Visual Experience Is Required for the Development of Eye Movement Maps in the Mouse Superior Colliculus.

Topographic maps are a fundamental feature of the brain's representations of the sensory environment as well as an efficient way to organize motor control networks. Although great progress has been made in our understanding of sensory map development, very little is known about how topographic representations for motor control develop and interface with sensory maps. Here we map the representation for eye movements in the superior colliculus (SC) in awake mice. As stimulation sites were sampled along the anterior-posterior axis, small amplitude, nasally directed (ipsiversive) saccadic eye movements were evoked by microstimulation in anterior SC, followed by a smooth progression to large, temporally directed (contraversive) movements in posterior SC. This progressive change of movement amplitude and direction is consistent with the global polarity of the retinotopic map in the superficial SC, just as in primates and cats. We then investigated the role of visual experience in the development of eye movement map by studying mice reared in complete darkness. Saccades evoked by SC stimulation as well as spontaneous saccadic eye movements were larger in the dark-reared mice, indicating that visual experience is required to fine-tune the gain of saccades and to establish normal eye movement maps in the SC. Our experiments provide a foundation for future studies to investigate the synaptic organization and developmental mechanisms of sensorimotor transformations in mice. SIGNIFICANCE STATEMENT: The superior colliculus (SC) is a midbrain structure important for multisensory integration and sensorimotor transformation. Here we have studied eye movement representations in the SC of mice, a species that has become a popular model in vision research because of available genetic tools. Our studies show mice make saccadic eye movements spontaneously and in response to SC stimulation. The mouse SC contains an eye movement map that has the same global polarity as the overlaying visual map, just like in cats and primates. Furthermore, we show that visual experience is required for establishing the normal eye movement map. Our study provides a necessary basis for future mechanistic studies of how SC motor maps develop and become aligned with sensory maps.