We review the foundational principles and neurobiological mechanisms underlying neural integration in the oculomotor system, emphasizing the historical and contemporary understanding of how the brain maintains stable gaze through intricate neural circuits. Beginning with Sir Charles Sherrington’s concept of the brain’s unified, spatially integrative operations, the discussion advances to David Robinson’s introduction of the neural integrator, highlighting the importance of temporal integration for sustained eye-position signals. Focusing on the nucleus prepositus hypoglossi (NPH) as a prototype, we will review the extrinsic and intrinsic connectivity, neuronal properties, and synaptic interactions that facilitate neural integration. We underscore the roles of specific neuron types, connectivity patterns, membrane mechanisms, and neurotransmitter influences, such as cholinergic and noradrenergic modulation, in maintaining persistent activity. This review also addresses the consequences of neural integrator failure, exemplified by gaze-evoked nystagmus, and discusses parallels between animal models and human clinical conditions, demonstrating how the dysfunctions in the neural circuitry lead to oculomotor deficits. Overall, the review delineates the complex network principles ensuring seamless sensorimotor integration in eye movement control.