Activation of the human primary motor cortex during observation of tool use
Introduction
Area F5 in the ventral premotor cortex of the monkey contains neurons that discharge both when the monkey performs goal-directed hand movements and when he observes another monkey or human to execute similar movements Di Pellegrino et al., 1992, Gallese et al., 1996. These “mirror neurons” seem to be a core part of a system that directly matches observed and executed actions Gallese et al., 1996, Rizzolatti et al., 1996a. Recent functional neuroimaging and electrophysiological studies indicate that mirror neurons exist also in the human brain. Areas comprising the human mirror-neuron system (MNS) include at least the inferior frontal gyrus and the primary motor cortex, and often the superior temporal sulcus and the inferior parietal lobule are activated as well Fadiga et al., 1995, Grafton et al., 1996, Hari et al., 1998, Iacoboni et al., 1999, Nishitani and Hari, 2000, Nishitani and Hari, 2002, Rizzolatti et al., 1996b. The MNS could have an important role both in understanding the meaning of the observed actions and in motor learning and imitation Gallese et al., 1996, Jeannerod, 1994, Rizzolatti et al., 1996a.
The F5 mirror neurons respond maximally when the monkey is observing goal-directed interactions of a hand with an object, such as placing, grasping, holding, and manipulation Di Pellegrino et al., 1992, Gallese et al., 1996. However, when the object is grasped with a tool (e.g., pliers and forceps), the monkey mirror neurons are either not activated at all (Rizzolatti et al., 1996a) or fire only very weakly (Gallese et al., 1996). These findings have led to the view that tool use does not activate the mirror neurons. However, the human and monkey MNSs may differ in several aspects; apart from the genetic differences, humans observe and use tools from early childhood, and one may envision that such experiences expand the motor repertoire of the MNS. Although some higher primates can use simple tools, only humans possess the neural capacity and the unique hand functionality for efficient precision grasp and the use of complex tools Ambrose, 2001, Marzke, 1997, Susman, 1998. Consequently, the human premotor areas could contain representations of category-specific knowledge of tools, likely reflecting the intrinsic properties of these objects Martin et al., 1995, Martin et al., 1996, Perani et al., 1995.
The involvement of the primary motor cortex in the human MNS was first shown with magnetoencephalography (MEG) by monitoring the level of the ∼20-Hz motor-cortex rhythm during observation of hand actions (Hari et al., 1998). Several lines of evidence suggest that the ∼20-Hz rhythm originates predominantly in the precentral primary motor cortex (for reviews, see Hari and Salmelin, 1997, and Hari and Salenius, 1999). First, oscillatory activity of similar frequency has been recorded intraoperatively from the anterior wall of the human central sulcus (Jasper and Penfield, 1949). Second, the sources of the ∼20-Hz component of the rolandic MEG rhythm are slightly more anterior to sources of the ∼10 Hz component that arises in the postcentral somatosensory cortex (Salmelin and Hari, 1994). Third, the ∼20-Hz rhythm is coherent with motor unit firing during isometric muscle contraction which also supports motor-cortex origin of the ∼20-Hz rhythm (Salenius et al., 1997). After electrical median nerve stimulus, the ∼20-Hz motor-cortex rhythm is first transiently, and bilaterally suppressed, and then 200–400 ms later strongly enhanced (Salmelin and Hari, 1994). This “rebound” likely reflects cortical inhibition, as has been argued on the basis of both MEG and transcranial magnetic stimulation studies Abbruzzese et al., 2001, Chen et al., 1999, Salmelin and Hari, 1994. Consequently, the rebound has been used as an indicator of the functional state of the primary motor cortex Hari et al., 1998, Schnitzler et al., 1997, Silén et al., 2000. The rebound is abolished during action execution Salenius et al., 1997, Schnitzler et al., 1997 and significantly suppressed during action observation (Hari et al., 1998). The suppression, indicating activation of the primary motor cortex, is typically bilateral, even if the action was unilateral Hari et al., 1998, Salenius et al., 1997.
Here, we monitored the level of the ∼20-Hz activity to find out whether the motor-cortex part of the human MNS would be activated by observation of tool use, in contrast to monkey mirror neurons that only react to direct hand-object contact. We expected that the more elaborate human MNS would react also to observation of actions performed with tools.
Section snippets
Subjects
We studied 10 healthy subjects. One male subject was discarded from the analysis because of an absence of any poststimulus ∼20-Hz rebound, leaving four females and five males (age range 22–34 years, mean ± SD 28.1 ± 3.1 years). All subjects were right-handed, as assessed by the Edinburgh Handedness Inventory, with a mean ± SD laterality quotient of 87.8 ± 18.5 and a range from 62.5 to 100. An informed oral consent was obtained from all subjects after explanation of the measurement. The study
Results
Fig. 2 (left) shows the sources of the ∼20-Hz activity superimposed on the surface rendition of the brain of Subject 3. In agreement with earlier observations, the dipoles are clustered just anterior to the central sulcus Hari et al., 1998, Salmelin and Hari, 1994. The Talairach coordinates for the median of all source locations were x = 35, y = −23, z = 48, thereby agreeing with the location of the primary motor cortex (Talairach and Tournoux, 1988).
Fig. 2 (right) shows for two subjects the
Discussion
The observed suppression of the ∼20-Hz rebound during observation of tool use indicates activation of the primary motor cortex. The effect was significantly stronger when the subjects observed goal-directed than non-goal-directed tool use. These data broaden the view of human MNS, suggesting that also actions performed with tools are represented in this circuitry.
In monkeys, actual contact of hand with the grasped object is required for F5 mirror neuron activation Gallese et al., 1996,
Acknowledgements
This study was supported by the Academy of Finland, Sigrid Jusélius Foundation, and the EU's Large-Scale Facility Neuro-BIRCH III at the Brain Research Unit of the Low Temperature Laboratory, Helsinki University of Technology. We thank Tuukka Raij and Hanna Renvall for valuable comments on the manuscript.
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