Functional organization of envelope-responsive neurons in early visual cortex: organization of carrier tuning...

It is well established that visual cortex neurons having similar selectivity for orientation, direction of motion, ocular dominance, and other properties of first-order (luminance-defined) stimuli are clustered into a columnar organization. However, the cortical architecture of neuronal responses to second-order (contrast/texture-defined) stimuli is poorly understood. A useful second-order stimulus is a contrast envelope, consisting of a finely detailed pattern (carrier) whose contrast varies on a coarse spatial scale (envelope). In this study, we analyzed the cortical organization of carrier tuning properties of neurons, which responded to contrast-modulated stimuli. We examined whether neurons tuned to similar carrier properties are clustered spatially and whether such spatial clusters are arranged in columns. To address these questions, we recorded single-unit activity, multiunit activity, and local field potentials simultaneously from area 18 of anesthetized cats, using single-channel microelectrodes and multielectrode arrays. Our data showed that neurons tuned to similar carrier spatial frequency are distributed in a highly clustered manner; neurons tuned to similar carrier orientation are also significantly clustered. Neurons along linear arrays perpendicular to the brain surface always exhibited similar optimal carrier spatial frequency, indicating a columnar organization. Multi-pronged tetrode recordings indicated that the diameter of these columns is ≥450 μm. Optimal carrier orientation was also significantly clustered but with finer-grain organization and greater scatter. These results indicate a fine anatomical structure of cortical organization of second-order information processing and suggest that there are probably more maps in cat area 18 than previously believed.