From Reflexes to Prediction: Kathleen E. Cullen’s Contribution to Modern Vestibular Neuroscience and Clinical Otoneurology—A Conceptual Narrative Review

Background: The vestibular system has traditionally been interpreted within a reflex-based framework, mainly centered on gaze stabilization, vestibulo-ocular reflex pathways, and peripheral vestibular deficits. This model remains essential, but it is insufficient to explain the full spectrum of postural, perceptual, visual-motion, and self-motion complaints observed in contemporary clinical otoneurology. Objective: This conceptual narrative review examines selected representative works by Kathleen E. Cullen as landmarks in a broader transition from reflex physiology to predictive, multimodal, context-dependent, body-centered self-motion control. Methods: This is not a systematic or bibliometric review. Papers were selected because they mark distinct conceptual steps in Cullen’s work: neural encoding of self-motion, peripheral and central coding strategies, multimodal integration, active versus passive self-motion, reafference suppression, body-centered encoding, proprioceptive prediction, vestibular cerebellar internal models, sensory reweighting, and clinical translation. Synthesis: Angelaki and Cullen’s 2008 synthesis and Cullen’s subsequent work demonstrate that vestibular processing is inherently multimodal from the earliest central stages and that neural representations of self-motion depend on behavioral context. Vestibular nuclei, visual-vestibular networks, and vestibular cerebellar circuits integrate labyrinthine signals with optic flow, proprioceptive, oculomotor, motor, cerebellar, cortical, and contextual information. This architecture enables the brain to distinguish expected from unexpected motion, suppress predictable vestibular reafference during voluntary action, compute internal estimates of body motion, adapt to altered sensory reliability, and reweight sensory inputs according to task demands. Conclusions: The clinical relevance of this trajectory is substantial. Patients may show preserved high-acceleration vestibulo-ocular reflex responses while experiencing persistent instability, visually induced dizziness, defective self-motion perception, or abnormal sustained vestibular processing. Such dissociations are not paradoxical when the vestibular system is understood as a predictive, distributed, body-centered control system. Cullen’s long lesson offers a neurophysiological foundation for a modern vestibular grammar in which clinical findings are interpreted across the reflexive, perceptual, postural, visual-vestibular, sustained, and predictive domains.