Mammalian brain development is characterized by disproportionate growth of the forebrain compared to other regions. However, the exact process driving this localized enlargement remains largely unknown. In order to characterize region specific birthdating patterns, we generated an atlas of neuronal birthdate in the mouse brain. We used two complementary birthdating techniques to systematically acquire the time of birth of neurons across a big variety of brain structures during the embryonic neurogenic period. We identified that most brain stem regions are born in a transient manner with the majority of neurogenesis taking place in the early stages of brain development, while the forebrain neurogenesis is sustained along a much longer time window. This sustained neurogenesis coincides with a lengthened cell cycle and a reduction of consumptive division of apical progenitor resulting in their preservation for longer time period. Using single-cell RNA sequencing, we identified functional spatio-temporal molecular programs regulating progenitors cycling properties. We used loss-of-function assay of the forebrain-enriched mitochondrial protein FAM210B to successfully decreased cell cycle length of neocortical progenitors and thus increase their consumptive division rate, creating a “hindbrain-like” scenario. These results reveal a parsimonious mechanism to locally regulate neuronal production, in which the time window during which progenitors generate cells is a critical determinant of region-specific brain expansion.