The role of sensory systems is to interpret real-world events to facilitate behavior. For instance, the visual system enacts compensatory eye movements based on a global motion representation, generated by combining local motion signals from the retina. However, due to the aperture problem, local motion signals are inherently ambiguous, and how the visual system solves the aperture problem is unclear. We studied how the mouse Nucleus of the Optic Tract (NOT) integrates retinal visual information and how this supports behavioral responses. NOT mediates the horizontal optokinetic reflex, the compensatory eye movement response to global visual shifts. NOT is the only non-retinal sensory structure necessary for this reflex and receives feedforward input from direction-selective retinal ganglion cells tuned to temporal motion (T-DSRGCs)[1]. NOT cells are direction selective[2,3], but their other functional properties are unknown. To investigate how NOT encodes motion across the visual field, we performed extracellular recordings in awake and anaesthetized mice (Fig.1a) and estimated receptive fields (RFs) in 186 cells. RFs had an elongated aspect ratio and their sizes ranged from ~10 (average for T-DSRGCs) to 55°, suggesting that single NOT cells encode motion direction in localized parts of the visual field but can integrate information over a much larger area compared to their retinal input (Fig.1b). At the population level, RFs were mostly located along and above the horizontal meridian, rather than spread across the entire visual field, as the distribution of T-DSRGCs in the retina would predict (Fig.1c). Using drifting gratings at different spatial locations, we found that both neural activity and strength of the optokinetic response (occurrence and gain) correlate with these spatial coordinates (Fig.1d), suggesting that NOT integrates motion information along the horizon. In sum, our findings demonstrate that the mouse optokinetic response relies on a specific region in visual space, that the receptive fields of NOT cells selectively cover this area, and that neural activity in NOT encodes motion information within this region. This organization likely supports the computation of horizontal optic flow during global visual shifts. These observations enhance our understanding of the mouse retina-NOT network and provide insight into how sensory systems extract behaviorally relevant information from the distributed representation of the sensory periphery.