The capacity to use tools is a fundamental evolutionary achievement. Its essence stands in the capacity to transfer a proximal goal (grasp a tool) to a distal goal (e.g., grasp food). Where and how does this goal transfer occur? Here, we show that, in monkeys trained to use tools, cortical motor neurons, active during hand grasping, also become active during grasping with pliers, as if the pliers were now the hand fingers. This motor embodiment occurs both for normal pliers and for ''reverse pliers,'' an implement that requires finger opening, instead of their closing, to grasp an object. We conclude that the capacity to use tools is based on an inherently goal-centered functional organization of primate cortical motor areas.neurophysiology ͉ tool use ͉ goal coding ͉ motor act
Social life rests in large part on the capacity to understand the intentions behind the behavior of others. What are the origins of this capacity? How is one to construe its development in ontogenesis? By assuming that action understanding can be explained only in terms of the ability to read the minds of others--that is, to represent mental states--the traditional view claims that a sharp discontinuity occurs in both phylogeny and ontogeny. Over the last few years this view has been challenged by a number of ethological and psychological studies, as well as by several neurophysiological findings. In particular, the functional properties of the mirror neuron system and its direct matching mechanism indicate that action understanding may be primarily based on the motor cognition that underpins one's own capacity to act. This article aims to elaborate and motivate the pivotal role of such motor cognition, providing a biologically plausible and theoretically unitary account for the phylogeny and ontogeny of action understanding and also its impairment, as in the case of autistic spectrum disorder.
Mirror neurons are a distinct class of neurons that discharge both during the execution of a motor act and during observation of the same or similar motor act performed by another individual. However, the extent to which mirror neurons coding a motor act with a specific goal (e.g., grasping) might also respond to the observation of a motor act having the same goal, but achieved with artificial effectors, is not yet established. In the present study, we addressed this issue by recording mirror neurons from the ventral premotor cortex (area F5) of two monkeys trained to grasp objects with pliers. Neuron activity was recorded during the observation and execution of grasping performed with the hand, with pliers and during observation of an experimenter spearing food with a stick. The results showed that virtually all neurons responding to the observation of hand grasping also responded to the observation of grasping with pliers and, many of them to the observation of spearing with a stick. However, the intensity and pattern of the response differed among conditions. Hand grasping observation determined the earliest and the strongest discharge, while pliers grasping and spearing observation triggered weaker responses at longer latencies. We conclude that F5 grasping mirror neurons respond to the observation of a family of stimuli leading to the same goal. However, the response pattern depends upon the similarity between the observed motor act and the one executed by the hand, the natural motor template.
What is the evolutionary origin of the human ability to understand and predict the behavior of others? Recent studies suggest that human infants' early capacity for understanding others' goal-directed actions relies on nonmentalistic strategies [1-8]. However, there is no consensus about the nature of the mechanisms underpinning these strategies and their evolutionary history. Comparative studies can shed light on these controversial issues. We carried out three preferential looking-time experiments on macaques, modeled on previous work on human infants [1-5], to test whether macaques are sensitive to the functional efficacy of familiar goal-related hand motor acts performed by an experimenter in a given context and to examine to which extent this sensitivity also is present when observing non-goal-related or unusual goal-related motor acts. We demonstrate that macaque monkeys, similar to human infants, do indeed detect action efficacy by gazing longer at less efficient actions. However, they do so only when the observed behavior is directed to a perceptible and familiar goal. Our results show that the direct detection of the functional fitness of action, in relation to goals that have become familiar through previous experience, is the phylogenetic precursor of intentional understanding.
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