In identical experiments in and out of a MR scanner, we recorded functional magnetic resonance imaging and electromyographic correlates of wrist stabilization against constant and time-varying mechanical perturbations. Positioning errors were greatest while stabilizing random torques. Wrist muscle activity lagged changes in joint angular velocity at latencies suggesting trans-cortical reflex action. Drift in stabilized hand positions gave rise to frequent, accurately directed, corrective movements, suggesting that the brain maintains separate representations of desired wrist angle for feedback control of posture and the generation of discrete corrections. Two patterns of neural activity were evident in the blood-oxygenation-level-dependent (BOLD) time series obtained during stabilization. A cerebello-thalamo-cortical network showed significant activity whenever position errors were present. Here, changes in activation correlated with moment-by-moment changes in position errors (not force), implicating this network in the feedback control of hand position. A second network, showing elevated activity during stabilization whether errors were present or not, included prefrontal cortex, rostral dorsal premotor and supplementary motor area cortices, and inferior aspects of parietal cortex. BOLD activation in some of these regions correlated with positioning errors integrated over a longer time-frame consistent with optimization of feedback performance via adjustment of the behavioral goal (feedback setpoint) and the planning and execution of internally generated motor actions. The finding that nonoverlapping networks demonstrate differential sensitivity to kinematic performance errors over different time scales supports the hypothesis that in stabilizing the hand, the brain recruits distinct neural systems for feedback control of limb position and for evaluation/adjustment of controller parameters in response to persistent errors.