Loss of dopamine neurons causes motor deterioration in Parkinson's disease patients. We have previously reported that in addition to acute motor impairment, the impaired motor behavior is encoded into long-term memory in an experience-dependent and task-specific manner, a phenomenon we refer to as aberrant inhibitory motor learning. Although normal motor learning and aberrant inhibitory learning oppose each other and this is manifested in apparent motor performance, in the present study, we found that memory of normal motor learning acquired prior to aberrant inhibitory learning remains preserved in the brain, suggesting the existence of independent storage. To investigate the neuronal circuits underlying these two opposing memories, we took advantage of the RNA-binding protein YTHDF1, an m6A RNA methylation reader involved in the regulation of protein synthesis and learning/memory. Conditional deletion of Ythdf1 in either D1 or D2 receptor-expressing neurons revealed that memory of normal learning is stored in the D1 (direct) pathway of the basal ganglia, while inhibitory memory is stored in the D2 (indirect) pathway. Furthermore, fiber photometry recordings of GCaMP signals from striatal D1 (dSPN) and D2 (iSPN) receptor-expressing neurons support the preservation of memory in normal learning in the direct pathway after aberrant inhibitory learning, with activities of dSPN predictive of motor performance. We also built a computational model based on activities of motor cortical neurons, dSPN and iSPN neurons, and their interactions through the basal ganglia loops that successfully explained various experimental observations. Building on the computational model, we investigated the neuronal population underlying normal and aberrant inhibitory learning via cFos expression, and studied the role of intracellular cAMP pathway in aberrant inhibitory learning using chemogenetic approaches. Finally, we explored potential approaches for rescuing and reversing aberrant inhibitory learning, and we found that D1 agonist treatment or prolonged normal learning could rescue aberrant inhibitory learning in mice. Together, these findings have important implications for novel approaches in treating Parkinson’s disease by reactivating preserved memory of normal learning, and in treating hyperkinetic movement disorders such as chorea or tics by erasing aberrant motor memories.