Growing evidence shows that mechanisms controlling CNS plasticity extend beyond the synapseand that alterations in myelin can modify conduction velocity, leading to changes in neuralcircuitry. Although it is widely accepted that newly generated oligodendrocytes (OLs) producemyelin in the adult CNS, the contribution of preexisting OLs to functional myelin remodeling isnot known. Here, we show that sustained activation of extracellular signal-regulated kinases 1and 2 (ERK1/2) in preexisting OLs of adult mice is sufficient to drive increased myelinthickness, faster conduction speeds, and enhanced hippocampal-dependent emotional learning.Although preexisting OLs do not normally contribute to remyelination, we show that sustainedactivation of ERK1/2 renders them able to do so. These data suggest that strategies designed topush mature OLs to reinitiate myelination may be beneficial both for enhancing remyelination indemyelinating diseases and for increasing neural plasticity in the adult CNS.