Motion of an image across the retina degrades visual accuracy, thus eye position must be held stationary. The horizontal eye velocity-to-position neural integrator (PNI), located in the caudal hindbrain of vertebrates, is believed to be responsible since the neuronal firing rate is sustained and proportional to eye position. The physiological mechanism for PNI function has been envisioned to be either (1) network dynamics within or between the bilateral PNI including brainstem/cerebellar pathways or (2) cellular properties of PNI neurons. These hypotheses were investigated by recording PNI neuronal activity in goldfish during experimental paradigms consisting of disconjugacy, commissurectomy and cerebellectomy.In goldfish, the eye position time constant ([tau]) is modifiable by short-term (~1 hr) visual feedback training to either drift away from, or towards, the center of the oculomotor range. Although eye movements are yoked in direction and timing, disconjugate motion during [tau] modification suggested separate PNIs to exist for each eye. Correlation of PNI neural activity with eye position during disconjugacy demonstrated the presence of two discrete neuronal populations exhibiting ipsilateral and conjugate eye sensitivity. During monocular PNI plasticity, [tau] was differentially modified for each eye corroborating coexistence of distinct neuronal populations within PNI.The hypothesized role of reciprocal inhibitory feedback between PNI was tested by commissurectomy. Both sustained PNI activity and [tau] remained with a concurrent nasal shift in eye position and decrease in oculomotor range. [tau] modification also was unaffected, suggesting that PNI function is independent of midline connections.The mammalian cerebellum has been suggested to play a dominant role for both [tau] and [tau] modification. In goldfish, cerebellar inactivation by either aspiration or pharmacology both prevented and abolished [tau] modifications, but did not affect eye position holding. PNI neurons still exhibited eye position related firing and modulation during training.By excluding all network circuitry either intrinsic or extrinsic to PNI, these results favor a cellular mechanism as the major determinate of sustained neural activity and eye position holding. By contrast, while cerebellar pathways are important for sustaining large [tau] (>20s), they are unequivocally essential for [tau] modification.