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An Expanded Visual Cortex for the Superior Colliculus

Abstract

Studies of cortical visual processing in mammals have traditionally focused on the visual pathway that ascends from the retina to primary visual cortex (V1) via the lateral geniculate nucleus of the thalamus (LGN), known as the geniculate pathway. However, visual information can also reach cortex through an alternate “extrageniculate” visual pathway in which retinal projections to the superior colliculus (SC) are relayed through the pulvinar nucleus of the thalamus (PN; also called the lateral posterior nucleus in rodents) before radiating to various regions of the visual cortex. While this extrageniculate pathway has been extensively characterized in primates and cats, its contribution to visually evoked activity in higher-order visual cortices is generally considered of lesser consequence than that of the geniculate pathway, at least in those higher-order visual cortices studied thus far. In the mouse, however, recent experiments have demonstrated that the SC is actually the principal driver of visually evoked activity in a higher-order visual area called postrhinal cortex (POR). The mouse has about ten other higher cortical visual areas whose visual responses are otherwise considered to largely rely on the retino-geniculo-V1 pathway. In this thesis, I use anatomical and functional approaches to determine the extent to which visual evoked responses across all higher visual areas of the mouse rely on the SC, and in particular on the extrageniculate retino-tecto-pulvinar pathway. I characterize the anatomical distribution of cortical projections from the SC through PN using retrograde, anterograde, and transsynaptic tracing methods, and assess their functional properties using a variety of circuit perturbations in combination with widefield calcium imaging and electrophysiology. This work reveals a lateromedial gradient of SC-dependency across the mouse visual cortex, with several lateral visual areas inheriting most of their visual responses from the SC via PN. We further demonstrate a potential role for this SC-dependent visual cortex in distinguishing self from externally generated visual motion. Together, these lateral cortices constitute a functionally distinct tecto-thalamic visual cortical system operating in parallel with the more medial canonical geniculo-striate system.

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