The motor cortex has long been known to play a central role in the generation and control of volitional movement, yet its intrinsic functional organization is not fully understood. Two alternate views on the functional organization of motor cortex have been proposed. Short-duration (>50 ms) intracortical stimulation (SD-ICMS) reveals a somatotopic representation of body musculature, whereas long-duration (~500 ms) ICMS (LD-ICMS) reveals a topographic representation of coordinated movement endpoint postures. The functional organization of motor cortex in the rat was probed using combined approaches of in vivo microstimulation, behavioural analysis of forelimb motor performance, and acute cortical cooling deactivation. The first study, using a rodent model of Parkinson’s disease and therapeutic deep brain stimulation of the subthalamic nucleus, determined that acute changes (<60 s) in cortical output function and motor performance are reflected in reversible alterations in movement thresholds and representation sizes. A second study characterized forelimb movement representations under SD-ICMS revealing a dual-representation (digit, wrist, elbow, shoulder) within rostral (RFA) and caudal (CFA) forelimb motor areas. LD-ICMS elicited forelimb reach-to-grasp behaviour (elevate, advance, grasp, retract) with a functional segregation between RFA (grasp) and CFA (elevate, advance, retract) representations. Behaviourally distinct functional roles between these two areas was confirmed through behavioural assessment during selective cortical cooling deactivation. A final study demonstrated increased movement representation overlap assessed with LD-ICMS following repeated kindled-seizures that was not attributed to changes in intracortical inhibition. Current experimentation provides the first causal evidence for movement-based rather than muscle-based functional organization of motor cortex and functional neocortical movement encoding in the rat.