Responses of human visual cortex to uniform surfaces

Abstract

Surface perception is fundamental to human vision, yet most studies of visual cortex have focused on the processing of borders. We therefore investigated the responses of human visual cortex to parametric changes in the luminance of uniform surfaces by using functional MRI. Early visual areas V1 and V2͞V3 showed strong and reliable increases in signal for both increments and decrements in surface luminance. Responses were significantly larger for decrements than for increments, which was fully accounted for by differences in retinal illumination arising from asymmetric pupil dynamics. Responses to both sustained and transient changes of illumination were transient. Signals in early visual cortex scaled linearly with the magnitude of change in retinal illumination, as did subjects' subjective ratings of the perceived brightness of the stimuli. Our findings show that early visual cortex responds strongly to surfaces and that perception of surface brightness is compatible with brain responses at the earliest cortical stages of processing.T he perception of surfaces is fundamental to visual behavior, yet little is known about how they are processed in visual cortex. Early studies suggested that neurons in visual cortex respond strongly to edges but only weakly or not at all to uniform illumination (1). Subsequent work has therefore focused almost exclusively on neural mechanisms of contour processing. Indeed, in most contemporary computational models, visual cortical cells are characterized as filters that are unresponsive to uniform illumination (2, 3). The presence of strong edge responses and weak surface responses in early visual cortex is contrary to the intuition that perception of surface brightness should be mediated by neurons responding strongly to the entire spatial extent of a surface. 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 (6-10). 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. However, the cortical response function for surfaces of uniform luminance in early visual areas, and its relationship to perceived brightness, has remained uninvestigated.We therefore sought to address this question by using functional MRI (fMRI) to characterize the relationship between parametric variations in surface luminance, cortical responses, and perceived brightness. Understanding such a relationship is a prerequisite for a complete understanding of the general mechanisms and principles that underlie perception of brightness.When studying responses to uniform surfaces, it is critical to avoid contamination by contour-related processes. With ...

The primary visual cortex fills in color

“…These results are not in accord with the previous studies, which indicated activation in areas including V2, V3͞VP, V3A, and V4v (39)(40)(41)(42)(43). Why does this discrepancy occur?…”

“…The spatially global nature of the activity for the filling-in only in V1 suggests that long-range horizontal connections in V1 (53), which previously have been found only with contour signals and edges (53), may occur even with non-contour-based feature signals such as colors and brightness. The result of the activity with the uniform disk stimulus in experiment 3 is basically the same as that with color filled-in transparency in experiment 1 and also is in accord with the recent finding that V1 activity in response to a uniform surface is the highest in early visual areas (43). These results suggest that long-range horizontal connections are involved in both the color filling-in processing and uniform surface processing.…”

Identifying natural images from human brain activity

“…Stanley and co-workers 26 reconstructed natural movies by modeling the luminance of individual image pixels as a linear function of single-unit activity in cat LGN. This approach assumes a linear relationship between luminance and the activity of the recorded units, but this condition does not hold in fMRI 27,28 .…”

Neuromagnetic Correlates of Perceived Brightness in Human Visual Cortex

“…An fMRI study by Goodyear & Menon (1998) reported that cortical activity in the primary visual cortex increased in the volume of regional activation, as well as activation intensity, as the luminance intensity increased. Furthermore, they reported a close relationship between perceived brightness contrast and responses in the primary visual cortex (e.g., Haynes, Lotto, & Rees, 2004;Osaka & Yamamoto, 1978;Wicke, Donchin, & Lindsley, 1964). Wicke et al (1964) showed that VEP peak latency varies with stimulus luminance and higher luminance yields faster latency.…”

“…Wicke et al (1964) showed that VEP peak latency varies with stimulus luminance and higher luminance yields faster latency. An fMRI study by Haynes, et al (2004) showed that the blood oxygenation level-dependent (BOLD) signals in the early visual cortex scaled linearly with the magnitude of change in retinal illumination, simultaneously correlating with subjective ratings of perceived brightness. These results indicate that perceived brightness may be encoded in the primary visual cortex.…”