Abstract
Visual sensitivities improve during early development. This improvement can be seen for a variety of tasks, and is not simply explained by functional changes in area V1, based on measurements of spatial contrast sensitivity. Looking downstream, recent work has demonstrated that adult neurons in cortical areas V2 and V4 are sensitive to the presence of statistics common to natural images - their “naturalness”. Neurons in V1 lack this sensitivity. We wondered whether naturalness sensitivity might provide a mechanism through which we could probe development downstream from area V1. We made longitudinal behavioral and neural measurements from two infant macaque monkeys at the ages of 6 and 12 mo, using texture stimuli parametrically varying in naturalness. We measured behavioral naturalness sensitivity with a visual search task, and paired these measurements with interleaved neural measurements to the same stimuli, using multielectrode “Utah” arrays implanted in areas V1/V2 and V4. Behaviorally, we found a robust increase in naturalness sensitivity across the ages tested. Physiologically, neural sensitivity to texture naturalness was consistent across age, but was greater in V4 than in V2 at both the single-site and population level. The time course of the neural response showed a naturalness signal that was earliest in V4, where it was coincident with the visual response. In V2, the naturalness response emerged only after an untuned transient; the initial transient was earlier in V2 than in V4, but the naturalness signal emerged first in V4. Both visual and naturalness-specific latencies in V4 became shorter with age. Taken together, our longitudinal data suggest that behavioral performance improves at least in part due to changes downstream from V2 and V4. Our analysis of response dynamics suggests that naturalness sensitivity may arise first in V4, before being fed back to earlier areas.