Elsevier

NeuroImage

Volume 23, Issue 1, September 2004, Pages 187-192
NeuroImage

Activation of the human primary motor cortex during observation of tool use

https://doi.org/10.1016/j.neuroimage.2004.06.010Get rights and content

Abstract

Tool use is a characteristic human trait, requiring motor skills that are largely learned by imitation. A neural system that supports imitation and action understanding by directly matching observed actions and their motor counterparts has been found in the human premotor and motor cortices. To test whether this “mirror-neuron system” (MNS) would be activated by observation of tool use, we recorded neuromagnetic oscillatory activity from the primary motor cortex of 10 healthy subjects while they observed the experimenter to use chopsticks in a goal-directed and non-goal-directed manner. The left and right median nerves were stimulated alternatingly, and the poststimulus rebounds of the ∼20-Hz motor-cortex rhythms were quantified. Compared with the rest condition, the level of the ∼20-Hz rhythm was suppressed during observation of both types of tool use, indicating activation of the primary motor cortex. The suppression was on average 15–17% stronger during observation of goal-directed than non-goal-directed tool use, and this difference correlated positively with the frequency of subjects' chopstick use during the last year. These results support the view that the motor-cortex activation is related to the observer's ability to understand and imitate motor acts.

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.

References (36)

  • R. Byrne et al.

    Learning by imitation: a hierarchical approach

    Behav. Brain Sci.

    (1998)
  • R. Chen et al.

    Modulation of motor cortex excitability by median nerve and digit stimulation

    Exp. Brain Res.

    (1999)
  • J. Decety et al.

    Brain activity during observation of actions. Influence of action content and subject's strategy

    Brain

    (1997)
  • G. Di Pellegrino et al.

    Understanding motor events: a neurophysiological study

    Exp. Brain Res.

    (1992)
  • L. Fadiga et al.

    Motor facilitation during action observation: a magnetic stimulation study

    J. Neurophysiol.

    (1995)
  • V. Gallese et al.

    Action recognition in the premotor cortex

    Brain

    (1996)
  • S.T. Grafton et al.

    Localization of grasp representations in humans by positron emission tomography. 2. Observation compared with imagination

    Exp. Brain Res.

    (1996)
  • R. Hari et al.

    Rhythmical corticomuscular communication

    NeuroReport

    (1999)
  • Cited by (147)

    • Modality-specific dysfunctional neural processing of social-abstract and non-social-concrete information in schizophrenia

      2021, NeuroImage: Clinical
      Citation Excerpt :

      Based on previous research, we hypothesized activation of the mPFC and a left frontal-temporal network (e.g., inferior frontal gyrus, middle temporal gyrus) for the processing of social-abstract information (Mitchell et al., 2002). For non-social-concrete information processing, we hypothesized left-lateralized regions including the lateral occipitotemporal cortex (LOTC), the superior temporal gyrus/sulcus (STG/STS), as well as pre/postcentral gyri forming the putative mirror neuron system (Järveläinen et al., 2004; Johnson-Frey, 2004; Johnson-Frey et al., 2003; Lingnau and Downing, 2015). We focused directly on group differences between a group of patients suffering from schizophrenia or schizoaffective disorder, and their age- and education-matched controls: for social content, as patients are well-known for their social cognition impairments, we expected patients to show reduced activation in the mPFC, irrespective of encoding modality (Frith, 2004); For non-social content, despite mixed findings from previous neuroimaging research on hand action observation on schizophrenia (Horan et al., 2014; Thakkar et al., 2014), following previous report on dysfunctional processing of non-social linguistic stimuli in schizophrenia (Kuperberg et al., 2008), we hypothesized neural modulation of the object-related regions for patients with schizophrenia for both gesture and speech modalities.

    • Investigating the Role of Alpha and Beta Rhythms in Functional Motor Networks

      2018, Neuroscience
      Citation Excerpt :

      The mental rehearsal or execution of a motor task that does not actually lead to physical execution is often referred to as motor imagery (Decety and Ingvar, 1990). Motor imagery has drawn a lot of attention especially due to the similar (to motor execution) activation patterns that it elicits in the human brain (Pfurtscheller and Neuper, 1997; Avikainen et al., 2002; Järveläinen et al., 2004) and it has been extensively utilized in rehabilitation practices and sports training. More importantly, motor imagery has been employed in cases of severe neurological disability (such as those caused by strokes or spinal cord injury) as a control modality of Brain-Computer Interfaces (BCIs) to promote communication or functional mobility restoration (Wolpaw et al., 2002; Birbaumer, 2006).

    View all citing articles on Scopus
    View full text