Novel visuomotor adaptation paradigm reveals a role of visual cortex in the plasticity of innate behaviors in mice

A long-standing hypothesis in sensory neuroscience suggests that the evolutionary expansion of cortex in mammals may contribute to sensory-dependent adaptation by acting on subcortical pathways that drive innate behavior. However, direct experimental evidence is lacking. Taking the visual system as a model, it is known that there is significant interaction between the evolutionarily conserved Superior Colliculus (SC) and the comparatively modern Visual Cortex (VC), key structures in the mammalian visual system. In the SC, local alignment is established between a retinotopic map of the visual field and a map of orienting movement vectors during development and drives accurate visually guided orienting behavior throughout an organisms lifespan. Interestingly mammals, like humans and non-human primates, readily adapt to altered visual experiences, while evolutionarily older vertebrates, like amphibians, lack this behavioral plasticity. To address this outstanding question, we have developed a novel behavioral paradigm for inducing visuomotor adaptation in freely moving mice that is analogous to paradigms utilized in primates. Our paradigm combines a visually guided orienting task and a novel mouse prism goggle system to shift the visual field. Using this paradigm, we demonstrate for the first time that mice gradually adapt to a chronic shift of their full visual field, suggesting this type of behavioral plasticity is conserved across mammalian species. Furthermore, we show that lesioning primary visual cortex (V1) prior to shifting the visual field disrupts normal visuomotor adaptation, suggesting that VC may play a generative role in the plasticity of fundamental visually guided behaviors. These findings lend support to the hypothesis that a particular evolutionary benefit of sensory cortex is the allowance for experience-dependent behavioral plasticity.