent studies in goldfish have demonstrated that the optokinetic response (OKR), a visually evoked reflexive eye movement, can transition into a predictive mode (pOKR) following exposure to periodic visual motion stimuli. In natural conditions the OKR operates alongside the vestibulo-ocular reflex (VOR) during head motion to achieve stable vision. Although the VOR rapidly counteracts head movement incompletely, the OKR reduces residual retinal image slip. Notably both reflexive eye movements share neural substrates in the cerebellum and brainstem, which have been demonstrated essential for pOKR acquisition. Here we hypothesized that the VOR could also acquire predictive control, and that predictive ability acquired through visual training as pOKR might transfer to the VOR. Using goldfish we found that periodic vestibular stimulation alone does not induce predictive VOR. However following pOKR acquisition through visual training the VOR evoked solely by vestibular stimulation exhibited predictive behaviour. These findings provide the first evidence that visually acquired predictive control can cross-modally transfer to the vestibular-motor system, which itself does not develop prediction through vestibular stimulation alone, highlighting the central role of cerebellar and brainstem circuits in integrating multimodal sensory inputs for adaptive predictive oculomotor behaviour. KEY POINTS: Predictive motor control compensates for sensorimotor delays by anticipating periodic events, yet its mechanisms have been studied mostly in visual and auditory systems, leaving vestibular-motor or cross-modal prediction largely unexplored. The vestibulo-ocular reflex (VOR) and optokinetic response (OKR), which stabilize vision during head motion in the light, share common brainstem and cerebellar circuits. Predictive OKR (pOKR) emerges after repeated exposure to periodic visual motion, enabling eye movements to decelerate prior to stimulus direction changes. Our results show that although periodic vestibular stimulation alone fails to induce predictive VOR, visual training that establishes pOKR enables predictive features to emerge in VOR-demonstrating for the first time, cross-modal transfer of predictive motor control. These findings reveal a novel form of cross-modal predictive motor learning and underscore the cerebellar-brainstem circuit's role in integrating multisensory experiences for adaptive motor function.