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 V1.

Responses of human visual cortex to uniform surfaces

“…The perceived brightness of a surface depends not only on surface luminance but also on the luminance distribution in the surrounding visual field (26, ʈ). It has already been demonstrated in cats and monkeys that single neurons in primary visual cortex exhibit a surround modulation that matches contextual effects in human brightness perception (6,9,27,28). By establishing the dynamics of surface-related responses in early visual cortex, our findings therefore provide the fundamental information necessary for the interpretation of future neuroimaging studies of contextual effects in human subjects.…”

“…Theoretical accounts of surface perception have therefore often postulated a processing of ''filling in'' that mediates creation of surface representations at some level in the visual system (4,5). However, more recent reports suggest that some cells in primary visual cortex do indeed respond to the luminance of uniform surfaces (6)(7)(8)(9)(10). Furthermore, in humans there is a close relationship between perceived brightness contrast and responses in primary visual cortex (11)(12)(13)(14)(15), suggesting that other sensations of brightness may also be encoded in primary visual cortex.…”

Perceived luminance depends on temporal context

“…The activity of these brightness-responsive neurons adapts with time: the firing rates peak after 100 ms and then drop off precipitously14. This decrease in firing is consistent with an adapting population, although in some circumstances the later part of the spike train may correspond to the response of a non-adapting population 14 . This raises the possibility that the two encodings could be multiplexed into the same population of cells in V1.…”

Neuromagnetic Correlates of Perceived Brightness in Human Visual Cortex

“…We found that the MEG response was better accounted for by log-scaled luminance (Table 1, middle) than was the physical luminance of the stimulus (Table 1, left). Some electrophysiological studies with non-human primates reported that the electrical activity of neurons in the primary visual cortex depends linearly on the logarithm of luminance (Kayama et al, 1979;Kinoshita & Komatsu, 2001). There are also a few fMRI and EEG studies of humans, which suggest that the activation intensity in the primary visual cortex is linearly dependent on the logarithm of luminance contrast (Avidan, Harel, Hendler, Ben-Bashat, Zohary, & Malach, 2002;Boynton, Demb, Glover, & Heeger, 1999;Goodyear & Menon, 1998;Souza, Gomes, Saito, Filho, & Silveira, 2007).…”

“…A few electrophysiological studies with non-human primates have reported that individual Correspondence concerning this article should be addressed to Aki Kondo, Research Center for Advanced Science and Technology, The University of Tokyo, 4-6-1, Komaba, Meguro-ku, Tokyo, 1538904, Japan, (email: kondo@fennel.rcast.u-tokyo.ac.jp). neurons exhibit a compressive dependency of discharge rate on luminance, and that neural activity depends linearly on the logarithm of luminance in the primary visual cortex (Kayama, Riso, Bartlett, & Doty, 1979;Kinoshita & Komatsu, 2001).…”