VTA projections to M1 are essential for reorganization of layer 2-3 network dynamics underlying motor learning.

Abstract

The primary motor cortex (M1) is crucial for motor skill learning. Previous studies demonstrated that skill acquisition requires dopaminergic VTA (ventral-tegmental area) signaling in M1, however little is known regarding the effect of these inputs at the neuronal and network levels. Using dexterity task, calcium imaging, chemogenetic inhibiting, and geometric data analysis, we demonstrate VTA-dependent reorganization of M1 layer 2-3 during motor learning. While average activity and average functional connectivity of layer 2-3 network remain stable during learning, activity kinetics, correlational configuration of functional connectivity, and average connectivity strength of layer 2-3 neurons gradually transform towards an expert configuration. Additionally, sensory tone representation gradually shifts to success-failure outcome signaling. Inhibiting VTA dopaminergic inputs to M1 during learning, prevents all these changes. Our findings demonstrate dopaminergic VTA-dependent formation of outcome signaling and new connectivity configuration of the layer 2-3 network, supporting reorganization of the M1 network for storing new motor skills.