The frontal-subcortical skeletomotor circuit is thought to be a motor processing network. However, the exact function of the circuit is poorly characterized. This fMRI study utilized a motor activation paradigm for both hands to probe circuit engagement and connectivity. Activation of the circuit decreased over time for the right hand, which suggests circuit engagement can vary during task execution. Changes in activation of the right dorsolateral prefrontal cortex were highly correlated with changes in activation of right skeletomotor circuit input, output and intrinsic nuclei for both the left and right-hand tasks, which indicates significant functional connectivity between these brain regions during motor activity. This finding suggests circuit involvement in motor execution may be more complex than predicted by the two-pathway hypothesis of circuit function. Finally, patterns of activation suggested that the two-pathway hypothesis does not completely explain activation in response to a synchronized motor task.