Eye-opening dependent elaboration and refinement of the cortical projection to the superficial superior colliculus in rats

Abstract

The superior colliculus (SC) is a multi-layered midbrain structure responsible for multimodal integration and orienting behavior in mammals. The superficial layers of the SC (sSC) receive direct visual input from retinal ganglion cells (RGC) as well as input from pyramidal cells in layer V of the ipsilateral visual cortex (VC). The retinal input is refined well before eye opening (EO) and RGC axons arborize topographically to form an appropriate map of visual space. The projection from VC is still broad and unrefined at the time of EO, however. In both sSC and VC, physiological and biochemical evidence indicate considerable synaptic refinement in response to EO, which occurs naturally at the end of the second postnatal week. These studies use anterograde filling of corticocollicular axons in combination with controlled eyelid opening and reclosing paradigms to compare the corticocollicular projections of age-matched eye-opened and eye-sutured littermates. Reconstructions of individual corticocollicular axons in rat pups and statistically sampled arborization patterns across the colliculus at set times before and after controlled eye-lid opening, show that the onset of pattern vision is critical for the establishment of registration between the cortical and collicular maps of visual space. Moreover, if pattern vision is delayed by prolonging eye-lid closure the cortical projection withdraws to single axon cylinders. A latent plasticity remains, however; the corticocollicular axons can reestablish topologically appropriate arborization if eye opening occurs within at least a week of its normal occurrence.