Early development of direction selectivity in higher visual cortex

Abstract

A fundamental aspect of visual motion processing is the computation of motion direction. In ferrets, as in primates, selectivity for motion direction is found both in early cortical stages like the primary visual cortex (V1) and in higher visual areas like the middle temporal (MT) area in primates and the postero-medial lateral suprasylvian (PMLS) area in ferrets. Little is known about how this critical tuning function develops in higher visual cortex. Here, by studying the development of the ferrets motion pathway, we first reveal the surprising finding that direction selectivity develops earlier in PMLS than in V1, contrary to the areas hierarchical positions. Our data, collected in animals of either sex, furthermore show that while direction selectivity is sensitive to visual experience in both areas, the sensitivity profile differs between them: Presentation of drifting gratings, containing the full complement of spatial and temporal cues generated by visual motion, can promote direction selectivity development in V1 and PMLS. In contrast, flashing stationary stimuli, which lack the spatial displacement of moving stimuli and only contain temporal changes, induce direction selectivity only in PMLS, not V1. Collectively our findings reveal significant deviations in PMLS development from that in V1, which will be important to account for in models of motion pathway development and of the developmental disorders that affect this pathway. The complex pattern of relative PMLS and V1 development also highlights the need to address interactions between areas in developmental research. Significance StatementWhile the development of early stages of visual cortex up to primary visual cortex (V1) has received much attention throughout the years, significantly less is known about that of higher visual cortex both on its own as well as in relationship to V1. Here, we focus on a core motion function, direction selectivity, to systematically characterize the coordinated development of multiple stages of the visual motion pathway in ferrets. Crucially, our data show that this coordinated development is surprising complex, and that the developmental status of the higher areas cannot be predicted based on that in lower areas. These findings may also provide clues why motion vision is particularly vulnerable to developmental disorders.