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In the developing visual system of mammals, retinal axons from the two eyes compete for postsynaptic partners. After eye opening, this process is regulated in part by homeostatically constrained competition for synaptic connectivity with target neurons. However, prior to eye opening, the functional and synaptic basis of binocular map development is unclear. To examine the role of binocular interactions during early stages of visual map development, we performed in vitro patch-clamp recordings from the superior colliculus (SC) of neonatal mice. Using newly designed slice preparations, we compared retinocollicular synapse development in the medial SC, which receives binocular input, and the lateral SC, which is predominantly monocular. Surprisingly, we found that at P6-7, when eye-specific segregation has just emerged, retinocollicular synapses were stronger and more mature and dendritic arbors were more elaborate in the medial than the lateral SC. Furthermore, monocular enucleation of the ipsilateral eye at P0 selectively reduced synaptic strength and dendritic branching in the medial SC and abolished the differences normally observed between the two slices at P6-7. This specifically implicates binocular interactions in the development of retinocollicular connectivity prior to eye opening. Our findings contrast with the predictions of a constrained-connectivity model of binocular map development and suggest instead that binocular competition prior to eye opening enhances retinocollicular synaptic strength and the morphological development of retino-recipient neurons.

Synapse maturation is enhanced in the binocular region of the retinocollicular map prior to eye opening