Oligodendrocyte maturation has been defined based on expression of developmentally regulated antigens. However, transitions at early stages of the lineage have not been functionally characterized fully in situ. Combining 2',3'-cyclic nucleotide 3'-phosphodiesterase (CNP)-promoter driven enhanced green fluorescent protein expression and whole-cell capacitance measurements permitted a reliable distinction between subcortical white matter NG2+ oligodendrocyte progenitors (OPs) and O4+ preoligodendrocytes (pre-OLs) in situ. We focused on K+ channels because their expression has been associated previously with the proliferation and differentiation potential of OPs. Using whole-cell patch clamp, we observed a downregulation of the delayed outward-rectifying current (IKDR) between the NG2+ and O4+ stages but no significant changes in transient K+-channel current (IKA) amplitude. Tyrosine kinase inhibition in NG2+ cells reduced IKDR amplitude with no effect on IKA, which mimicked the endogenous changes observed between OPs and pre-OLs. Tyrosine kinase inhibition also reduced the proliferative capacity of NG2+ OPs in slice cultures. Conversely, acute platelet-derived growth factor receptor-alpha (PDGFR-alpha) activation caused an increase of IKDR in NG2+ but not in O4+ cells. Consistent with this finding, PDGFR-alpha immunoreactivity was confined to NG2+ cells with undetectable levels in O4+ cells, suggesting that PDGFR-alpha signaling is absent in pre-OLs in situ. Importantly, the PDGF-induced increase of IKDR in NG2+ cells was prevented by tyrosine kinase inhibition. Together, these data indicate that PDGFR-alpha and tyrosine kinase activity act via a common pathway that influences functional expression of K+ channels and proliferative capacity of OPs in situ.