Neural measurements of sensitivity to texture naturalness in developing macaques

Performance on a variety of visual tasks improves across early development. By identifying a neural substrate for this improvement, we can improve our understanding of visual function. Previous measurements of spatial contrast sensitivity, made in the LGN, V1, and V2, could not account for behavioral improvements. We wondered whether a stimulus feature that is more tightly linked to a specific neural locus could help us target developmental improvements. The model of Portilla and Simoncelli generates textures matched in spectral content, but varying in the strength of their naturalistic image statistics. Importantly, neuronal sensitivity to this “naturalness” is not seen in adult area V1, but is seen in adult areas V2 and V4. Using 96-channel multielectrode arrays, we recorded neural responses from areas V1, V2 and V4 from macaques at six and twelve months of age both to bandpass-filtered noise stimuli varying in contrast (as well as spatial frequency and orientation), and to texture stimuli varying in naturalness. We used standard classification techniques to measure both spatial contrast and texture naturalness sensitivity from recorded spiking activity, and we interleaved behavioral measurements from the same animals for comparison. Neural sensitivity to both contrast and naturalness was similar across age. While contrast sensitivity was similar between areas, naturalness sensitivity was greater in area V4 than in V2, as we and others have found in data from adults. These results suggest that the hierarchical processing of texture sensitivity observed in adults is established early in development.