Research ReportDynamics of the EEG power in the frequency and spatial domains during observation and execution of manual movements
Introduction
The existence of neurons that fire both during the execution and during the observation of a motor act provides strong evidence for a neural-based functional link between perception and action (for a review see Rizzolatti and Sinigaglia, 2010). Such neurons were found in the ventral premotor cortex (F5) and the anterior intra-parietal sulcus (aIPS) of the macaque monkey (di Pellegrino et al., 1992, Fogassi et al., 2005). More recently, studies reported the existence of such neurons in humans based on functional brain imaging (fMRI; Buccino et al., 2004; for reviews see Fabbri-Destro and Rizzolatti, 2008, Morin and Grezes, 2008), transcranial magnetic stimulation (TMS; Fadiga et al., 1995), electroencephalography (EEG; Cochin and Martineau, 1998, Perry and Bentin, 2009; for a review see Pineda, 2005), magneto-encephalography (MEG; Hari et al., 1998; for a review see Hari, 2006) and single-cell recordings (Mukamel et al., 2010). The human mirror-neuron system (hMNS) was shown primarily in the triangle linking the inferior frontal cortex, the superior temporal sulcus (STS) and the anterior intraparietal sulcus (aIPS) (e.g., Iacoboni and Dapretto, 2006), or extended to also include limbic structures and other cortical regions (e.g., Gazzola and Keysers, 2009; for a recent meta-analysis see Molenberghs et al., 2012).
The hMNS has been implicated in many human abilities that involve the interaction with others (for reviews see Rizzolatti and Craighero, 2004, Rizzolatti and Sinigaglia, 2010) such as imitation (Iacoboni, 2005, Iacoboni et al., 1999) and speech perception (Rizzolatti and Arbib, 1998). Furthermore, by implicitly simulating the other's actions, the hMNS is assumed to facilitate the understanding of the other's intentions (Blakemore and Decety, 2001, Iacoboni et al., 2005) and emotions (Dapretto et al., 2006, Schulte-Ruther et al., 2007). Consequently, it is proposed that the hMNS is involved in the formation of social skills (Gallese, 2007, Gallese, 2008) as well as the basis for empathy (Hooker et al., 2010, Molnar-Szakacs, 2011; for an alternative view see Decety, 2010). Finally, the hMNS has also been implicated in motor learning (Stefan et al., 2008), and is presumed to play a key role in the evolution of language (Arbib, 2005, Corballis, 2010).
The EEG manifestation that has been associated with the hMNS is the reduction of power in the alpha range (8–12 Hz) over the sensorimotor cortex immediately prior or concomitant with motor activity. This phenomenon has been labeled mu suppression (Pfurtscheller and Berghold, 1989). It is generally accepted that it reflects an event-related desynchronization (ERD) during the performance of a motor task, which is a reliable marker of excitation of neural networks involved in that task (Goldman et al., 2002; for a review, see Pineda, 2005). The distribution of this ERD across the scalp is thought to be determined by the brain systems that are activated during task performance. Hence, mu suppression may partially reflect the activity of the motor system (e.g., Pfurtscheller et al., 1997). The association of this neural manifestation to the hMNS is suggested by studies showing that mu rhythms are suppressed not only during motor execution but also during observation of an action performed by another person. This mirror-like property of neuronal activation is parallel to the basic feature of the MNS found in monkeys using single-cell recordings in cortical areas (for a review see Pineda, 2005).
Despite the recent proliferation of mu suppression studies, there are several basic characteristics of this phenomenon that still require additional investigation. For example, it is not entirely clear how mu suppression distributes over the scalp. Since mu suppression is assumed to reflect primarily motor activity and because mirror neurons in the monkey have been found primarily in premotor and parietal areas, it has been hypothesized that mu suppression indexes downstream modulation of primary sensorimotor neurons by mirror neurons' activity (Muthukumaraswamy et al., 2004). Therefore, many studies that reported the effect of action observation on the modulation of the 8–12 Hz frequency band, focused only on activity recorded from C3 and C4 electrodes placed over the sensorimotor cortex (Oberman et al., 2005, Oberman et al., 2008, Perry and Bentin, 2009, Woodruff and Maaske, 2010). Indeed, Oberman et al., 2005, Oberman et al., 2008 did not find a consistent pattern of mu suppression at other scalp sites. However, as mentioned above, many studies suggest that the hMNS includes regions extending also into the limbic system and temporal lobes. Indeed, several authors reported EEG suppression in the alpha/mu frequency range also at frontal (Cochin and Martineau, 1998, Perry et al., 2010), parietal (Cochin et al., 1998, Cochin and Martineau, 1998, Orgs et al., 2008) and occipital sites (Perry and Bentin, 2010, Perry et al., 2011), which calls for a more thorough investigation of the distribution of this phenomenon across the scalp.
Another aspect of mu suppression that awaits further investigation is the determination of the frequency band that maximizes the manifestation of the hMNS. Whereas it is generally accepted that at rest the EEG synchronizes within the 8–12 Hz range (for a review see Pfurtscheller et al., 1996), several studies that investigated the ERD of these “idling rhythms” focused on narrow frequencies bands (Cochin and Martineau, 1998, Pfurtscheller and Berghold, 1989, Pfurtscheller et al., 2000). For example, Pfurtscheller et al. (2000) analyzed separately mu suppression in the low-alpha range (8–10 HZ) and the high-alpha range (10–12 Hz), prior and during hand and foot movements. They found that in the low range, mu suppression is largely distributed across the somatosensory cortex while its distribution in the high range is more limited and seems to reflect the activity of the limb that actually moves. A focus on even narrower frequency ranges is evident in studies where the specific frequency at which mu suppression was maximal has been selected for each subject separately (Khulman, 1978, Muthukumaraswamy and Johnson, 2004, Muthukumaraswamy et al., 2004, Stancak and Pfurtscheller, 1996, Streltsova et al., 2010). For example, Khulman (1978) found 10.1 Hz to be the mean frequency (across subjects) at which the ERD was maximal during manual execution. Using a similar selection procedure, Stancak and Pfurtscheller (1996) found that the mean frequency at which ERD is maximal prior and during finger movements is 9.8 Hz and 10.1 Hz in right- and left-handed participants, respectively. Whereas such studies are not available in the action–perception literature, several studies distinguished between higher and lower alpha ranges, reporting higher suppression in the low-range during action observation (e.g., Perry et al., 2010). The above findings suggest that considering the modulation of EEG in the 8–12 Hz frequency range as the exclusive and integrated manifestation of the hMNS might be too simplistic, and that this phenomenon requires a more systematic investigation.
In order to address the above issues, we decided to examine the spatial distribution of EEG desynchronization in narrow frequency-bands, covering the entire alpha range and the surrounding frequencies, during execution and observation of manual movements.
Finally, since in daily life the actions of others are observed from different viewpoints, we compared the EEG modulation induced by observation of motor actions from allocentric (i.e., facing the actor) and egocentric viewpoints (i.e., seeing the actor from behind). Note that whereas the actor's right and left corresponds with the observer's right and left hands in the egocentric perspective condition, the relationship is reversed in the allocentric condition. This analysis was motivated by inconsistency in current literature with respect to the response magnitudes when comparing these two perspectives (Alaerts et al., 2009, Maeda et al., 2002). Following Perry and Bentin (2009) we hypothesized that observing unilateral upper-limb actions from an egocentric viewpoint would elicit bilateral suppression with a greater magnitude in the contralateral hemisphere (i.e., greater suppression in the left hemisphere during observation of right upper limb movements from an egocentric perspective, and vice versa). In contrast, observing the same actions from an allocentric viewpoint was hypothesized to elicit greater suppression in the ipsilateral hemisphere (i.e., greater suppression in the right hemisphere during observation of the right-hand movement, and vice versa). Tentative support for this hypothesis comes from MEG and fMRI studies (Kilner et al., 2009, Shmuelof and Zohary, 2008) although other studies found a more or less symmetric activity across hemispheres (Molnar-Szakacs et al., 2006).
Section snippets
Suppression patterns in the frequency and spatial domains
Since action-observation related desynchronization was reported previously in frequencies lower than the traditional alpha range (Cochin et al., 2001, Martineau et al., 2008), we systematically explored the magnitude of desynchronization in discrete frequencies within and also adjacent to the alpha range. The EEG suppression indices reflecting the modulation of 4–12 Hz (alpha/mu and theta ranges) at each site of interest and in each experimental condition are presented in the supplementary
Discussion
The aim of this study was to explore the spatial extent and the frequency range of EEG desynchronization patterns thought to reflect the activation of the hMNS. We investigated the degree to which various discrete frequency bands within the traditional mu range (8–12 Hz) and outside this range are modulated during execution and observation of movement. EEG modulation in each condition was recorded at different sites over the cortical mantle with an emphasis on comparison between sites close to
Participants
The sample included 29 participants (15 male) ranging in age from 25 to 75 years (mean age=55.34, SD=11.88; 83% over 50 years old). The relatively large age-range was determined by matching the current sample of healthy participants with a group of stroke patients who participated in a different study. All participants were right-handed, reported normal or corrected-to-normal visual acuity, and had no history of psychiatric or neurological disorders. They signed an informed consent approved by
Acknowledgments
This research project was carried out by the first author in partial fulfillment of the requirements for the PhD degree at the Sackler Faculty of Medicine - Tel Aviv University, under the supervision of Shlomo Bentin, Dario G. Liebermann and Nachum Soroker. We dedicate the paper in memory of Professor Shlomo Bentin, who recently passed away in a tragic accident. We wish to thank the participants for their cooperation in the experiment. This research was partially funded by the Legacy Foundation
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Shlomo Bentin passed away on July 13th 2012.