Do mirror neuron areas mediate mu rhythm suppression during imitation and action observation?

https://doi.org/10.1016/j.ijpsycho.2013.05.019Get rights and content

Highlights

  • Mirror neuron activity is thought to mediate mu suppression but evidence is lacking.

  • Sequential EEG–fMRI correlates electrophysiology to BOLD signal without MR-artefact.

  • Mu suppression modulates activity in motor preparation and attention brain areas.

  • Mu rhythm suppression is not specific to activation of the mirror neuron system.

Abstract

Mu rhythm is an EEG measure of resting motor neurons, which is normally suppressed by input because of action observation or movement execution. This characteristic has caused mu suppression to be used as proxy marker for mirror neuron activation. However, there is little direct evidence that fluctuations in mu rhythm suppression reflect concurrent fluctuations in mirror neuron activity. A manual imitation paradigm was used to look at correlations between mu rhythm and BOLD response, by recording sequential EEG and fMRI measures to allow within-subject correlation analyses. Participants were instructed to imitate or observe actions involving the movement of a handle with their right hand. Mu power modulation, defined as mu power changes between conditions, correlated negatively with BOLD response in right inferior parietal lobe, premotor cortex and inferior frontal gyrus; putative mirror neuron areas. Clusters were also identified in bilateral cerebellum, left medial frontal gyrus, right temporal lobe and thalamus. This suggests that mu suppression involves a range of structures that modulate motor preparation activities and are sensitive to visual input, including but not restricted to the human analogue of the mirror neuron system.

Introduction

Mu rhythm is a frequency measured using electroencephalography (EEG) that has been studied since 1950s. Mu waves are detected in the 8–13 Hz frequency range and are thought to be the result of synchronous discharges by resting neurons in the sensorimotor area of the brain, usually measured over the somatosensory cortex (e.g. Kuhlman, 1978, Anderson and Ding, 2011). Suppression occurs when these neurons receive input, particularly during motor act preparation (Pfurtscheller et al., 2006). Further to this, it has been demonstrated that observation of an action causes mu suppression, though to a lesser degree than motor activity (Cochin et al., 1999). This includes undirected movements (Muthukumaraswamy and Johnson, 2004), moving robot hands (Oberman et al., 2007), and point-light stimuli showing biological motion (Ulloa and Pineda, 2007). Rorschach cards that imply movement create a larger amount of suppression than cards without implied movement (Giromini et al., 2010). Researchers have also found an effect of anticipatory spatial attention on pre-stimulus mu rhythm in the contralateral hemisphere for a somatosensory task, further suggesting that mu suppression plays a role in task preparation as well as execution (Anderson and Ding, 2011). Although this broader suppression effect indicates a general role for mu rhythm suppression, results have previously been taken as evidence that the degree of mu wave suppression may serve as proxy marker for the sensitivity of the motor system to action observation. It is thought that a subset of neurons known as mirror neurons is responsible for this sensitivity.

Mirror neurons, which are active during both the observation and execution of the same action, are thought to be closely connected to the electrophysiological mu suppression signal. This subset of neurons was first observed using single-cell recordings in the ventral premotor cortex (F5) region of macaques (DiPellegrino et al., 1992). Other macaque mirror neuron areas include the inferior parietal lobule (in particular the prefrontal gyrus but also intraparietal areas) and the prefrontal cortex (Rizzolatti and Sinigaglia, 2010). Demonstrating the presence of mirror neurons in humans is challenging, as mirror neurons account for only a small percentage of the overall neurons in any brain region. Some success has been achieved using transcranial magnetic stimulation (TMS; Fadiga et al., 1995, Gangitano et al., 2004) and electromyography (EMG; Cattaneo et al., 2007). Much work has relied on functional Magnetic Resonance Imaging (fMRI) to capture the Blood Oxygen Level Dependent (BOLD) signal thought to reflect mirror neuron activity. FMRI has enabled researchers to discover patterns consistent with mirror neuron activation, indicating a wide range of regions. Some studies have used computational analysis methods on MRI data to try to get a more detailed idea of where mirror neurons are located (Kilner et al., 2009, Oosterhof et al., 2010). Research has implicated the inferior parietal lobe (Rizzolatti and Craighero, 2004), Broca's area (located in the left inferior frontal gyrus; Kohler et al., 2002), the premotor cortex (Gallese et al., 2004), supplementary motor areas (Iacoboni and Dapretto, 2006), and possibly the insula (Gallese et al., 2004), with other regions of the human brain currently under investigation. Mirror neurons can be broadly congruent, focusing only on the goal, or strictly congruent, firing only when an observation matches exactly to the same action (Gallese et al., 1996).

Mirror neurons are posited to reside in or connect to most of the brain, working together with other types of neurons to enable not just vicarious action–excitation but also vicarious emotions and sensations to be experienced (Keysers and Gazzola, 2009). For example, the somatosensory cortex works together closely with the putative mirror neuron areas, contributing information on touch (Keysers et al., 2004) and maintaining a self-other distinction (Avikainen et al., 2002). However, because the BOLD signal is an indirect measure of neuronal activity it cannot be concluded from fMRI research that a higher BOLD signal in a region during both observation and execution occurs because the same neurons are firing, only that the same voxels are experiencing an increase in blood flow. Some researchers argue that mirror neurons simply reflect motor preparation, and that they do not encode the meaning of actions (Hickock, 2009). Others have argued that the neural match between action and observation is a matter of associative learning (e.g. Catmur et al., 2009). The majority of research however supports the existence of an observation–execution-matching mechanism and its use in action understanding, including tentative results from human single-cell recordings (Mukamel et al., 2010).

Mirror neurons and mu suppression react in similar ways to perceived action stimuli, and so researchers have suggested “that mu wave suppression to observed actions can be used as a selective measure of activity of this [mirror neuron] system” (Oberman et al., 2007, p. 2195). However, despite promising findings it remains unclear as to whether or not this is the case. Although the largest mu suppression effect occurs during goal-directed actions, which is consistent with what we know about mirror neuron activity, it is not clear that mu suppression variability is specifically linked to fluctuations in mirror neuron activity. Furthermore, activation in mirror neuron areas does not always occur in the same way as mu suppression, an issue that might be confounded by the use of diverging experimental paradigms and stimuli in fMRI and EEG research.

Recently, research has sought to determine whether mu suppression provides an accurate measure of mirror neuron activity, as has so often been claimed. Perry and Bentin (2009) used an fMRI paradigm that had previously activated mirror neuron areas during observation and execution to collect EEG data, to see if they could find a correlation between their measure of mu rhythm suppression and previously obtained fMRI measures of mirror neuron activity. Though they found a significant correlation, this only provides evidence of an indirect relationship, as Perry and Bentin did not correlate measures within subjects. More recently, Arnstein et al. (2011) employed a simultaneous EEG–fMRI design to correlate activity in mirror neuron areas with mu suppression by analysing the conjunction between multiple observation and execution tasks, performed both in- and outside the MR-scanner. They found voxels activated during both observation and execution in the inferior parietal lobe, dorsal premotor cortex and somatosensory cortex, though not in the inferior frontal gyrus, and concluded that not all mirror neuron areas strictly relate to mu rhythm suppression. The only other simultaneous EEG–fMRI study previously performed (Mizuhara and Inui, 2010) mainly calls for caution in making definitive statements about a possible correlation, highlighting the possible role of movement confounds from areas beyond the somatosensory cortex, where mu suppression is measured. Yet researchers have been conducting research into mirror neurons using only mu rhythm measurements long before these comparison studies existed (e.g. Muthukumaraswamy et al., 2004).

The main aim of this study was to examine whether mu rhythm fluctuation during imitation and action observation predicted activity in mirror neuron areas measured by fMRI, using a paradigm and method of data analysis that differs substantially from previous combined mu suppression — mirror neuron research. We also sought to discover whether activity in other brain areas might correlate with mu suppression. To address these questions, a sequential EEG–fMRI design was used, which enables the recording of neurological and electrophysiological measurements of the same individual within the same environment. We hypothesised that changes in mu power concurrent with task demands would correlate negatively with BOLD signal in putative mirror neuron areas.

Section snippets

Participants

Sixteen right-handed males took part in the study, with no history of illnesses that could affect the brain. Age ranged from 19 to 43, with a mean of 26.7 (SD: 7.19). All participants gave written consent, with ethical approval given by the University of Aberdeen ethics review board.

EEG

EEG data was collected using a Brain Products (Gilching, Germany) BrainAmp MR plus 64-channel fMRI compatible EEG system with BrainVision Recorder (version 1.10). Electrode-skin impedance was limited to below 20 kΩ.

Results

This study aimed to test the hypothesis that mu power suppression measured over the somatosensory cortex during action and action–observation would correlate with changes in BOLD response in mirror neuron areas during imitation and observation. We chose to exclude one participant due to an unalterable shift in their functional MR-images and non-compliance in the handle-move condition. Hereafter “mu power” relates to the voltage calculated from the Fast Fourier Transform analysis of the EEG time

Discussion

Our initial hypothesis predicted that the amount of mu rhythm suppression would correlate with increased BOLD response during imitation and observation in those areas that are responsible for producing mu suppression. The role that some researchers (e.g. Oberman et al., 2007, Ulloa and Pineda, 2007) believe mirror neuron areas play in mu suppression was not found in the whole brain analyses. However, the modulation analysis, which looked at the co-variance between mu power and BOLD signal over

Acknowledgements

Research conducted as part of LB's MSc, overseen by Dr. David Turk and Professor Neil Macrae. Dr. Douglas Potter and Cui Fang gave advice on EEG analysis; Dr. Potter also provided much welcome feedback on this article. The task was run with the help of Gordon Buchan and a team of radiographers. GW and JHGW are members of SINAPSE (www.sinapse.ac.uk), a pooling initiative funded by the Scottish Funding Council and the Chief Scientist Office of the Scottish Executive, who also originally purchased

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    Present address: Aberdeen Biomedical Imaging Centre, University of Aberdeen, Lilian Sutton Building, Foresterhill, Aberdeen AB25 2ZD, UK.

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