| Abstract: | Illusory figures demonstrate the visual system’s ability to infer surfaces under conditions of fragmented sensory input. To investigate the role of midlevel visual area V4 in visual surface completion, we used multielectrode arrays to measure spiking responses to two types of visual stimuli: Kanizsa patterns that induce the perception of an illusory surface and physically similar control stimuli that do not. Neurons in V4 exhibited stronger and sometimes rhythmic spiking responses for the illusion-promoting configurations compared with controls. Moreover, this elevated response depended on the precise alignment of the neuron’s peak visual field sensitivity (receptive field focus) with the illusory surface itself. Neurons whose receptive field focus was over adjacent inducing elements, less than 1.5° away, did not show response enhancement to the illusion. Neither receptive field sizes nor fixational eye movements could account for this effect, which was present in both single-unit signals and multiunit activity. These results suggest that the active perceptual completion of surfaces and shapes, which is a fundamental problem in natural visual experience, draws upon the selective enhancement of activity within a distinct subpopulation of neurons in cortical area V4.Visual illusions are valuable stimuli for studying the neural basis of visual processing because they reveal the brain’s internal mechanisms for interpreting sensory input. Illusory figures, for example, exploit the visual system’s capacity to construct contours, shapes, and surfaces despite the lack of a continuous physical border (1, 2). Illusory figures are perceived by a range of phylogenetically diverse species, including monkeys, cats, owls, and bees, pointing to perceptual completion as a fundamental aspect of natural vision (3).Neural correlates of illusory figures have been found in a wide range of brain areas. Recordings in monkeys revealed that illusory figures evoke spiking responses from neurons in visual areas as early as V1 and V2 and as late as the inferotemporal cortex (4–9). Neuroimaging studies in humans similarly found responses to illusory figures throughout visual cortex (10–13).Several theoretical models postulate mechanisms of illusory figure perception (14–19). A common feature of these models is spatial integration of the inducing elements combined with an active interpolation to complete the surface. These processes are frequently assigned to neurons in midlevel areas, whose receptive fields are large enough to cover separate elements yet sensitive enough to distinguish between local features such as orientation, curvature, and colinearity (20, 21). A range of evidence suggests that visual area V4 in particular may play an active role in surface completion. First, the receptive fields of V4 neurons are large by comparison with V1 and V2 receptive fields and are therefore able to integrate information across spatially separated stimulus components (22). Second, psychophysical studies demonstrate that the perception of certain similar illusory figures varies over visual space in a manner consistent with the retinotopy of V4 (23, 24). Third, both human (10–13) and nonhuman primate (25) functional imaging studies reveal responses to illusory contours and surfaces in area V4. Fourth, ablation of area V4 in the macaque selectively impairs performance on discrimination tasks that involve illusory contours (26).Here we investigate the neural representation of illusory surfaces in macaque area V4 using Kanizsa patterns known to give rise to the perception of illusory surfaces. Illusion-promoting patterns elicited electrophysiological responses that were often rhythmic and were significantly enhanced in their firing rate compared with physically similar control patterns that did not promote the illusion. This enhancement depended critically on the spatial alignment of the illusory surface with the point of peak V4 receptive field sensitivity, or “RF focus.” Only neurons with receptive fields focused on the illusory surface showed elevated responses to the illusory surface, whereas those with receptive fields focused on the inducing elements did not. This effect was observed for neurons whose receptive fields, as defined by conventional mapping techniques, were several degrees in size and overlapped with both the illusory surface and the inducer elements. These observations suggest that V4 neurons play an active role in the representation of illusory surfaces and are sensitive to stimulus details much finer than would be predicted based on receptive field size alone. |
