Abstract Brain function is based on neural systems that comprise a combination of long-range recurrent connections among many brain regions and local circuits to perform specific computations within each region. Our goal is to understand how a full neural system mediates specific brain functions. We address this general question through investigation of a specific visual-motor behavior in non-human primates: visual guidance of smooth pursuit eye movements. The neural system for pursuit includes extrastriate visual area MT, the smooth eye movement region of the frontal eye fields (FEFSEM), the dorsolateral pontine nucleus (DLPN) and nucleus reticularis tegmenti pontis (NRTP) in the brainstem, and the floccular complex of the cerebellum. The major deliverable of this project is an understanding of the neural system for smooth pursuit eye movements in terms of the features of a canonical visual-motor/sensory-motor circuit. Our first aim will ask how signals are transformed in the cortico-cortical pathways between MT and FEFSEM. We will record multiple signal units simultaneously in both structures while varying the degree of correlation in small patches of moving dots to control the reliability of visual motion signals. In addition to asking how signals are transformed between the two areas, we will use noise correlations between simultaneously recorded neurons in MT and FEFSEM to constrain the architecture of their interconnections. Our second aim will reveal the nature of the visual-motor transformation in a cortico-ponto-cerebellar pathway from MT and FEFSEM to the floccular complex of the cerebellum. We will complement existing data from MT and the pons by recording in FEFSEM and the floccular complex under conditions that will complete our understanding of the representation and processing of visual- motor gain and expectations of target speed. Our third aim will explore recurrent connections from the floccular complex of the cerebellum to the motor cortex for pursuit, FEFSEM. We will stimulate in the floccular complex during both fixation and steady-state tracking while recording from neurons in FEFSEM. The proposed experiments will extend our knowledge of the operation of the sensory-motor circuit for pursuit, place it in the context of the architecture of a canonical visual-motor/sensory-motor system, and reveal what transformations occur in local circuits versus in long-range connections between nodes of the full system.