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During development, melanopsin-expressing intrinsically photosensitive retinal ganglion cells (ipRGCs) become light sensitive much earlier than rods and cones. IpRGCs project to many subcortical areas, whereas physiological functions of these projections are yet to be fully elucidated. Here, we found that ipRGC-mediated light sensation promotes synaptogenesis of pyramidal neurons in various cortices and the hippocampus. This phenomenon depends on activation of ipRGCs and is mediated by the release of oxytocin from the supraoptic nucleus (SON) and the paraventricular nucleus (PVN) into cerebral-spinal fluid. We further characterized a direct connection between ipRGCs and oxytocin neurons in the SON and mutual projections between oxytocin neurons in the SON and PVN. Moreover, we showed that the lack of ipRGC-mediated, light-promoted early cortical synaptogenesis compromised learning ability in adult mice. Our results highlight the importance of light sensation early in life on the development of learning ability and therefore call attention to suitable light environment for infant care. [Display omitted] • Light sensation through ipRGCs early in life promotes cortical synaptogenesis • Light enhances CSF oxytocin level via an ipRGCs-SON-PVN oxytocin neuron circuit • Oxytocin is essential for light-promoted ipRGC-mediated synaptogenesis • Lack of light sensation in early development impairs learning ability in adult mice Light sensation by intrinsically photosensitive retinal ganglion cells early in life ensures proper learning ability in adult mice by activating oxytocin-releasing neurons, which in turn promotes cortical synaptogenesis. [ABSTRACT FROM AUTHOR]