Assembly of Receptive Fields in Cat Visual Cortex

The origin of orientation selectivity in the responses of simple cells in cat visual cortex serves as a model problem for understanding cortical circuitry and computation. The feedforward model of Hubel and Wiesel [1] posits that this selectivity arises simply from the spatial organization of the receptive fields of thalamic inputs synapsing on each simple cell. Much evidence, including a number of recent intracellular studies, supports a primary role of the thalamic inputs in determining simple-cell response properties including orientation tuning. And yet, while the feedforward model seems to explain the broad outline of simple-cell properties, there are number of detailed aspects of the behavior of simple cells that have appeared not to be accounted for by the feedforward model. These properties include contrast invariance of orientation tuning, the exact relationship between receptive field geometry and orientation tuning, and the dynamics of orientation tuning. The apparent failures of the feedforward model have prompted the development of a class of models that rely on feedback circuitry within the cortex: Properly arranged feedback from excitatory connections within an orientation column and inhibitory connections to adjacent columns can account for many of the properties that the feedforward models miss. The feedforward and feedback models are different enough in character that they make radically different predictions about the nature of the computation performed by the cortex, the feedforward models acting more like passive filters, and the feedback models more actively shaping the representation of the retinal image. I will review a series of experiments designed to test these two models, and present evidence that the feedforward models, with little modification, can account in detail for the behavior of cortical simple cells.