Learning Task-Related Activities From Independent Local-Field-Potential Components Across Motor Cortex Layers

Motor cortical microcircuits receive inputs from dispersed cortical and subcortical regions in behaving animals. However, how these inputs contribute to learning and execution of voluntary sequential motor behaviors remains elusive. Here, we analyzed the independent components extracted from the local field potential (LFP) activity recorded at multiple depths of rat motor cortex during reward-motivated movement to study their roles in motor learning. Because slow gamma (30–50 Hz), fast gamma (60–120 Hz), and theta (4–10 Hz) oscillations temporally coordinate task-relevant motor cortical activities, we first explored the behavioral state- and layer-dependent coordination of motor behavior in these frequency ranges. Consistent with previous findings, oscillations in the slow and fast gamma bands dominated during distinct movement states, i.e., preparation and execution states, respectively. However, we identified a novel independent component that dominantly appeared in deep cortical layers and exhibited enhanced slow gamma activity during the execution state. Then, we used the four major independent components to train a recurrent network model for the same lever movements as the rats performed. We show that the independent components differently contribute to the formation of various task-related activities, but they also play overlapping roles in motor learning.