The role of V1 in the processing of surface lightness is a subject of ongoing debate. The evidence for the role of early cortical processing comes from two main sources: animal single-cell physiology and human fMRI studies. Rossi et al. (
1996), using extracellular recordings from individual cells in cat primary visual cortex, found that a significant percentage of the neurons correlated with perceived lightness rather than with the light level in the receptive field. This finding was further confirmed by Rossi and Paradiso (
1999) and by MacEvoy and Paradiso (
2001). In addition, in areas 17 and 18 of cat visual cortex, Hung et al. (
2007) have demonstrated the similarity between border-to-surface interactions of neurons responding to changes in real luminance and to changes in lightness. In monkeys, Roe et al. (
2005) did not find a correlation with lightness perception earlier than in thin stripes of V2. All of the above studies, however, were done with anesthetized animals, which could have affected the outcome. Using recordings from V1 neurons in awake-behaving monkeys, Kinoshita and Komatsu (
2001) found that the activity in a relatively large group of neurons correlates with lightness perception rather than luminance. These studies raise the possibility that the neural mechanisms underlying lightness perception can be operating at the earliest stages of cortical visual processing, in V1 or V2.
There is, however, little agreement between the findings of different human fMRI studies. Using a Craik-O'Brien-Cornsweet brightness illusion, Boyaci et al. (
2007) observed an increase in neural activity in areas V1–V3, correlating with lightness perception. However, another study (Perna et al.,
2005), using the same illusion in a different spatial configuration, showed an increase in neural activity in higher order visual areas, including the caudal region of intrapariatal sulcus and lateral occipital sulcus, but no increase in activity in areas V1–V4. Conversely, Boucard et al. (
2005) showed activation in early retinotopic cortical areas in response to induced illusory lightness modulation in a circular test field of constant luminance. The lightness modulation in that experiment was obtained by varying the luminance of the surrounding area at a rate of 1 Hz. However, in a later study (Cornelissen et al.,
2006), after the luminance contrast effects from the border of the test field were carefully taken into account, the increase in neural activity in V1, V2, and V3 was no longer observed. This study raises the possibility that some of the previous findings of neural activity correlated with lightness perception in early retinotopic visual areas were caused by a distant luminance border artifact rather than perceived lightness change.
We addressed this problem by juxtaposing the predictions of the border luminance contrast account and the lightness perception account and showed that the fMRI signal in V1 correlates with lightness perception rather than just physical luminance contrast at the border. The highest fMRI activity was observed in the ROIs corresponding to the static test disk when the luminance of the disk was equal to time-average luminance of the surround (and thus the border luminance contrast was minimal). By parametrically adjusting the luminance of the test disk, we observed a close relationship between the fMRI signal and the amount of perceived lightness induction.
Our findings are, in part, consistent with the results of Cornelissen et al.'s (
2006) study in that the strongest fMRI signal for each disk luminance level was at the border, rather than in the center of the disk. Cornelissen et al. (
2006) used this result to substantiate their argument that fMRI signal in the ROIs corresponding to the disk reflects the neural activity caused by physical contrast at the border. However, they overlooked the possibility that perceptual lightness induction also increases at the border, which could lead to an increase in fMRI signal.
Interestingly, both our behavioral and fMRI data showed spatial non-uniformity. The behavioral results showed that the perception of lightness induction is strongest near the border and weakest in the center of the disk. This finding is consistent with that of Cornsweet (
1970) and Davidson (
1968), who have reported similar perceived spatial non-uniformities in
static setups. The fMRI signal was also the highest at the border and smallest in the center. This observation further supports the idea that activity in V1 correlates with lightness perception. However, our results do not completely exclude the possibility that the decrease in fMRI signal toward the center reflects, at least in part, the spread of neural activity caused by luminance contrast at the border (Cornellissen et al.,
2006). The spatial non-uniformity that we observed is unlikely to be task specific. Since subjects were asked to maintain fixation in the behavioral experiment, the difference in nulling amplitudes across disk position could potentially be explained by different temporal sensitivities at different eccentricities. We have addressed this issue in a separate behavioral study (Pereverzeva and Murray, in preparation) and found that changing the location of fixation does not affect the nulling amplitude in the patches. These findings lend further support to the non-uniformity of lightness induction perception. It also should be noted that most subjects reported that during the free viewing, the perceived induced flicker in the static disk was stronger near the border than at the center.
We were surprised to find elevated fMRI signal in the ROIs corresponding to the center and the middle regions of the disk at 50% IL in the real flicker condition. These results, however, may be explained by the fact that our study did not attempt to disambiguate the border contrast and absolute luminance of the disk. There is some evidence that, independently of contrast, luminance can affect the firing rate of neurons in primary visual cortex. A recent single-unit study of cat primary visual cortex showed that for many neurons, there is a contrast/luminance trade-off in the firing rate (Geisler, Albrecht, & Crane,
2007). The neurons described in this study could achieve the same firing rate when exposed to the stimuli of lower contrast and higher overall luminance as when exposed to stimuli of higher contrast but lower luminance. The trade-off was nonlinear, so a group of similarly behaved neurons could be more active at higher luminance even though the contrast has decreased. If these findings extend to neurons in human visual cortex, they may be responsible for the elevated fMRI signal at higher luminance in the real flicker condition.
In summary, we have demonstrated that neural activity in V1 correlates with lightness perception. However, it is important to emphasize that in order to arrive at an estimate of surface reflectance the visual system uses multiple cues, such as the range of luminances present in the image (Brainard & Maloney,
2004; Webster & Mollon,
1995), as well as 3-dimensional interpretations of the scene, illuminant cues, object cues, and shadows (Adelson,
1993; Gilchrist,
1977; Knill & Kersten,
1991; Lotto, Williams, & Purves,
1999). Further research is needed to examine how these other cues contribute to the neural processing of lightness information.