Neural representation of the luminance and brightness of a uniform surface in the macaque primary visual cortex

Abstract

The perceived brightness of a surface is determined not only by the luminance of the surface (local information), but also by the luminance of its surround (global information). To better understand the neural representation of surface brightness, we investigated the effects of local and global luminance on the activity of neurons in the primary visual cortex (V1) of awake macaque monkeys. Single- and multiple-unit recordings were made from V1 while the monkeys were performing a visual fixation task. The classical receptive field of each neuron was identified as a region responding to a spot stimulus. Neural responses were assessed using homogeneous surfaces at least three times as large as the receptive field as stimuli. We first examined the sensitivity of neurons to variation in local surface luminance, while the luminance of the surround was held constant. The activity of a large majority of surface-responsive neurons (106/115) varied monotonically with changes in surface luminance; in some the dynamic range was over 3 log units. This monotonic relation between surface luminance and neural activity was more evident later in the stimulus period than early on. The effect of the global luminance on neural activity was then assessed in 81 of the surface-responsive neurons by varying the luminance of the surround while holding the luminance of the surface constant. The activity of one group of neurons (25/81) was unaffected by the luminance of the surround; these neurons appear to encode the physical luminance of a surface covering the receptive field. The responses of the other neurons were affected by the luminance of the surround. The effects of the luminances of the surface and the surround on the activities of 26 of these neurons were in the same direction (either increased or decreased), while the effects on the remaining 25 neurons were in opposite directions. The activities of the latter group of neurons seemed to parallel the perceived brightness of the surface, whereas the former seemed to encode the level of illumination. There were differences across different types of neurons with regard to the layer distribution. These findings indicate that global luminance information significantly modulates the activity of surface-responsive V1 neurons and that not only physical luminance, but also perceived brightness, of a homogeneous surface is represented in VI.