Distinct Mechanisms for Size Tuning in Primate Visual Cortex

Most neurons in primary visual cortex (V1) are selective for stimulus size, a property with important implications for salient feature detection. Size selectivity involves dynamic interactions between neuronal circuits that establish the classical (center) and extraclassical (surround) of a neuron's receptive field. Although much is known about the tuning properties and stimulus selectivity of the center and surround subunits, relatively little is known about how these subunits interact to achieve size selectivity. To address this question, we examined the temporal dynamics of size selectivity in two classes of pyramidal neurons at similar hierarchical processing stages in V1 of alert monkeys. These two classes were comprised of neurons in cortical layer 6 with identified projections to the lateral geniculate nucleus. While both neuronal groups displayed comparable levels of size selectivity, the temporal dynamics of their tuning differed significantly. We compared the size tuning profiles of each cell type with a series of sum-of-Gaussian models and discovered that the receptive fields of neurons with fast-conducting axons contained an excitatory center and a suppressive surround with similar onset timing. In contrast, neurons with slow-conducting axons used two center components-an early wide-field component and a delayed narrow-field component that increased activity-in addition to the surround component. The early, wide-field component represents a novel mechanism for cortical neurons to integrate contextual information. These results demonstrate that size tuning in cortical neurons is established via multiple unique mechanisms, dictated by the rich circuit architecture in which neurons are embedded.