Refinement and maintenance of receptive field size in primary visual cortex occurs without visual experience in mice

Abstract

A critical step in visual cortical maturation is refinement of receptive field (RF) size, producing higher acuity vision. This was previously studied using species with well-developed vision (e.g., carnivores, primates), in which visual experience was necessary for refinement but not maintenance of RFs in visual cortex. In contrast, in Syrian hamsters, a crepuscular species with low visual acuity, dark rearing had no effect on RF refinement in juveniles, but RFs re-enlarged in adulthood, resulting in reduced acuity. These inter-species differences raise the question of whether the need for visual experience is primarily related to the phylogenetic position of the species or to its ecological niche. Here we report that dark rearing had no effect on development or maintenance of RF properties of visual cortical neurons in nocturnal mice. Mice with lifelong visual deprivation refined and maintained their RF size over time. Furthermore, the development of stimulus direction tuning was unaffected by dark rearing. In contrast, surround suppression, orientation tuning and the sharpness of direction tuning were abnormal in dark reared mice. These and our previous results from hamsters show that species living in an ecological niche with minimal daylight exposure require little to no visual experience to develop and maintain refined RFs. This study is an important step in developing a better understanding of the role of visual experience in the development of visual processing circuitry and suggests that diurnal mammals may be a better model for human visual cortical development than mice. SIGNIFICANCE STATEMENTThe role of visual experience in development and plasticity of receptive fields in visual cortex was initially studied using animals with well-developed visual systems (carnivores, primates). Mice have been used more recently, primarily because of genetic manipulations. Now that gene alteration is possible in other species, whether mice are the best choice for visual development and plasticity studies needs reevaluation. We assayed the role of visual experience in mouse visual cortical development, focusing on receptive field refinement. We report that visual experience is unnecessary for the refinement of receptive fields in visual cortex, suggesting that mice (Mus musculus) may not be the best animal model to demonstrate how visual experience influences the development of visual cortical circuitry in humans.