Functional cell classes and functional architecture in the early visual system of a highly visual rodent.

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 suggested the existence of cell classes with unique functional response properties, and in visual cortex of many mammals these functional response properties show considerable spatial organization termed functional architecture. In recent years, there has been considerable interest in understanding the cellular mechanisms that underlie visual responses and plasticity in intact animals, and studies of individual neurons in brain slices have identified distinct cell classes on the basis of anatomical features, synaptic connectivity, or gene expression. However, the relationships between cell classes identified in studies of brain slices and those in the intact animal remain largely unclear. Rodents offer many advantages for investigating these relationships, as they are appropriate for a wide variety of experimental techniques and genetically modified mice are relatively easy to obtain or produce. Unfortunately, a barrier to using these animals in vision research is a lack of understanding of the relationship of rodent visual systems to the visual systems in more commonly studied mammals such as carnivores and non-human primates. Here we review recent comparative studies of functional response properties in LGN and V1 of a highly visual diurnal rodent, 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 V1, the squirrel has many orientation-selective neurons, and these orientation-selective cells can be further subdivided into simple and complex cells. Despite the fact that squirrel has greater visual acuity and a physically larger V1 than some mammals that have orientation maps in V1, we do not find orientation maps in V1 of squirrel, which is similar to results in other less visual rodents. 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.