Mirror-neuron system recruitment by action observation: Effects of focal brain damage on mu suppression
Introduction
Execution of a motor act and observation of that act performed by others, have been found to activate a common neural substrate. This was first demonstrated in cortical neurons of macaque monkeys, hence termed “mirror neurons” (for a review see Rizzolatti and Sinigaglia, 2010). Neurons with mirror-like properties were found primarily in the ventral premotor cortex (F5) and around the anterior intra-parietal sulcus (aIPS) of the macaque (di Pellegrino et al., 1992, Fogassi et al., 2005). More recently, studies suggested 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), single-unit recording (Mukamel et al., 2010), magneto-encephalography (MEG; for a review see Hari, 2006) and electroencephalography (EEG; Cochin et al., 1999, Muthukumaraswamy et al., 2004, Perry and Bentin, 2009; for a review see Pineda, 2005). The human MNS (hMNS) is thought to reside in a network comprised of the inferior frontal gyrus (IFG), the anterior part of the inferior parietal lobule (aIPL) and the ventral premotor cortex, with the possible addition of cortical regions such as the superior parietal lobule (SPL) (e.g., Caspers et al., 2010, Filimon et al., 2007, Gazzola and Keysers, 2009, Gazzola et al., 2007, Grezes et al., 2003, Keuken et al., 2011, Molenberghs et al., 2012). The extensive hMNS research in the last two decades has been motivated by the alleged importance of this system in action understanding (Rizzolatti and Craighero, 2004, Rizzolatti and Sinigaglia, 2010), imitation (Iacoboni, 2005, Iacoboni et al., 1999), motor learning (Stefan et al., 2008), speech perception (Rizzolatti and Arbib, 1998), language development (Arbib, 2005, Corballis, 2010, Gallese, 2008), and formation of key social skills such as understanding the intentions (Blakemore and Decety, 2001, Iacoboni et al., 2005) and the emotional state of others (Dapretto et al., 2006, Gallese, 2007, Schulte-Ruther et al., 2007).
EEG research typically quantifies the assumed hMNS activity by focusing on mu rhythms, which are EEG oscillations within the alpha range (8-12 Hz), measured over the sensorimotor regions. The EEG power in this range is reduced during the execution of a motor action (Pfurtscheller and Berghold, 1989) and also during observation of a similar action performed by another person (Muthukumaraswamy et al., 2004, Perry and Bentin, 2009; for a review see Pineda, 2005, Woodruff and Maaske, 2010). This characteristic led researchers to assume that mu suppression represents the recruitment of a hMNS, since this dual activation mode reflects the basic property of the monkeys’ mirror neurons (for a review see Pineda, 2005). However, the specificity of the suppression phenomenon (i.e., being related to a mirror mechanism) is far from being clear in light of the difficulty to pinpoint EEG sources and the difficulty to dissociate between the alpha and mu suppression phenomena during action observation.
Alpha and mu suppression are measured in the same EEG frequency range (8-12 Hz). Alpha rhythms are desynchronized in association with visual stimulation and during processing that involves attention and memory, especially over the occipital cortex (Khulman, 1978, Klimesch, 1997, Klimesch et al., 2007). In contrast, mu rhythms are desynchronized typically during execution of movement, most prominently over the sensorimotor cortex (Andrew and Pfurtscheller, 1997, Khulman, 1978, Perry et al., 2011; for a review see Pineda, 2005). In the case of action observation (a visual processing activity related to viewing biological movement) the suggested distinction between alpha and mu is not trivial, and the cortical distribution of suppression patterns showed inconsistencies. Several recent studies found a widespread suppression across the scalp and even greater suppression at occipital sites than at central sites (Perry and Bentin, 2010, Perry et al., 2010, Perry et al., 2011), whereas other studies found suppression to manifest predominantly at central sites (Frenkel-Toledo et al., 2013, Oberman et al., 2005, Oberman et al., 2008). Perry and Bentin (2010) suggested that the suppression seen in anterior sites might also reflect the recruitment of attention resources needed for task performance rather than a ‘simulation mechanism’. It is clear that suppression patterns depend, to a large extent, on the exact definition of the task subjects are required to perform with respect to the observed movements. Given this inconsistency in earlier research, the fact that both alpha and mu suppression phenomena are measured in the same frequency range and the low spatial resolution of EEG recording, additional evidence is needed to corroborate the notion that mu suppression denotes activation specific to a hMNS.
The relation between mu event-related desynchronization (ERD) and manual motor activity is supported also by a small number of studies conducted in stroke patients. Pfurtscheller et al. (1980) found in two of five stroke patients with mild hemiparesis reduced alpha ERD over the affected hemisphere during voluntary movement of both the paretic and the non-paretic hand, compared to the ERD recorded over the unaffected hemisphere. In a different study, the same research group described a reduced response of the alpha/mu ERD over the affected hemisphere not only during hand movement but also during speech (Pfurtscheller et al., 1984). Platz et al. (2000) found in three patients with somatosensory deficits (without overt paresis) reduced alpha/mu ERD at central sites during both preparation and execution of movements with the affected upper limb. Pfurtscheller et al. (1981) and recently Stepien et al. (2011) found that patients with cortical stroke show an inter-hemispheric central alpha ERD asymmetry during both the paretic and non-paretic hand movement, with attenuation of the ERD over the affected hemisphere, whereas patients with subcortical stroke tend to show a symmetric alpha/mu ERD.
The aforementioned findings in stroke patients corroborate the notion that alpha/mu ERD marks the recruitment of cortical neurons involved in movement execution. Demonstration that ERD in the 8-12 Hz range is affected by cortical lesions also during action observation would support a more specific linkage between mu suppression and activation of a hMNS. Thus, we examined here the degree to which the 8-12 Hz frequency range is modulated during observation of movement in stroke patients with damage to different parts of the brain. Our hypothesis was that if mu suppression during action observation reflects hMNS activity, its magnitude in the affected hemisphere (recorded from electrodes placed over the sensorimotor areas) will be lower relative to the unaffected hemisphere, similarly to the effect of unilateral cortical stroke on execution-related suppression (Pfurtscheller et al., 1980, Pfurtscheller et al., 1981, Pfurtscheller et al., 1984, Platz et al., 2000, Stepien et al., 2011). Moreover, based on earlier research concerning the cortical location of the putative hMNS (Arnstein et al., 2011, Caspers et al., 2010, Gazzola and Keysers, 2009, Gazzola et al., 2007, Keuken et al., 2011, Molenberghs et al., 2012; for a review see Rizzolatti and Sinigaglia, 2010), we assumed that the extent of damage within the posterior parietal cortex (IPL, SPL), the inferior frontal gyrus (IFG) and the ventral premotor cortex would correlate with the magnitude of mu-suppression in patients with stroke (the greater the damage is, the less suppression is expected). Based on previous (Marshall et al., 2009, Perry et al., 2010) and on our recent findings (Frenkel-Toledo et al., 2013) that showed that action observation affects the lower mu range (8-10 Hz) more than the upper range (10-12Hz), we expected the above effect of cortical damage to be shown mainly in the lower range.
Section snippets
Participants
Thirty-eight first-incident stroke patients (22 males) ranging in age from 24 to 76 years (mean and standard deviation: 55.4 ± 13.7 years) participated in this study. The patients were recruited during their hospitalization at the Loewenstein Rehabilitation Hospital (LRH), Ra'anana, Israel. Time after stroke onset till admission to the study ranged between 23 and 132 days (mean and standard deviation: 58.7 ± 29.7 days). Patients were included in the study only if they did not suffer from psychiatric or
The effect of uni-hemispheral damage on mu suppression
Normal group distribution of data was found for the suppression indices in all the experimental conditions using Kolmogorov–Smirnov tests. Our analysis was aimed at comparing the EEG suppression induced by action observation in the affected and unaffected hemispheres, in central versus occipital sites, in the low (8-10 Hz) and high (10-12 Hz) mu ranges. The suppression index (averaged across the different viewing perspectives; see Methods) was analyzed using a four-way ANOVA with repeated
Discussion
The goal of this study was to explore further the connection between mu suppression and activation of the hMNS. Investigation of the specificity of this connection is important because if a specific relationship is demonstrated, mu suppression could be used more reliably as an electrophysiological marker of hMNS recruitment in various cognitive and motor activities (e.g., Marshall et al., 2009, Perry et al., 2011, Woodruff and Maaske, 2010, Woodruff et al., 2011). We examined how damage to
Acknowledgments
This research project was carried out by the first author in partial fulfillment of the requirements for a PhD degree at the Sackler Faculty of Medicine, Tel-Aviv University, under the supervision of Nachum Soroker, Dario G. Liebermann and Shlomo Bentin. This research was partially funded by the Legacy Foundation granted through the Loewenstein Rehabilitation Hospital, the Rivka Necht Foundation, the Stanley Steyer School of Health Professions of the Sackler Faculty of Medicine, Tel-Aviv
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Shlomo Bentin passed away on July 13th 2012.