Receptive field focus of visual area V4 neurons determines responses to illusory surfaces

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 perception | illusory contours | modal completion | nonhuman primate | visual cortex V isual 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 ...

A recurrent neural model for proto-object based contour integration and figure-ground segregation

“…The receptive fields of these neurons are similar to those proposed by Craft et al (2007). Other types of grouping neurons may also exist, including those that respond to gratings (Hegdé and Van Essen, 2007), illusory surfaces (Cox et al, 2013), or 3D surfaces (He and Nakayama, 1995; Hu et al, 2015). We do not attempt to model the whole array of grouping neurons that may exist, but only those necessary for reproducing the neurophysiological experiments referred to here.…”

Acuity-independent effects of visual deprivation on human visual cortex

“…We then measure evoked responses at early latencies before the time that IC selectivity arises to assess the integrity of early visual cortex, and compare these responses to those measured at longer latencies after robust IC selectivity has been established. Previous single-unit studies that have used ICs of the type used in the present study indicate that they are first extracted no later than V2 (31,42,43) or V4 (34). Given the difference in species and stimuli, we will refer in the following to evoked responses that lack IC sensitivity as having arisen in "early" visual cortex, rather than in specific visual areas.…”

“…Our approach is similar in spirit to existing psychophysical approaches: We use a stimulus configuration-illusory contours (ICs)-that previous single-unit studies have shown to be first extracted in extrastriate cortex (31)(32)(33)(34). ICs, also referred to as subjective contours, render object borders that are perceptually vivid but that are created in the absence of luminance contrast or chrominance gradients (35).…”

Representation of illusory and physical rotations in human MST: A cortical site for the pinna illusion

“…The answer to this question is not immediately known. However, in other illusion studies of single‐cell recordings in macaque V2 and V4, it has been reported that some cortical neurons respond even more strongly to illusory contour stimuli than to physical control stimuli [Cox et al, ; Pan et al, ; von der Heydt and Peterhans, ; von der Heydt et al, ]. We therefore compared response intensities elicited by the illusory and physical rotation stimuli in terms of the percentage of changes in BOLD signals.…”