Our understanding of the functions of motor system evolved remarkably in the last 20 years. This is the consequence not only of an increase in the amount of data on this system but especially of a paradigm shift in our conceptualization of it. Motor system is not considered anymore just a “producer” of movements, as it was in the past, but a system crucially involved in cognitive functions. In the present study we review the data on the cortical organization underlying goal-directed actions and action understanding. Our review is subdivided into two major parts. In the first part, we review the anatomical and functional organization of the premotor and parietal areas of monkeys and humans. We show that the parietal and frontal areas form circuits devoted to specific motor functions. We discuss, in particular, the visuo-motor transformation necessary for reaching and for grasping. In the second part we show how a specific neural mechanism, the mirror mechanism, is involved in understanding the action and intention of others. This mechanism is located in the same parieto-frontal circuits that mediate goal-directed actions. We conclude by indicating future directions for studies on the mirror mechanism and suggest some major topics for forthcoming research.

Experiments in monkeys demonstrated that many parietal and premotor neurons coding a specific motor act (e.g., grasping) show a markedly different activation when this act is part of actions that have different goals (e.g., grasping for eating vs. grasping for placing). Many of these “action-constrained” neurons have mirror properties firing selectively to the observation of the initial motor act of the actions to which they belong motorically. By activating a specific action chain from its very outset, this mechanism allows the observers to have an internal copy of the whole action before its execution, thus enabling them to understand directly the agent's intention. Using electromyographic recordings, we show that a similar chained organization exists in typically developing children, whereas it is impaired in children with autism. We propose that, as a consequence of this functional impairment, high-functioning autistic children may understand the intentions of others cognitively but lack the mechanism for understanding them experientially.

Mirror neurons are a distinct class of neurons that transform specific sensory information into a motor format. Mirror neurons have been originally discovered in the premotor and parietal cortex of the monkey. Subsequent neurophysiological (TMS, EEG, MEG) and brain imaging studies have shown that a mirror mechanism is also present in humans. According to its anatomical locations, mirror mechanism plays a role in action and intention understanding, imitation, speech, and emotion feeling.

Though other species of primates also use tools, humans appear unique in their capacity to understand the causal relationship between tools and the result of their use. In a comparative fMRI study, we scanned a large cohort of human volunteers and untrained monkeys, as well as two monkeys trained to use tools, while they observed hand actions and actions performed using simple tools. In both species, the observation of an action, regardless of how performed, activated occipitotemporal, intraparietal, and ventral premotor cortex, bilaterally. In humans, the observation of actions done with simple tools yielded an additional, specific activation of a rostral sector of the left inferior parietal lobule (IPL). This latter site was considered human-specific, as it was not observed in monkey IPL for any of the tool videos presented, even after monkeys had become proficient in using a rake or pliers through extensive training. In conclusion, while the observation of a grasping hand activated similar regions in humans and monkeys, an additional specific sector of IPL devoted to tool use has evolved inHomo sapiens, although tool-specific neurons might reside in the monkey grasping regions. These results shed new light on the changes of the hominid brain during evolution.