Retino-Cortical Mapping Ratio Predicts Columnar and Salt-and-Pepper Organization in Mammalian Visual Cortex

Summary: In the mammalian primary visual cortex, neural tuning to stimulus orientation is organized in either columnar or salt-and-pepper patterns across species. For decades, this sharp contrast has spawned fundamental questions about the origin of functional architectures in visual cortex. However, it is unknown whether these patterns reflect disparate developmental mechanisms across mammalian taxa or simply originate from variation of biological parameters under a universal development process. In this work, after the analysis of data from eight mammalian species, we show that cortical organization is predictable by a single factor, the retino-cortical mapping ratio. Groups of species with or without columnar clustering are distinguished by the feedforward sampling ratio, and model simulations with controlled mapping conditions reproduce both types of organization. Prediction from the Nyquist theorem explains this parametric division of the patterns with high accuracy. Our results imply that evolutionary variation of physical parameters may induce development of distinct functional circuitry. : Across mammalian species, orientation tuning in the primary visual cortex is arranged in different manners, such as columnar orientation map in primates or salt-and-pepper organization in rodents. Here, Jang et al. propose that the retina-to-cortex sampling ratio is the key factor in determining the organization of the orientation tuning. Keywords: primary visual cortex, orientation tuning, columnar orientation map, salt-and-pepper organization, retino-cortical sampling, retinal ganglion cell, statistical wiring model, magnification factor, Nyquist frequency, receptive field