Functional organization of lateral geniculate nucleus and primary visual cortex of the gray squirrel, Sciurus carolinensis

Over the last 50 years, studies of receptive field properties in mammalian visual brain structures such as lateral geniculate nucleus (LGN) and primary visual cortex (V1) have identified classes of cells with unique functional response properties, and in visual cortex of many mammals these response properties show considerable spatial organization termed functional architecture. Recently, there has been interest in understanding the cellular mechanisms that underlie these visual responses and their functional architecture. Rodents offer many advantages for such studies, as they are appropriate for a wide variety of experimental techniques. Squirrels are highly visual diurnal rodents that may be excellent model preparations for understanding mechanisms of function and disease in the human visual system. In an effort to uncover organizing principles of the early visual system and to understand the relationship between the visual systems of rodents and other mammals, my colleagues and I have examined functional response properties and functional organization in the early visual system of the gray squirrel. In the LGN, our data are consistent with the idea that all mammals have a class of LGN neurons that is sustained, another class that is transient, and a third class of more heterogeneous cells, but some response properties such as linearity of spatial summation, contrast gain, and dependence of receptive field size on eccentricity vary from species to species. In squirrel V1, individual neurons show orientation selectivity as they do in other mammals, but squirrels lack smooth, repeating maps of orientation-selective cells that are found in primates, carnivores, and tree shrews. These differences cannot be explained by differences in visual acuity or V1 size. We suggest that orientation maps are not necessary for high acuity vision or orientation selectivity and that cortical functional architecture can vary greatly from species to species. Studies of horizontal interactions suggest that local horizontal connections are made among cells that are nearby rather than among cells that have similar orientation preferences. Finally, we do not find evidence for patchy horizontal connections in squirrel V1, suggesting that the existence of patchy horizontal connections and orientation maps may be functionally linked.