Regular articleActivations related to “mirror” and “canonical” neurones in the human brain: an fMRI study
Introduction
The understanding of goal-directed action requires mechanisms by which the subject can understand the action that is appropriate for an object, as well as mechanisms by which the subject can read the intention conveyed by goal-directed actions performed by others. Within the ventral premotor area F5, there are neurones that discharge during goal-directed actions (Rizzolatti et al., 1988). Among these neurones, Rizzolatti et al 1988, Rizzolatti et al 1996a, Gallese et al 1996 have discovered two populations that have different visual responses, though they are indistinguishable as far as their motor properties are concerned.
The first type, called “canonical neurones,” become active when the monkey simply views an object, as well as when the monkey grasps that object. The bank of F5 is the target of projections originating from the anterior intraparietal area (AIP), which has similar functional properties to those of F5 Taira et al 1990, Sakata et al 1995, Murata et al 2000. On the basis of these common properties, it has been proposed that the AIP-F5 circuit plays a role in transforming the intrinsic properties of objects into the appropriate hand movements (Jeannerod et al., 1995). The description of the object features, in terms of its affordances, is carried out in the parietal area AIP and then transmitted to the premotor area F5, where potential actions are encoded Murata et al 1997, Fagg and Arbib 1998, Rizzolatti and Fadiga 1998.
The second type, called “mirror neurones,” fire both when the monkey observes an agent acting with the hand upon an object and when the monkey grasps the object itself. Neurones with similar visual properties to these F5 convexity neurones have been recorded in the superior temporal sulcus (STS, Perrett et al., 1990) and in area 7b/PF located in the rostral part of the convexity of the anterior inferior parietal cortex (Fogassi et al., 1998). This STS-7b-F5 circuit may subserve the internal representation of actions evoked by the observation of the actions of others and may play a role in both imitation and recognition of action Jeannerod 1994, Rizzolatti et al 1996a, Rizzolatti and Arbib 1998, Gallese and Goldman 1998; Carey et al., 1997; Rizzolatti and Arbib 1998, Gallese and Goldman 1998.
Brain imaging experiments have been carried out in humans in order to investigate the existence and the localization of cortical circuits similar to those described in monkey. Subjects have been scanned during (1) the perception of manmade objects Martin et al 1995, Martin et al 1996, Grafton et al 1997, Perani et al 1999, Chao and Martin 2000, Grèzes and Decety 2002, (2) the manipulation of objects Grafton et al 1996, Binkofski et al 1999, or (3) the perception of simple finger movements Iacoboni et al 1999, Hermsdorfer et al 2001, pantomimes Decety et al 1997, Grèzes et al 1998, Buccino et al 2001, or object-directed actions Rizzolatti et al 1996b, Grafton et al 1996, Perani et al 2001, Buccino et al 2001, Decety et al 2002, Chaminade et al 2002. Common activations have been found in premotor and posterior parietal cortex. Activations have also been reported in the region of Broca’s area, which some have suggested to be the human homologue of monkey premotor area F5 Grafton et al 1996, Rizzolatti et al 1996b, Iacoboni et al 1999, Buccino et al 2001.
However, a recent meta-analysis of PET studies (Grèzes and Decety, 2001) failed to show reliable activation in Broca’s areas during action observation, and this led the authors to propose that the ventral premotor cortex, rather than Broca’s area, might be homologous to F5. Nonetheless, there could be two reasons for the absence of reliable activations in the ventral premotor cortex and/or Broca’s areas during action observation, action execution, and imitation. The first is that PET may be less sensitive than fMRI (see Joliot et al., 1999). Second, it has been shown that the neural network engaged is influenced by the type of action presented and by the tasks required during the observation phase (Grèzes et al., 1998). Finally, none of the studies cited have included conditions within the same paradigm where subjects perceive both objects and gestures, whether for passive observation and for movement execution.
Our experiment uses event-related fMRI to investigate all conditions within the same study in which canonical neurones and mirror neurones fire in the macaque premotor cortex. Humans can imitate gestures whether directed to an object or not. We therefore tested both conditions, even though mirror neurones in monkeys do not respond to the sight of a hand mimicking an action in the absence of an object. Subjects viewed video recordings of objects, grasping movements, or objects being grasped. They were required either to passively observe or to execute the appropriate grasp toward a manipulandum. The aim of the present experiment was to functionally identify mirror and canonical circuits in humans and to tentatively localize the human homologue of F5. The human brain regions homologous to the monkey canonical and mirror circuits should be active for viewing an object alone (canonical neurones) and for viewing hands grasping objects (mirror neurones), as well as for executing the appropriate grasp (canonical and mirror neurones).
Section snippets
Subjects
Twelve right-handed male subjects (range, 19–39 years) with no neurological or psychiatric history participated in the imaging study. All gave informed consent according to procedures approved by the Joint Ethics Committee of the National Hospital for Neurology and Neurosurgery (UCLH NHS Trust) and Institute of Neurology (UCL).
Stimuli
The stimuli consisted of color video recordings (3.5 s each) of objects, grasping pantomimes, and objects being grasped. The baseline condition consisted of a stationary
Conjunction analysis
We performed conjunction analyses in order to describe the neural network common to both contexts (passive observation and execution) elicited by the perception of object, gesture, or object being grasped (Table 1). The observation of object, irrespective of context (OOvsOB and EOvsEB), was associated with activation in the left ventral precentral sulcus. There was no significant activation in the parietal cortex for this conjunction. It is clear from Fig. 1B that this is because the area was
Canonical circuit (OO and EO)
We found a parietopremotor circuit to be active during observation of manipulable objects. This circuit includes an area located in the anterior part of the intraparietal sulcus, at the junction with the postcentral sulcus, as well as the ventral sector of the precentral sulcus, at the junction between premotor area 6 and Broca’s area 44.
The left anterior part of the intraparietal sulcus was active during passive observation of manipulable objects, but also during all conditions, including the
Acknowledgements
We are grateful for the assistance of the radiographers. The Wellcome Trust supported J. Grèzes, J. Rowe, RE. Passingham, and the Wellcome Department of Imaging Neuroscience.
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