Development of radial frequency pattern perception in macaque monkeys.

Infant primates see poorly, and most perceptual functions mature steadily beyond early infancy. Behavioral studies on human and macaque infants show that global form perception, as measured by the ability to integrate contour information into a coherent percept, improves dramatically throughout the first several years after birth. However, it is unknown when sensitivity to curvature and shape emerges in early life or how it develops. We studied the development of shape sensitivity in 18 macaques, aged 2 months to 10 years. Using radial frequency stimuli, circular targets whose radii are modulated sinusoidally, we tested monkeys' ability to radial frequency stimuli from circles as a function of the depth and frequency of sinusoidal modulation. We implemented a new four-choice oddity task and compared the resulting data with that from a traditional two-alternative forced choice task. We found that radial frequency pattern perception was measurable at the youngest age tested (2 months). Behavioral performance at all radial frequencies improved with age. Performance was better for higher radial frequencies, suggesting the developing visual system prioritizes processing of fine visual details that are ecologically relevant. By using two complementary methods, we were able to capture a comprehensive developmental trajectory for shape perception.

Developmentally stable representations of naturalistic image structure in macaque visual cortex.

We studied visual development in macaque monkeys using texture stimuli, matched in local spectral content but varying in "naturalistic" structure. In adult monkeys, naturalistic textures preferentially drive neurons in areas V2 and V4, but not V1. We paired behavioral measurements of naturalness sensitivity with separately-obtained neuronal population recordings from neurons in areas V1, V2, V4, and inferotemporal cortex (IT). We made behavioral measurements from 16 weeks of age and physiological measurements as early as 20 weeks, and continued through 56 weeks. Behavioral sensitivity reached half of maximum at roughly 25 weeks of age. Neural sensitivities remained stable from the earliest ages tested. As in adults, neural sensitivity to naturalistic structure increased from V1 to V2 to V4. While sensitivities in V2 and IT were similar, the dimensionality of the IT representation was more similar to V4's than to V2's.

Shape encoding consistency across colors in primate V4.

Neurons in primate cortical area V4 are sensitive to the form and color of visual stimuli. To determine whether form selectivity remains consistent across colors, we studied the responses of single V4 neurons in awake monkeys to a set of two-dimensional shapes presented in two different colors. For each neuron, we chose two colors that were visually distinct and that evoked reliable and different responses. Across neurons, the correlation coefficient between responses in the two colors ranged from -0.03 to 0.93 (median 0.54). Neurons with highly consistent shape responses, i.e., high correlation coefficients, showed greater dispersion in their responses to the different shapes, i.e., greater shape selectivity, and also tended to have less eccentric receptive field locations; among shape-selective neurons, shape consistency ranged from 0.16 to 0.93 (median 0.63). Consistency of shape responses was independent of the physical difference between the stimulus colors used and the strength of neuronal color tuning. Finally, we found that our measurement of shape response consistency was strongly influenced by the number of stimulus repeats: consistency estimates based on fewer than 10 repeats were substantially underestimated. In conclusion, our results suggest that neurons that are likely to contribute to shape perception and discrimination exhibit shape responses that are largely consistent across colors, facilitating the use of simpler algorithms for decoding shape information from V4 neuronal populations.

Equiluminance cells in visual cortical area v4.

We report a novel class of V4 neuron in the macaque monkey that responds selectively to equiluminant colored form. These "equiluminance" cells stand apart because they violate the well established trend throughout the visual system that responses are minimal at low luminance contrast and grow and saturate as contrast increases. Equiluminance cells, which compose ∼22% of V4, exhibit the opposite behavior: responses are greatest near zero contrast and decrease as contrast increases. While equiluminance cells respond preferentially to equiluminant colored stimuli, strong hue tuning is not their distinguishing feature-some equiluminance cells do exhibit strong unimodal hue tuning, but many show little or no tuning for hue. We find that equiluminance cells are color and shape selective to a degree comparable with other classes of V4 cells with more conventional contrast response functions. Those more conventional cells respond equally well to achromatic luminance and equiluminant color stimuli, analogous to color luminance cells described in V1. The existence of equiluminance cells, which have not been reported in V1 or V2, suggests that chromatically defined boundaries and shapes are given special status in V4 and raises the possibility that form at equiluminance and form at higher contrasts are processed in separate channels in V4.

Partial occlusion modulates contour-based shape encoding in primate area V4.

Past studies of shape coding in visual cortical area V4 have demonstrated that neurons can accurately represent isolated shapes in terms of their component contour features. However, rich natural scenes contain many partially occluded objects, which have "accidental" contours at the junction between the occluded and occluding objects. These contours do not represent the true shape of the occluded object and are known to be perceptually discounted. To discover whether V4 neurons differentially encode accidental contours, we studied the responses of single neurons in fixating monkeys to complex shapes and contextual stimuli presented either in isolation or adjoining each other to provide a percept of partial occlusion. Responses to preferred contours were suppressed when the adjoining context rendered those contours accidental. The observed suppression was reversed when the partial occlusion percept was compromised by introducing a small gap between the component stimuli. Control experiments demonstrated that these results likely depend on contour geometry at T-junctions and cannot be attributed to mechanisms based solely on local color/luminance contrast, spatial proximity of stimuli, or the spatial frequency content of images. Our findings provide novel insights into how occluded objects, which are fundamental to complex visual scenes, are encoded in area V4. They also raise the possibility that the weakened encoding of accidental contours at the junction between objects could mark the first step of image segmentation along the ventral visual pathway.