Using the photopigment melanopsin, intrinsically photosensitive retinal ganglion cells (ipRGCs) respond directly to light to drive circadian clock resetting and pupillary constriction. We now report that ipRGCs are more abundant and diverse than previously appreciated, project more widely within the brain, and can support spatial visual perception. A Cre-based melanopsin reporter mouse line revealed at least five subtypes of ipRGCs with distinct morphological and physiological characteristics. Collectively, these cells project beyond the known brain targets of ipRGCs to heavily innervate the superior colliculus and dorsal lateral geniculate nucleus, retinotopically-organized nuclei mediating object localization and discrimination. Mice lacking classical rod-cone photoreception, and thus entirely dependent on melanopsin for light detection, were able to discriminate grating stimuli from equiluminant gray, and had measurable visual acuity. Thus, non-classical retinal photoreception occurs within diverse cell types, and influences circuits and functions encompassing luminance as well as spatial information.

The virtual optomotor system provides a simple and precise method for rapidly quantifying mouse vision. Behavioral measures of vision in mice are essential for interpreting the results of experiments designed to reveal the cellular and molecular mechanisms of vision and visual development and for evaluating potential treatments for visual diseases.

We have developed a simple computer-based discrimination task that enables the quick determination of visual acuities in rodents. A grating is displayed randomly on one of two monitors at the wide end of a trapezoidal-shaped tank containing shallow water. Animals are trained to swim toward the screens, and at a fixed distance, choose the screen displaying the grating and escape to a submerged platform hidden below it. Both mice and rats learn the task quickly. Performance falls below 70% when the spatial frequency is increased beyond 0.5 cycles in most C57BU6 mice, and around 1.0 cycles per degree (cpd) in Long-Evans rats.

Slow horizontal head and body rotation occurs in mice and rats when the visual field is rotated around them, and these optomotor movements can be produced reliably in a virtual-reality system. If one eye is closed, only motion in the temporal-to-nasal direction for the contralateral eye evokes the tracking response. When the maximal spatial frequency capable of driving the response ("acuity") was measured under monocular and binocular viewing conditions, the monocular acuity was identical to the binocular acuity measured with the same rotation direction. Thus, the visual capabilities of each eye can be measured under binocular conditions simply by changing the direction of rotation. Lesions of the visual cortex had no effect on the acuities measured with the virtual optokinetic system, whereas perceptual thresholds obtained previously with the Visual Water Task are. The optokinetic acuities were also consistently lower than acuity estimates from the Visual Water Task, but contrast sensitivities were the same or better. These data show that head-tracking in a virtual optokinetic drum is driven by subcortical, lower frequency, and contralateral pathways.