Do mirror neuron areas mediate mu rhythm suppression during imitation and action observation?
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
References (46)
- et al.
Attentional modulation of the somatosensory mu rhythm
Neuroscience
(2011) - et al.
Modulated activation of the human SI and SII cortices during observation of hand actions
NeuroImage
(2002) - et al.
EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder
Brain and Cognition
(2007) - et al.
ALE meta-analysis of action observation and imitation in the human brain
NeuroImage
(2010) - et al.
A unifying view of the basis of social cognition
Trends in Cognitive Sciences
(2004) - et al.
The feeling of movement: EEG evidence for mirroring activity during the observation of static, ambiguous stimuli in the Rorschach cards
Biological Psychology
(2010) - et al.
Expanding the mirror: vicarious activity for actions, emotions, and sensations
Current Opinion in Neurobiology
(2009) - et al.
A touching sight: SII/PV activation during the observation and experience of touch
Neuron
(2004) Functional topography of the human mu rhythm
Electroencephalography and Clinical Neurophysiology
(1978)- et al.
Single-neuron responses in humans during execution and observation of actions
Current Biology
(2010)
Mu rhythm modulation during observation of an object-directed grasp
Cognitive Brain Research
EEG evidence for mirror neuron dysfunction in autism spectrum disorders
Cognitive Brain Research
EEG evidence for mirror neuron activity during the observation of human and robot actions: toward an analysis of the human qualities of interactive robots
Neurocomputing
Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: the mirror neuron hypothesis
Neuropsychologia
Mirror activity in the human brain while observing hand movements: a comparison between EEG desynchronization in the mu-range and previous fMRI results
Brain Research
Mu rhythm (de)synchronization and EEG single-trial classification of different motor imagery tasks
NeuroImage
Tool perception suppresses 10–12 Hz μ rhythm of EEG over the somatosensory area
Biological Psychology
EEG study of the mirror neuron system in children with high functioning autism
Brain Research
Brain lateralization of motor imagery: motor planning asymmetry as a cause of movement lateralization
Neuropsychologia
Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes
Cognitive Brain Research
Recognition of point-light biological motion: Mu rhythms and mirror neuron activity
Behavioural Brain Research
Imitation, mirror neurons and autism
Neuroscience and Biobehavioral Reviews
Mu-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal and somatosensory cortices
Journal of Neuroscience
Cited by (102)
Mirror neurons, neural substrate of action understanding?
2022, EncephaleEEG measures of sensorimotor processing and their development are abnormal in children with isolated dystonia and dystonic cerebral palsy
2021, NeuroImage: ClinicalCitation Excerpt :The ERD is usually followed by a rebound in mu activity (ERS), which in the past was thought to reflect an “idling” rhythm, but is more recently considered to reflect active inhibition of the motor network or a resetting of the sensorimotor system ready for subsequent activities (Pineda, 2005; Demas et al., 2019; Gaetz et al., 2010, 2011). Modulation of mu activity also occurs during observation of a movement and is therefore considered to reflect activity within the human mirror neuron system (Cannon et al., 2014; Fox et al., 2016; Braadbaart et al., 2013; Lepage and Theoret, 2006; Woodruff and Klein, 2013). However, the degree of mu suppression is greater when the observed action is goal-orientated (Lepage and Theoret, 2006) or when observing a movement performed live rather than on video (Ruysschaert et al., 2013), and active movement leads to greater mu desynchronisation than observed motor activity (Cannon et al., 2014).
- 1
Present address: Aberdeen Biomedical Imaging Centre, University of Aberdeen, Lilian Sutton Building, Foresterhill, Aberdeen AB25 2ZD, UK.