Protracted functional and structural reorganization of human prefrontal cortex supports lateralized category geometries

Abstract

Despite being visually responsive, how prefrontal cortex represents visual categories across development and how this compares to posterior visual cortex remains unknown. Here, we show that ventrolateral prefrontal cortex (VLPFC) follows a fundamentally distinct developmental trajectory. Using functional and quantitative MRI in children and adults, we demonstrate that VLPFC exhibits reliable and structured category-selective responses in childhood that undergo prolonged reorganization into mature, hemisphere-specific representational geometries. Right VLPFC progressively organizes categories along an animate-inanimate axis, while left VLPFC consolidates a word-selective organization, a lateralization that strengthens across development. This restructuring contrasts sharply with ventral temporal cortex (VTC), which exhibits bilaterally organized, adult-like category structure in childhood. Critically, prefrontal representational structure emerges in alignment with conserved folding patterns of the precentral and inferior frontal sulci, suggesting that cortical anatomy provides a stable scaffold for the maturation of abstract representations. Quantitative MRI further reveals a non-linear trajectory of tissue development in right VLPFC, marked by adolescent reductions in macromolecular content and increased microstructural heterogeneity in adulthood, a pattern not observed in VTC. Together, these findings demonstrate that VLPFC undergoes prolonged, anatomically constrained refinement of category-related geometry characterized by hemisphere-specific taxonomies, rather than simply inheriting representational structure from sensory cortex. O_LIUnlike VTC (which shows early, bilateral, and stable category organization), VLPFC contains reliable, category-selective representations from childhood that undergo prolonged, hemisphere-specific developmental refinement rather than simple amplification C_LIO_LIRight VLPFC progressively consolidates an animate-inanimate representational axis across development, while left VLPFC establishes an early, stable word-selective organization consistent with language network maturation C_LIO_LIFunctional boundaries in VLPFC align with conserved intrasulcal folding motifs (plis de passage), demonstrating that anatomical scaffolding of category-selective responses extends beyond sensory cortex to prefrontal association cortex C_LIO_LIRight VLPFC undergoes adolescent pruning of cortical tissue microstructure diverging sharply from the continuous tissue proliferation observed in ventral temporal cortex C_LI