In generating motor commands, the brain seems to rely on internal models that predict physical dynamics of the limb and the external world. How does the brain compute an internal model? Which neural structures are involved? We consider a task where a force field is applied to the hand, altering the physical dynamics of reaching. Behavioral measures suggest that as the brain adapts to the field, it maps desired sensory states of the arm into estimates of force. If this neural computation is performed via a population code, i.e., via a set of bases, then activity fields of the bases dictate a generalization function that uses errors experienced in a given state to influence performance in any other state. The patterns of generalization suggest that the bases have activity fields that are directionally tuned, but directional tuning may be bimodal. Limb positions as well as contextual cues multiplicatively modulate the gain of tuning. These properties are consistent with the activity fields of cells in the motor cortex and the cerebellum. We suggest that activity fields of cells in these motor regions dictate the way we represent internal models of limb dynamics.