Distinct Neocortical Progenitor Lineages Fine-tune Neuronal Diversity in a Layer-specific Manner

Abstract How the variety of neurons that organize into neocortical layers and functional areas arises is a central question in the study of cortical development. While both intrinsic and extrinsic cues are known to influence this process, whether distinct neuronal progenitor groups contribute to neuron diversity and allocation is poorly understood. Using in vivo genetic fate-mapping combined with whole-cell patch clamp recording, we show that the firing pattern and apical dendritic morphology of excitatory neurons in layer 4 of the barrel cortex are specified in part by their neural precursor lineage. Further, we show that separate precursors contribute to unique features of barrel cortex topography including the intralaminar position and thalamic innervation of the neurons they generate. Importantly, many of these lineage-specified characteristics are different from those previously measured for pyramidal neurons in layers 2–3 of the frontal cortex. Collectively, our data elucidate a dynamic temporal program in neuronal precursors that fine-tunes the properties of their progeny according to the lamina of destination.