Motion and Orientation Selectivity in the Mouse Superior Colliculus

Sensory neurons often display an ordered spatial arrangement that enhances the encoding of specific features on different sides of natural borders in the visual field. In the early visual system, this has been observed in the chromatic organization of mouse photoreceptors to match the natural distribution of color above and below the horizon [1]; and in the primate superior colliculus where neurons in the upper visual field have smaller receptive fields to support more accurate saccades [2]. In central visual areas a second natural border is formed by the confluence of information from the two eyes, the monocular-binocular border [3]. Here we investigate whether receptive field properties of neurons in the mouse superior colliculus show any systematic organization about the monocular-binocular border. The superior colliculus is a layered midbrain structure that plays a significant role in the orienting responses of the eye, head and body [4]. Its superficial layers receive direct input from the majority of retinal ganglion cells and are retinotopically organized [5,6]. Using two-photon calcium imaging, we recorded the activity of collicular neurons from the superficial layers of awake mice while determining their direction selectivity, orientation selectivity and retinotopic location. These recordings revealed that nearby direction-selective neurons have a strong tendency to prefer the same motion direction. In retinotopic space, the local preference of direction-selective neurons shows a sharp transition in the preference for nasal versus temporal motion at the monocular-binocular border. The maps representing orientation and direction appear to be independent. These results illustrate the important coherence between the spatial organization of inputs and response properties within the visual system and suggest a re-analysis of the receptive field organization within the superior colliculus from an ecological perspective.status: publishe