Motor learning drives region-specific transcriptomic remodeling in the motor cortex and dorsal striatum

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Summary Motor learning depends on coordinated activity across the motor cortex (M1) and dorsal striatum (dSTR), yet the molecular mechanisms driving learning-related synaptic and circuit remodeling remain unclear. Here, we combine activity-dependent genetic labeling (TRAP) with single-cell RNA sequencing to generate an unbiased, cell type-resolved transcriptional atlas of behaviorally engaged populations during a forelimb reaching task. We identify diverse activated neurons across M1 and dSTR, including a striking enrichment of Htr3a-expressing interneurons (Htr3a INs) in M1 that are selectively recruited during skilled reaching, as confirmed by two-photon calcium imaging. Corticostriatal projection neurons and striatal spiny projection neurons show subtype-and region-specific transcriptional remodeling involving genes linked to synaptic function, translation, and metabolism. Glial cells—including astrocytes, oligodendrocytes, and microglia— exhibit similarly robust, stage-and region-dependent gene regulation. These findings provide a comprehensive molecular framework for motor learning and highlight coordinated, cell type-specific transcriptional programs in neurons and glia that shape the encoding and retrieval of motor memory. Highlights - Motor learning activates interneuron cell types in motor cortex and striatum - Htr3a-expressing interneurons in motor cortex are specifically activated while performing a learned reaching behavior - Transcriptome remodeling exhibited distinct patterns between motor cortex and striatum - Glial cells showed stage- and region-specific transcriptomic alteration patterns that align with those in neurons

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