Periventricular heterotopia (PH) is a cortical malformation characterized by misplaced neurons adjacent to the lateral ventricles, commonly associated with epilepsy. It is genetically diverse, and its underlying mechanisms are not fully understood. While recent research suggests that neuronal differentiation can also be affected, it has traditionally been considered a neuronal migration disorder, supported by the identification of mutations in neuronal-enriched cytoskeletal genes. Furthermore, it is still unclear why only some neurons are affected in this condition, while the majority of other cortical cells can successfully reach their cortical position. In this context, we examined the effects of the PH-associated MAP1B gene (a microtubule-associated protein gene highly expressed in developing neurons) in the mouse cortex. Using in utero electroporation, we found that knocking down (KD) Map1b leads to the ectopic positioning of cells in the periventricular region of the brain. Surprisingly, we uncovered a dual role of Map1b in cortical development, by regulating both neuronal migration and neural stem cell differentiation. Using live imaging of organotypic slices and single-cell RNA sequencing, we identified a subpopulation of mis-migrating neurons that emerges only after Map1b-KD in progenitor cells. Strikingly, we discovered an alternative localization for MAP1B in neural stem cells dictating their differentiation. Our findings shed light on the multifaceted roles of proteins in cortical development and their relevance to the etiology behind neuronal heterotopias, emphasizing differentiation defects as the core of this ‘migration’ disorder.