Over the past two decades single cell recordings in primates and neuroimaging experiments in humans have uncovered the key properties of visuo-motor mirror neurons located in monkey premotor cortex and parietal cortices as well as homologous areas in the human inferior frontal and inferior parietal cortices which presumably house neurons with similar response properties. One of the most interesting claims regarding the human mirror neuron system (MNS) is that its activity reflects high-level action understanding. If this was the case, one would expect signal in the MNS to differentiate between meaningful and meaningless actions. In the current experiment we tested this prediction using a novel paradigm. Functional magnetic resonance images were collected while participants viewed (i) short films of object-directed actions (ODAs) which were either semantically meaningful, i.e. a hand pressed a stapler or semantically meaningless, i.e. a foot pressed a stapler, (ii) short films of pantomimed actions and (iii) static pictures of objects. Consistent with the notion that the MNS represents high-level action understanding, meaningful and meaningless actions elicited BOLD signal differences at bilateral sites in the supramarginal gyrus (SMG) of the inferior parietal lobule (IPL) where we observed a double dissociation between BOLD response and meaningfullness of actions. Comparison of superadditive responses in the inferior frontal gyrus (IFG) and IPL (supramarginal) regions revealed differential contributions to action understanding. These data further specify the role of specific components of the MNS in understanding object-directed actions.