Postnatal development of the receptive-field organization of the macaque V2 neurons

Visual capacities of primates are limited near birth. Our previous electrophysiological investigations on the neural basis of reduced vision in infant macaque monkeys revealed that contrary to earlier observations, the responses of individual V1 neurons are qualitatively adult-like as early as 6-14 days after birth and well tuned to stimulus orientation, spatial and temporal frequency, size, contrast, and disparity by 4 weeks of age. However, we know very little about the functional maturation of extrastriate visual neurons. In adults, multiple inputs from V1 neurons tuned to various local stimulus features (e.g., orientation) are thought to converge on V2 neurons and as a result, many of these early extrastriate neurons may acquire ‘new’ sensitivities to more complex features of visual scenes. Here we used dynamic dense noise stimuli and a novel reverse correlation analysis (local spectral reverse correlation) to reveal the local sensitivities of V2 neurons to stimulus orientation and spatial frequency within their receptive fields (‘subfields’) in anesthetized 4-, 8- and 16-week-old infant monkeys. As early as 4 weeks of age, the spatial matrix of the subfields having facilitatory profiles exhibited a relatively high degree of homogeneity for the preferred orientation and spatial frequency. However, at this age, a substantially higher percentage of V2 neurons compared to adults exhibited the maximum orientation differences between neighboring subfields that were relatively large (e.g., > 45 degrees). The maximum activation strength (z-max score) of the facilitatory profiles in 4-week-old monkeys was relatively lower than in older infants or adults. As in adults, many units from infants had suppressive profiles regardless of their age. However, the percentage of neurons with suppressive profiles was lower in 4-week-old monkeys than in adults although the maximum activation strength of their suppressive profiles was similar to that in adults. These immaturities mostly disappeared by 8 weeks of age. Our results suggest that the functional connections of V2 neurons exhibit moderate immaturities at 4 weeks of age while an adult-like receptive-field center organization is largely attained by 8 weeks of age.