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Cells that express the NG2 proteoglycan are the largest proliferative progenitor population in the postnatal central nervous system (CNS). Although this entire population has long been considered to be oligodendrocyte progenitors, numerous NG2+ cells are present in the cerebral cortex, where relatively little myelination occurs, and also persist long after myelination is complete in the CNS. Several studies have alluded to the presence of distinct NG2+ cell subtypes based on marker expression, but no experimentally derived hypotheses about the physiological role of these subtypes has been proposed. In the current study, whole-cell patch-clamp data from acutely isolated slices demonstrate that subcortical white matter and cortical NG2+ cells display distinct membrane properties in addition to possessing differing K+- and Na+-channel expression profiles. A striking observation is that a subpopulation of cortical, but not white matter NG2+ cells, elicit depolarization-induced spikes that are akin to immature action potentials. Our data demonstrate that a population of cortical NG2+ cells display physiological properties that differ from their white matter counterparts.