The Extrageniculate Visual Pathway Generates Distinct Response Properties in the Higher Visual Areas of Mice

Visual information conveyed through the extrageniculate visual pathway, which runs from the retina via the superior colliculus (SC) and the lateral posterior nucleus (LPN) of the thalamus to the higher visual cortex, plays a critical role in the visual capabilities of many mammalian species. However, its functional role in the higher visual cortex remains unclear. Here, we observed visual cortical area activity in anesthetized mice to evaluate the role of the extrageniculate pathway on their specialized visual properties. The preferred stimulus velocities of neurons in the higher visual areas (lateromedial [LM], anterolateral [AL], anteromedial [AM], and rostrolateral [RL] areas) were measured using flavoprotein fluorescence imaging and two-photon calcium imaging and were higher than those in the primary visual cortex (V1). Further, the velocity-tuning properties of the higher visual areas were different from each other. The response activities in these areas decreased after V1 ablation; however, the visual properties’ differences were preserved. After SC destruction, these preferences for high velocities disappeared, and their tuning profiles became similar to that of the V1, whereas the tuning profile of the V1 remained relatively normal. Neural tracer experiments revealed that each of these higher visual areas connected with specific subregions of the LPN. The preservation of visual property differences among the higher visual areas following V1 lesions and their loss following SC lesions indicate that pathways from the SC through the thalamus to higher cortical areas are sufficient to support these differences. [Display omitted] •The velocity-tuning properties of mouse visual cortical areas are variable•The differences in the visual properties were preserved after V1 ablation•SC destruction disturbed the properties of the higher visual areas•Each of these higher visual areas is connected with specific LPN subdivisions Tohmi et al. observe visual properties of mouse higher visual areas after lesioning the V1 or superior colliculus (SC) and show that unique properties of the higher visual areas depend on inputs from the SC via distinct subregions of the lateral posterior nucleus of the thalamus.