Neural sensitivity to radial frequency patterns in the visual cortex of developing macaques

Abstract

Visual resolution, contrast sensitivity and form perception improve gradually with age. In nonhuman primates, the sensitivity and resolution of cells in the retina, lateral geniculate nucleus and primary visual cortex (V1) also improve, but not enough to account for the perceptual changes. So, what aspects of visual system development limit visual sensitivity in infants? Improvements in behavioral sensitivity might arise from maturation of regions downstream of V1 such as V2, V4 and pIT, which are thought to support increasingly complex perceptual abilities. We recorded the responses of populations of neurons in areas V1, V2, V4, and pIT to radial frequency patterns - a type of global form stimulus. Subjects were three young monkeys between the ages of 19 and 54 weeks, and a single adult animal. We found that neurons and neural populations in V4 reliably encoded global form in radial frequency stimuli at the earliest ages we studied, while V1 neurons do not. V2 and pIT populations also showed some degree of selectivity for these patterns at early ages, especially at higher radial frequency values. We did not find significant, systematic changes in neural decoding performance that could account for the improvement in behavioral performance over the same age range in an overlapping group of animals (Rodriguez Deliz et al., 2024). Finally, consistent with our prior behavioral results, neural populations in V4 show highest sensitivity for the higher radial frequency values which contain the highest concentration of curvature and orientation cues. SIGNIFICANCE STATEMENTInfants have remarkably limited ability to discriminate shapes. These limitations cannot be fully explained by postnatal changes in their eyes, visual thalamus, or primary visual cortex. The perception of shape requires integration of local cues across space to create global form information. We therefore examined populations of neurons in extrastriate visual cortex to learn whether information represented in these regions might limit infants abilities to process global forms. We found instead that extrastriate areas involved in global form processing function maturely early in life, by the age of 4-6 months, suggesting that infants perceptual limits are set by other aspects of brain development.