Microstructural pruning in human prefrontal cortex scaffolds its functional reorganization across development

Abstract

Neural representations in occipitotemporal cortex emerge during development in response to visual experience with ecological stimulus categories, such as faces or words. While similar category-selective representations have also been observed in the frontal lobe, how they emerge across development, whether current models of brain development extend to prefrontal cortex, and the extent to which such high-level representations are anatomically consistent across the lifespan is unknown. Through a combination of functional and quantitative MRI scans, we observe previously undescribed cortical folding patterns in human-specific inferior frontal cortex whose consistency reveals that childhood representations for visual object categories rearrange into stable adulthood patterns. This functional restructuring was distinct from occipitotemporal cortex where adult-like response patterns only scale in magnitude across development. The unique form of functional development in prefrontal cortex was accompanied by restructuring of cortical tissue properties: macromolecules are pruned across adolescence in prefrontal cortex while they proliferate in temporal cortex. These results suggest visual representations in distinct cortical lobes undergo distinct developmental trajectories, and that human-specific prefrontal cortex shows an especially protracted maturational process that necessitates late-stage tissue restructuring detectable in the living brain.