Building surfaces from borders in Areas 17 and 18 of the cat

Abstract

Several brightness illusions indicate that borders can dramatically affect the perception of adjoining surfaces. In the Craik-O'Brien-Cornsweet illusion, in particular, two equiluminant surfaces can appear different in brightness due to the contrast border between them. Although the psychophysical nature of this phenomenon has been well characterized, the neural circuitry underlying this effect is unexplored. Here, we have asked whether there are cells in visual cortex which respond to edge-induced illusory brightness percepts such as the Cornsweet. Using optical imaging and single unit recordings methods, we have studied responses of the primary (Area 17) and second (Area 18) visual cortical areas of the anesthetized cat to both real luminance change and Cornsweet brightness change. We find that there are indeed cells whose responses are modulated in phase with the modulation of the Cornsweet stimulus. These cells are present in both Area 17 and Area 18, but are more prevalent in Area 18. These responses are generally weak and are found even when receptive fields are distant from the contrast border. Consistent with perception, cells which respond to the Cornsweet border are modulated in antiphase to the Narrow Real (another border-induced illusory brightness stimulus). Remarkably, we also find evidence of edge-induced responses to illusory brightness change using intrinsic signal optical imaging. Both real luminance change and edge-induced brightness change produces a greater imaged response in Area 18 than in Area 17. Thus, in the absence of direct luminance stimulation, cells in visual cortex can respond to modulation of distant border contrasts. We suggest that the perception of surface brightness was encoded in the early visual cortical pathway by both surface luminance contrast signals in Area 17 (Rossi, A. F., Rittenhouse, C. D., & Paradiso, M. A. (1996). The representation of brightness in primary visual cortex. Science, 273, 1104-7) and border-induced contrast signals that predominate in Area 18.

No Functional Magnetic Resonance Imaging Evidence for Brightness and Color Filling-In In Early Human Visual Cortex

“…Neurophysiological studies in monkey suggest that a subpopulation of V1 and V2 neurons respond to luminance modulations well outside their classical receptive field (Kinoshita and Komatsu, 2001;Roe et al, 2005), in a manner qualitatively consistent with brightness perception. Similar results have been reported in cats (Rossi et al, 1996;Rossi and Paradiso, 1999;Hung et al, 2001). Friedman et al (2003), however, found no evidence for color filling-in signals in V1 and V2 of awake behaving monkeys.…”

“…Recent modeling work suggests that the majority of V1 responses reported by Kinoshita and Komatsu (2001) can be understood on the basis of local and mean luminance processing and that only a small minority of responses are consistent with edge-driven surface activity, such as brightness filling-in (Vladusich et al, 2006). We speculate that the properties of these previously determined surface-responsive neurons (Rossi et al, 1996;MacEvoy et al, 1998;Rossi and Paradiso, 1999;Hung et al, 2001;Kinoshita and Komatsu, 2001;Roe et al, 2005) may in fact arise from the mechanisms underlying the extended edge responses we observed in our study, and so are presumably not directly related to our perception of brightness, color, or filling-in.…”

“…Neurophysiological studies of monkey and cat visual cortex provide some support for the filling-in hypothesis. A small proportion of neurons, responding to the interiors of achromatic surfaces, exhibit properties consistent with aspects of human brightness constancy (MacEvoy and Paradiso, 2001), brightness induction (Rossi et al, 1996;Rossi and Paradiso, 1999;Kinoshita and Komatsu, 2001;Peng and Van Essen, 2005), the Craik-Cornsweet-O'Brian brightness illusion (Hung et al, 2001; Roe et al, 2005), and surface completion of the retinal blind spot (Komatsu et al, 2000(Komatsu et al, , 2002. No neurophysiological study, however, has yet revealed evidence of a topographic cortical representation corresponding to uniform surface regions von der Heydt et al, 2003).…”

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.…”

Cortical processing of a brightness illusion

“…How the brain encodes such local and global brightness cues is unknown. Only a few studies have examined neuronal response to uniform surfaces (4)(5)(6)(7)(8)(9). These studies have shown that although cells modulated by luminance change are found as early as the retina and lateral geniculate nucleus (LGN), those modulated by perceived brightness change, which occur independent of actual luminance change over the receptive field (RF), can be found as early as the primary visual cortex (V1).…”