The development of the cerebral cortex requires coordinated regulation of proliferation, specification, migration and differentiation of cortical progenitors into functionally integrated neurons. The completion of the neurogenic program requires a dynamic interplay between cell intrinsic regulators and extrinsic cues, such as growth factor and neurotransmitters. We previously demonstrated a role for extrasynaptic glycine receptors (GlyRs) containing the a2 subunit in cerebral cortical neurogenesis, revealing that endogenous GlyR activation promotes interneuron migration in the developing cortical wall. The proliferative compartment of the cortex comprises apical progenitors that give birth to neurons directly or indirectly through the generation of basal progenitors, which serve as amplification step to generate the bulk of cortical neurons. The present work shows that genetic inactivation of Glra2, the gene coding the a2 subunit of GlyRs, disrupts dorsal cortical progenitor homeostasis with an impaired capability of apical progenitors to generate basal progenitors. This defect results in an overall reduction of projection neurons that settle in upper or deep layers of the cerebral cortex. Overall, the depletion of cortical neurons observed in Glra2-knockout embryos leads to moderate microcephaly in newborn Glra2-knockout mice. Taken together, our findings support a contribution of GlyR a2 to early processes in cerebral cortical neurogenesis that are required later for the proper development of cortical circuits. The cerebral cortex develops from the forebrain and contains different classes of neurons distributed within layers that are regionally organized into sensory, motor and association areas. Cerebral cortex layering arises inside-out as progenitors give birth to successive waves of pyramidal projection neurons in the dorsal telencephalon 1 and GABAergic interneurons in the ventral forebrain.2 Projection neurons migrate radially to settle in appropriate layers of the cortical plate (CP) from where they grow axonal projections towards cortical or subcortical targets. Interneurons migrate from the ganglionic eminences along multiple tangential paths to integrate local cortical networks. More generally, the development of the cortex progresses through successive steps including proliferation, specification, migration and neuronal differentiation. Disrupting the completion of one or several of these cellular events may lead to severe cortical malformations underlying neurological disorders characterized by learning and intellectual disability or epilepsy.