Mu-Suppression Neurofeedback Training Targeting the Mirror Neuron System: A Pilot Study.

Neurofeedback training (NFT) is a promising adjuvant intervention method. The desynchronization of mu rhythm (8-13 Hz) in the electroencephalogram (EEG) over centro-parietal areas is known as a valid indicator of mirror neuron system (MNS) activation, which has been associated with social skills. Still, the effect of neurofeedback training on the MNS requires to be well investigated. The present study examined the possible impact of NFT with a mu suppression training protocol encompassing 15 NFT sessions (45 min each) on 16 healthy neurotypical participants. In separate pre- and post-training sessions, 64-channel EEG was recorded while participants (1) observed videos with various types of movements (including complex goal-directed hand movements and social interaction scenes) and (2) performed the "Reading the Mind in the Eyes Test" (RMET). EEG source reconstruction analysis revealed statistically significant mu suppression during hand movement observation across MNS-attributed fronto-parietal areas after NFT. The frequency analysis showed no significant mu suppression after NFT, despite the fact that numerical mu suppression appeared to be visible in a majority of participants during goal-directed hand movement observation. At the behavioral level, RMET accuracy scores did not suggest an effect of NFT on the ability to interpret subtle emotional expressions, although RMET response times were reduced after NFT. In conclusion, the present study exhibited preliminary and partial evidence that mu suppression NFT can induce mu suppression in MNS-attributed areas. More powerful experimental designs and longer training may be necessary to induce substantial and consistent mu suppression, particularly while observing social scenarios.

Motor-related cortical oscillations distinguish one's own from a partner's contributions to a joint action.

The ability to distinguish between one's own and others' actions is a requirement for successful joint action. Such a distinction might be supported by dissociable motor activity underlying each partner's individual contributions to the joint action. However, little research has directly compared motor activity associated with one's own vs. others' actions during joint action. The current study investigated whether motor-related cortical oscillations distinguish between self- and partner-produced actions when partners take turns producing taps to meet a joint timing goal. Across two experiments, the degree of beta suppression differentiated one's own from a partner's actions, with more suppression occurring during one's own actions than during a partner's actions. Self-partner differences in mu suppression were also evident, particularly when partners produced actions in succession. Increased beta suppression was also observed during partners' actions when they were followed by one's own actions, suggesting that the coordination demands imposed by the joint action could affect the pattern of beta reactivity during a turn-taking joint action. Together, these findings demonstrate that dynamic patterns of motor activity underpin successful joint action and that periods of distinct motor activity are associated with one's own contributions to a joint action.

Live vs video interaction: sensorimotor and visual cortical oscillations during action observation.

Increasingly, in the field of communication, education, and business, people are switching to video interaction, and interlocutors frequently complain that the perception of nonverbal information and concentration suffer. We investigated this issue by analyzing electroencephalogram (EEG) oscillations of the sensorimotor (mu rhythm) and visual (alpha rhythm) cortex of the brain in an experiment with action observation live and on video. The mu rhythm reflects the activity of the mirror neuron system, and the occipital alpha rhythm shows the level of visual attention. We used 32-channel EEG recorded during live and video action observation in 83 healthy volunteers. The ICA method was used for selecting the mu- and alpha-components; the Fourier Transform was used to calculate the suppression index relative to the baseline (stationary demonstrator) of the rhythms. The main range of the mu rhythm was indeed sensitive to social movement and was highly dependent on the conditions of interaction-live or video. The upper mu-range appeared to be less sensitive to the conditions, but more sensitive to different movements. The alpha rhythm did not depend on the type of movement; however, a live performance initially caused a stronger concentration of visual attention. Thus, subtle social and nonverbal perceptions may suffer in remote video interactions.

Neural, physiological and behavioural correlates of empathy for pain in Tourette syndrome.

Persons with Tourette syndrome show altered social behaviours, such as echophenomena and increased personal distress in emotional situations. These symptoms may reflect an overactive mirror neuron system, causing both increased automatic imitation and a stronger tendency to share others' emotions. To test this, we measured the individual level of echophenomena with a video protocol and experimentally induced empathy for pain in 21 participants with Tourette syndrome and 25 matched controls. In the empathy for pain paradigm, pictures of hands and feet in painful or neutral situations were presented, while we measured participants' EEG and skin conductance response. Changes in somatosensory mu suppression during the observation of the pictures and pain ratings were compared between groups, and correlations were calculated with the occurrence of echophenomena, self-reported empathy and clinical measures. Our Tourette syndrome sample showed significantly more echophenomena than controls, but the groups showed no behavioural differences in empathic abilities. However, controls, but not patients with Tourette syndrome, showed the predicted increased mu suppression when watching painful compared to neutral actions. While echophenomena were present in all persons with Tourette syndrome, the hypothesis of an overactive mirror neuron system in Tourette syndrome could not be substantiated. On the contrary, the Tourette syndrome group showed a noticeable lack of mu attenuation in response to pain stimuli. In conclusion, we found a first hint of altered processing of others' emotional states in a brain region associated with the mirror neuron system.

Does Tactile Stimulation of the Face Affect the Processing of Other Faces? Neural and Behavioural Effects of Facial Touch.

The integration of vision and touch is proposed as a critical factor for processing one's own body and the bodies of others in the brain. We hypothesize that tactile stimulation on an individual's face may change the ability to process the faces of other, but not the processing of other visual images. We aimed to determine if facial touch increased the activity of the mirror system and face recognition memory of the observer. Therefore, mu suppression was measured to compare the effect of facial touch in performing two visual tasks. The participants observed faces and non-face visual images under two sets of conditions. In the first condition, a robotic finger touched the participant's cheek while in the second condition, no touch occurred. Upon each observational task, the participants were given in a recognition test. Behavioral results indicated that facial touch improved recognition performance for faces, but not for non-face visual images. Tactile stimulation increased mu suppression in both occipital and central electrodes during face processing; however, the suppression did not significantly change during non-face visual processing. Our findings support the concept that the brain uses a self-body representation, as a reference to understand the mental states or behaviors of others.

An examination of mindfulness on Mu suppression and pain empathy and its relation to trait empathy.

There have been multiple benefits reported from the practice of mindfulness meditation. Recently social functioning, including empathy, has emerged as one such possible benefit. However, the literature is mixed and it is unknown if mindfulness has an effect on the neural mechanism involved in empathy. Therefore, we conducted a large-scale experimental study involving over 100 participants that were either enrolled in a behavioral or EEG experiment to examine pain empathy and mu suppression, respectively. We also measured state and trait mindfulness and trait empathy. Results did not show a change in pain empathy or mu suppression in response to an acute mindfulness manipulation. However, pain empathy responses were able to be predicted significantly better when the component of state mindfulness involving decentering was incorporated into a regression model compared to trait empathy alone. Also, trait empathy was related to trait mindfulness. Collectively, state decentering may be involved in increased pain empathy, while trait mindfulness appears more related to general trait empathy. Further research is warranted to better understand the potential benefit a brief mindfulness meditation may produce in the realm of brain activity and social functioning.

Down and up! Does the mu rhythm index a gating mechanism in the developing motor system?

Developmental research on action processing in the motor cortex relies on a key neural marker - a decrease in 6-12 Hz activity (coined mu suppression). However, recent evidence points towards an increase in mu power, specific for the observation of others' actions. Complementing the findings on mu suppression, this raises the critical question for the functional role of the mu rhythm in the developing motor system. We here discuss a potential solution to this seeming controversy by suggesting a gating function of the mu rhythm: A decrease in mu power may index the facilitation, while an increase may index the inhibition of motor processes, which are critical during action observation. This account may advance our conception of action understanding in early brain development and points towards critical directions for future research.

Peak frequency of the sensorimotor mu rhythm varies with autism-spectrum traits.

Autism spectrum disorder (ASD) is a neurodevelopmental syndrome characterized by impairments in social perception and communication. Growing evidence suggests that the relationship between deficits in social perception and ASD may extend into the neurotypical population. In electroencephalography (EEG), high autism-spectrum traits in both ASD and neurotypical samples are associated with changes to the mu rhythm, an alpha-band (8-12 Hz) oscillation measured over sensorimotor cortex which typically shows reductions in spectral power during both one's own movements and observation of others' actions. This mu suppression is thought to reflect integration of perceptual and motor representations for understanding of others' mental states, which may be disrupted in individuals with autism-spectrum traits. However, because spectral power is usually quantified at the group level, it has limited usefulness for characterizing individual variation in the mu rhythm, particularly with respect to autism-spectrum traits. Instead, individual peak frequency may provide a better measure of mu rhythm variability across participants. Previous developmental studies have linked ASD to slowing of individual peak frequency in the alpha band, or peak alpha frequency (PAF), predominantly associated with selective attention. Yet individual variability in the peak mu frequency (PMF) remains largely unexplored, particularly with respect to autism-spectrum traits. Here we quantified peak frequency of occipitoparietal alpha and sensorimotor mu rhythms across neurotypical individuals as a function of autism-spectrum traits. High-density 128-channel EEG data were collected from 60 participants while they completed two tasks previously reported to reliably index the sensorimotor mu rhythm: motor execution (bimanual finger tapping) and action observation (viewing of whole-body human movements). We found that individual measurement in the peak oscillatory frequency of the mu rhythm was highly reliable within participants, was not driven by resting vs. task states, and showed good correlation across action execution and observation tasks. Within our neurotypical sample, higher autism-spectrum traits were associated with slowing of the PMF, as predicted. This effect was not likely explained by volume conduction of the occipitoparietal PAF associated with attention. Together, these data support individual peak oscillatory alpha-band frequency as a correlate of autism-spectrum traits, warranting further research with larger samples and clinical populations.

The degree of mu rhythm suppression in women is associated with presence of children as well as empathy and anxiety level.

In experiments on observing and performing social gestures, the level of mu rhythm suppression is associated with the activity of the mirror neuron system (MNS), which is responsible for the perception and understanding of nonverbal signals in social communication. In turn, while MNS activity may be associated primarily with empathy, it is also associated with other psychological and demographic factors affecting the effectiveness of cortical neural networks. In this study, we verified the influence of empathy, state and trait anxiety levels, presence and number of children, and age on the mu-suppression level in 40 women. We used 32-channel EEG recorded during observation, and synchronous execution of various hand movements. The ICA infomax method was used for decomposing and selecting the left hemisphere component of the mu-rhythm. Mu-suppression was higher in women with one child, with higher levels of empathy, and with lower anxiety levels. It is possible that MNS activity is stronger in women during parental care.

Mu rhythm suppression over sensorimotor regions is associated with greater empathic accuracy.

When people encounter others' emotions, they engage multiple brain systems, including parts of the sensorimotor cortex associated with motor simulation. Simulation-related brain activity is commonly described as a 'low-level' component of empathy and social cognition. It remains unclear whether and how sensorimotor simulation contributes to complex empathic judgments. Here, we combine a naturalistic social paradigm with a reliable index of sensorimotor cortex-based simulation: electroencephalography suppression of oscillatory activity in the mu frequency band. We recruited participants to watch naturalistic video clips of people ('targets') describing emotional life events. In two experiments, participants viewed these clips (i) with video and sound, (ii) with only video or (iii) with only sound and provided continuous ratings of how they believed the target felt. We operationalized 'empathic accuracy' as the correlation between participants' inferences and targets' self-report. In Experiment 1 (US sample), across all conditions, right-lateralized mu suppression tracked empathic accuracy. In Experiment 2 (Israeli sample), this replicated only when using individualized frequency-bands and only for the visual stimuli. Our results provide novel evidence that sensorimotor representations-as measured through mu suppression-play a role not only in low-level motor simulation, but also in higher-level inferences about others' emotions, especially when visual cues are crucial for accuracy.

Social context shapes neural processing of others' actions in 9-month-old infants.

From infancy, neural processes for perceiving others' actions and producing one's own actions overlap (neural mirroring). Adults and children show enhanced mirroring in social interactions. Yet, whether social context affects mirroring in infancy, a time when processing others' actions is crucial for action learning, remains unclear. We examined whether turn-taking, an early form of social interaction, enhanced 9-month-olds' neural mirroring. We recorded electroencephalography while 9-month-olds were grasping (execution) and observing live grasps (observation). In this design, half of the infants observed and acted in alternation (turn-taking condition), whereas the other half observed several times in a row before acting (blocked condition). Replicating previous findings, infants showed significant 6- to 9-Hz mu suppression (indicating motor activation) during execution and observation (n = 24). In addition, a condition (turn-taking or blocked) by time (action start or end) interaction indicated that infants engaged in turn-taking (n = 9), but not in the blocked context (n = 15), showed more mirroring when observing the action start compared with the action end. Exploratory analyses further suggest that (a) there is higher visual-motor functional connectivity in turn-taking toward the action's end, (b) mirroring relates to later visual-motor connectivity, and (c) visual attention as indexed by occipital alpha is enhanced in turn-taking compared with the blocked context. Together, this suggests that the neural processing of others' actions is modulated by the social context in infancy and that turn-taking may be particularly effective in engaging infants' action perception system.

Age-related Differences in Mu Rhythm During Emotional Destination Memory Task.

BACKGROUND: Destination memory defined as the ability to remember to whom we addressed a piece of information is found to be impaired in normal aging. Theories of affect development and research findings have shown that emotional charging improves performance on memory tasks, and also that Mu rhythm is desynchronized as an index of mirror neuron activation during such tasks. OBJECTIVE: In this paper, we sought to investigate the differences in Mu rhythm during an emotional destination memory task, between younger and older adults. METHODS: 16 cognitively normal older adults, recruited from Alzheimer's disease day center and 16 young adults, recruited via advertisements, participated in this experimental study. We investigated destination memory of emotionally charged faces (Emotional Destination Memory, EDM) while applying electroencephalograph (EEG) in real time in young versus older adults. We measured Mu rhythm in frontal, fronto-temporal and central areas. EEG data has been pre-processed, segmented in non-overlapping epochs, and independent component analysis (ICA) has been conducted to reject artifacts. RESULTS: Results showed that young adults performed better than older adults in remembering facts associated with angry faces. Also, different neurophysiological activation was found, with older adults showing Mu suppression in frontal and fronto-temporal regions, specifically in F3, F7 and F8 electrodes, in contrast with young adults who showed Mu enhancement. Regarding within group differences, it was found that in the older adults group, electrodes F8 and central C3 were the most activated, while in the young adults group, C3 was the most activated electrode. CONCLUSION: The findings suggest better behavioral performance of young adults as a result of better cognitive state and adaptive bias. On a neurophysiological level, it is suggested that older adults employ Mu suppression, thus possible activation of mirror neurons, as a compensatory mechanism while mirroring properties are not spontaneously activated in young adults.

Is there a relationship between EEG and sTMS neurophysiological markers of the putative human mirror neuron system?

The mirror neuron system (MNS) has been theorized to play a neurobiological role in a number of social cognitive abilities and is commonly indexed putatively in humans via interpersonal motor resonance (IMR) and mu suppression. Although both indices are thought to measure similar neuronal populations (i.e., "mirror neurons"), it has been suggested that these methods are unrelated, and therefore, incompatible. However, prior studies reporting no relationships were typically conducted in small and underpowered samples. Thus, we aimed to investigate this potential association in a large sample of neurotypical adults (N = 116; 72 females). Participants underwent transcranial magnetic stimulation (TMS), electromyography (EMG), and electroencephalography (EEG) during the observation of videos of actors performing grasping actions in order to index IMR and mu suppression (in beta, lower alpha, and upper alpha bandwidths). A series of linear regressions revealed no associations between IMR and each of the mu suppression bandwidths. Supplementary Bayesian analyses provided further evidence in favor of the null (B01  = 8.85-8.93), providing further support for no association between the two indices of MNS activity. Our findings suggest that these two measures may indeed be unrelated indices that perhaps assess different neurophysiological aspects of the MNS. These results have important implications for future studies examining the MNS.

Does agency matter? Neural processing of robotic movements in 4- and 8-year olds.

Despite the increase in interactions between children and robots, our understanding of children's neural processing of robotic movements is limited. The current study theorized that motor resonance hinges on the agency of an actor: its ability to perform actions volitionally. As one of the first studies with a cross-sectional sample of preschoolers and older children and with a specific focus on robotic action (rather than abstract non-human action), the current study investigated whether the perceived agency of a robot moderated children's motor resonance for robotic movements, and whether this changed with age. Motor resonance was measured using electroencephalography (EEG) by assessing mu power while 4 and 8-year-olds observed actions performed by agentic versus non-agentic robots and humans. Results show that older children resonated more strongly with non-agentic than agentic robotic or human movement, while no such differences were found for preschoolers. This outcome is discussed in terms of a predictive coding account of motor resonance. Importantly, these findings contribute to the existing set of studies on this topic by showing that, while keeping all kinematic information constant, there is a clear developmental difference in how children process robotic movement depending on the level of agency of a robot.

Is motor cortex deactivation during action observation related to imitation in infancy? A commentary on Köster et al., 2020.

Sensorimotor alpha suppression is present both during the observation and execution of actions, and is a commonly used tool to investigate neural mirroring in infancy. Köster et al. (2020) used this measure to investigate infants' motor cortex activation during the observation of action demonstrations and its relationship to subsequent imitation of these actions. Contrary to what is implied in the paper and to common findings in the literature, the study's results appear to suggest that the motor system was deactivated during the observation of the actions, and that greater deactivation during action observation was associated with a greater tendency to copy the action. Here we present potential methodological explanations for these unexpected findings and discuss them in relation to common recommendations in the field.

Superior Facilitation of an Action Observation Network by Congruent Character Movements in Brain-Computer Interface Action-Observation Games.

Action observation (AO) is a promising strategy for promoting motor function in neural rehabilitation. Recently, brain-computer interface (BCI)-AO game rehabilitation, which combines AO therapy with BCI technology, has been introduced to improve the effectiveness of rehabilitation. This approach can improve motor learning by providing feedback, which can be interactive in an observation task, and the game contents of the BCI-AO game paradigm can affect rehabilitation. In this study, the effects of congruent rather than incongruent feedback in a BCI-AO game on mirror neurons were investigated. Specifically, the mu suppression with congruent and incongruent BCI-AO games was measured in 17 healthy adults. The mu suppression in the central motor cortex was significantly higher with the congruent BCI-AO game than with the incongruent one. In addition, the satisfaction evaluation results were excellent for the congruent case. These results support the fact that providing feedback congruent with the motion of an action video facilitates mirror neuron activity and can offer useful guidelines for the design of BCI-AO games for rehabilitation.

Transcranial Direct Current Stimulation Effect on Virtual Hand Illusion.

Virtual reality (VR) is effectively used to evoke the mirror illusion, and transcranial direct current stimulation (tDCS) synergistically facilitates this illusion. This study investigated whether a mirror virtual hand illusion (MVHI) induced by an immersive, first-person-perspective, virtual mirror system could be modulated by tDCS of the primary motor cortex. Fourteen healthy adults (average age 21.86 years ±0.47, seven men and seven women) participated in this study, and they experienced VR with and without tDCS-the tDCS and sham conditions, each of which takes ∼30 minutes-on separate days to allow the washout of the tDCS effect. While experiencing VR, the movements of the virtual left hand reflected the flexion and extension of the real right hand. Subsequently, electroencephalogram was recorded, the magnitude of the proprioceptive shift was measured, and the participants provided responses to a questionnaire regarding hand ownership. A significant difference in the proprioceptive shift was observed between the tDCS and sham conditions. In addition, there was significant suppression of the mu power in Pz, and augmentation of the beta power in the Pz, P4, O1, and O2 channels. The difference in proprioceptive deviation between the two conditions showed significant negative correlation with mu suppression over the left frontal lobe in the tDCS condition. Finally, the question "I felt that the virtual hand was my own hand" received a significantly higher score under the tDCS condition. In short, applying tDCS over the motor cortex facilitates the MVHI by activating the attentional network over the parietal and frontal lobes such that the MVHI induces more proprioceptive drift, which suggests that the combination of VR and tDCS can enhance the immersive effect in VR. This result provides better support for the use of the MVHI paradigm in combination with tDCS for recovery from illnesses such as stroke.

A study of EEG mu neurofeedback during action observation.

The mirror system is a brain network that gets activated during action performance and observation. Brain mu waves have been used as a mirror system activity index; however, mu rhythm is prone to contamination by occipital alpha wave activity, thus raising a concern regarding its reliability as an index of the mirror system activity. In this study, we investigated whether mu suppression can be used as an index of neurofeedback training, which influences mirror system activities. Participants observed videos of hand movement under three different conditions: central mu feedback (muFB), occipital alpha feedback (aFB), and simple observation without any feedback (OBS). Results showed that at the 4-5 min mark, mu wave was most significantly suppressed in the central site at muFB. We thus demonstrated the possibility of increasing mu wave suppression in feedback training using a specific stimulus such as motion observation.

Encoding, storage, and response preparation-Distinct EEG correlates of stimulus and action representations in working memory.

Working memory (WM) allows for the active storage of stimulus- and higher level representations, such as action plans. This electroencephalography (EEG) study investigated the specific electrophysiological correlates dissociating action-related from stimulus-related representations in WM using three different experimental conditions based on the same stimulus material. In the experiment, a random sequence of single numbers (from 1 to 6) was presented and participants had to indicate whether the current number (N0 condition), the preceding number (N-1 condition), or the sum of the current and the preceding number (S-1 condition) was odd or even. Accordingly, participants had to store a stimulus representation in S-1 and an action representation in N-1 until the onset of the next stimulus. In the EEG, the storage of stimulus representations (S-1) was reflected by a fronto-central slow wave indicating the rehearsal of information that was required for the response in the following trial. In contrast, the storage of action representations (N-1) went along with a posterior positive slow wave, suggesting that the action plan was actively stored in WM until the presentation of the next stimulus. Crucially, preparing for the next response in N-1 was associated with increased contralateral mu/beta suppression, predicting the response time in the given trial. Our findings, thus, show that the WM processes for stimulus- and action representations can be clearly dissociated from each other with a distinct sequence of EEG correlates for encoding, storage, and response preparation.

Social perceptions of warmth and competence influence behavioral intentions and neural processing.

Perceptions of the primary social dimensions, warmth and competence, determine how we view and relate to social targets. To discern how warmth and competence might affect neural processing and its downstream behavioral consequences, we manipulated impressions of targets' warmth and competence and then measured intentions toward the target and motor resonance, a neural process previously linked to social processing. While EEG was recorded, 66 participants watched videos of people performing a simple motor activity and completed a measure of hypothetical intentions to help or harm. Both perceptions of warmth and competence predicted an increase in helping intentions. Moreover, participants showed the least motor resonance with high competence-medium warmth targets, suggesting the importance of both social dimensions in driving neural simulation of targets' actions. Perceptions of a person's warmth and competence can affect not only how others might intend to treat them, but also how they might process their basic experiences on a neural level.