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 (for example, [1-3]). In central visual areas, one prominent natural border is formed by the confluence of information from the two eyes, the monocular-binocular border [4]. 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 [5]. Its superficial layers receive direct input from the majority of retinal ganglion cells and are retinotopically organized [6, 7]. Using two-photon calcium imaging, we recorded the activity of collicular neurons from the superficial layers of awake mice and determined their direction selectivity, orientation selectivity, and retinotopic location. This 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.

The processing of motion in visual scenes is important for detecting and tracking moving objects as well as for monitoring self-motion through the induced optic flow. Specialized neural circuits have been identified in the vertebrate retina for detecting motion direction or for distinguishing between object motion and self-motion, although little is known about how information about these distinct features of visual motion is combined. The salamander retina, which is a widely used model system for analyzing retinal function, contains object-motion-sensitive (

SummaryNeurons in sensory systems are often tuned to particular stimulus features. During complex naturalistic stimulation, however, multiple features may simultaneously affect neuronal responses, which complicates the readout of individual features. To investigate feature representation under complex stimulation, we studied how direction-selective ganglion cells in salamander retina respond to texture motion where direction, velocity, and spatial pattern inside the receptive field continuously change. We found that the cells preserve their direction preference under this stimulation, yet their direction encoding becomes ambiguous due to simultaneous activation by luminance changes. The ambiguities can be resolved by considering populations of direction-selective cells with different preferred directions. This gives rise to synergistic motion decoding, yielding more information from the population than the summed information from single-cell responses. Strong positive response correlations between cells with different preferred directions amplify this synergy. Our results show how correlated population activity can enhance feature extraction in complex visual scenes.