The connectivity principles underlying the emergence of orientation selectivity in primary visual cortex (V1) of mammals lacking an orientation map (such as rodents and lagomorphs) are poorly understood. We present a computational model in which random connectivity gives rise to orientation selectivity that matches experimental observations. The model predicts that mouse V1 neurons should exhibit intricate receptive fields in the two-dimensional frequency domain, causing a shift in orientation preferences with spatial frequency. We find evidence for these features in mouse V1 using calcium imaging and intracellular whole-cell recordings. Pattadkal et al. show that orientation selectivity can emerge from random connectivity, and offer a distinct perspective for how computations occur in the neocortex. They propose that a random convergence of inputs can provide signals for orientation preference in contrast with the dominant model that requires a precise arrangement.Fil: Pattadkal, Jagruti J.. University of Texas at Austin; Estados UnidosFil: Mato, German. Comisión Nacional de Energía Atómica. Gerencia del Área de Energía Nuclear. Instituto Balseiro; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: van Vreeswijk, Carl. Centre National de la Recherche Scientifique; FranciaFil: Priebe, Nicholas J.. University of Texas at Austin; Estados UnidosFil: Hansel, David. Centre National de la Recherche Scientifique; Franci