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We show that loss of <jats:italic>Kif3a<\/jats:italic>, an important functional component of primary cilia, leads to the degeneration of primary cilia, marked overgrowth of the cortex, and altered cell cycle kinetics within cortical progenitors. The G1 phase of the cell cycle is shortened through a mechanism likely involving reduced Gli3 activity and a resulting increase in expression of cyclin D1 and <jats:italic>Fgf15<\/jats:italic>. The defects in Gli3 activity alone are sufficient to accelerate cell cycle kinetics and cause the molecular changes seen in brains that lack cilia. Finally, we show that levels of full\u2010length and repressor Gli3 proteins are tightly regulated during normal development and correlate with changes in expression of two known Shh\u2010target genes, <jats:italic>CyclinD1<\/jats:italic> and <jats:italic>Fgf15<\/jats:italic>, and with the normal lengthening of the cell cycle during corticogenesis. These data suggest that Gli3 activity is regulated through the primary cilium to control cell cycle length in the cortex and thus determine cortical size. \u00a9 2011 Wiley Periodicals, Inc. 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