The cortical scene processing network emerges in infancy, prior to independent navigation experience

Abstract

Sighted people rely on vision to recognize and navigate the local environment. By adulthood, human cortex contains at least three regions that respond selectively to visual scene information, but it remains unknown when or how these regions develop. One hypothesis is that scene selectivity emerges gradually in regions that initially prefer certain low-level visual features (e.g., peripheral visual input, high spatial frequencies, rectilinearity), and then exposure to the visual statistics of natural scenes drives the emergence of scene selective responses. However, both aspects of this hypothesis remain to be tested: how early scene selectivity first arises in human development, and whether it is driven by passive exposure to visual statistics. We therefore collected functional magnetic resonance imaging data from awake 2-9-month-old infants while they watched videos of real-world scenes with ego-motion, as well as faces, objects, and scrambled videos. We found stronger responses to scenes than control conditions in the location of all three scene regions. Scene-selective responses could not be explained by low-level visual properties of the stimuli, and were found in infants as young as 2-5 months old, with no evidence of age-related change. We also measured infants experience independently navigating (e.g., crawling), which was not necessary for the development of scene-selectivity. In sum, cortical regions are scene-selective in human infants prior to independent navigation, and after only limited exposure to visual scene statistics. Significance statementDespite extensive work on the functional organization of scene processing in the human adult visual cortex, little is known about the developmental origins of category selectivity for visual scenes. Here we used fMRI in awake human infants to discover that all three regions of the known visual scene processing system are present within the first few months of life - the youngest age yet detected. Scene-selective cortex therefore develops after only a few months of limited visual exposure, and prior to active experience using visual scene information to plan and guide independent navigation (e.g., by crawling). These findings provide a fundamental constraint on theories of how scene selectivity develops in high-level visual cortex.