A plea to explore interpersonal neurofeedback as a possible
intervention for children on the Autism Spectrum
Literature Thesis by Lena Adel (12720178), MSc Brain and Cognitive Sciences,
Universiteit van Amsterdam
Supervision and Assessment: dr. Suzanne Dikker, Max Planck Center for
Language, Music and Emotion, New York University
Examination: dr. Tim Ziermans, Programme Group Brain and Cognition,
Universiteit van Amsterdam
In this thesis, I will use identity-first language (e.g autistic child) and person-first language (e.g. child with ASC/autism) interchangeably. Identity-first language is often favoured by autistic adults and parents, while person-first terminology is favoured by professionals (Kenny et al., 2016).
Abstract
Diverging socio-communicative skills represent one of the core characteristics of Autism Spectrum Conditions (ASC). In reality, those skills manifest in social interaction between two or more people. Despite this, ‘conventional’ theories on the causes of ASC as well as therapy approaches are usually focussed on the autistic individual. Here, I present approaches that emphasise the reciprocity involved in dynamic interaction and the role the social environment plays in theorising ASC. I furthermore provide empirical evidence on interpersonal aspects in ASC. After introducing the method of neurofeedback and elucidating its feasibility for children with ASC, I review interpersonal neurofeedback and its previous applications. Eventually, the arguments from the reviewed literature are combined with a discussion of additional considerations. This leads up to three main arguments: the emphasis lies on interpersonal aspects in ASC, neurofeedback applications are highly feasible, interpersonal synchrony is an authentic measure of social competence. Those arguments indicate that interpersonal neurofeedback as an intervention for children with ASC should be explored thoroughly through research as soon as possible.
List of abbreviations
ABA - Applied Behavioural Analysis
ASC - Autism Spectrum Condition(s)
ASD - Autism Spectrum Disorder(s)
ATEC - Autism Treatment Evaluation Checklist
BCI - Brain Computer Interface(s)
EEG - Electroencephalography
fMRI - functional Magnetic Resonance Imaging
fNIRS - functional Near InfraRed Spectroscopy
MEG - Magnetoencephalography
RMET - Reading the Mind in the Eyes Test
SRS - Social Responsiveness Scale
tASC - transcranial Altering Current Stimulation
TD - Typically Developing, Typical Development
tDSC - transcranial Direct Current Stimulation
ToM - Theory of Mind
QEEG - Quantitative Electroencephalography
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1. Introduction
Successful social communication is crucial in the fundamentally social environment we find ourselves in throughout the entire courses of our lives. For people with Autism Spectrum Disorders (ASD), getting by in this social environment is often more challenging. ASD is defined as a neurodevelopmental disorder. It is characterised by difficulties with social communication and social interaction and restricted and repetitive patterns in behaviours, interests, and activities (American Psychological Association, 2013). However, the manifestation, extent and severity of those defining core characteristics in ASD is highly variable.
As the term ‘disorder’ suggests a merely pathological condition, I will replace the term ASD with Autism Spectrum Conditions (ASC) hereafter.
1.1 Theory
Socio-communicative competence is made up out of a variety of social verbal and non-verbal behaviours. Many accounts explain the difficulties in socio-communicative competence in ASC by atypical social simulation or imitation abilities. Those abilities are assumed to be mediated by underlying neural mechanisms comprising the mirror neuron system, or more generally speaking, by some form of neural resonance system that allows for picking up others’ sentiments. Examples include the assumption that a deficient perceptual recognition or a mapping deficit from sensory input to motor modalities leads to difficulties in social understanding in ASC. This mapping deficit entails difficulties to internally simulate perceived actions and attune motor mimicry (Williams et al., 2004). Or the well-known theory that poor Theory of Mind (ToM; Premack & Woodruff, 1978) abilities comprise difficulties in reflecting upon the content of one’s own as well as others’ mental states. Such mental states include beliefs, intentions, emotions, desires and imagination. Those difficulties with reflecting mental states could in turn be responsible for the irregularities that can be observed in social interaction of children with ASC early on (Simon Baron-Cohen, 2000; Frith et al.,
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1991). Additionally, the concept of embodied resonance or embodied simulation (Gallese, 2006; Gallese & Sinigaglia, 2018) suggests that ToM it is not restricted to metacognitive capability but also includes an experiential aspect. This account goes with Lipps’ original notion of empathy (1907) which states that in order to feel empathy, one needs to integrate the other’s experience into one’s own. Therapeutic measures are restricted to the overt, metacognitive part and do not necessarily foster embodied simulation. Thus, for autistic children, this experiential part could depict the more severe issue regarding their social competence.
1.2 Therapy
Specific autistic characteristics start being present early in life and most institutions fail to adopt an environment that is accessible and integrative for neurodivergent children. Well aligned approaches to therapy enable autistic children less restricted daily functioning and a higher quality of life from an early age on. The most commonly applied therapy method is Applied Behavioural Analysis (ABA). It is based on the elimination or decrease of ‘unfavourable’ behaviour while fostering favourable behaviour. ABA can be applied in all areas that constitute difficulties for autistic children. It is usually an intensive intervention with high frequency. Pharmacological therapy with psychotropic medication to address e.g. aggression, self-injurious behaviour, hyperactivity, anxiety or sleep problems has proven to be a valuable addition to ABA (Rosenberg et al., 2010).
With growing accessibility of technical devices over the past few decades, computer-based interventions including serious game applications have become a common part of ASC therapy. Serious games are digital games with an agenda of educational design and beyond entertainment (Sørensen & Meyer, 2007). They aim to support learning and positive behaviour changes. Many of those games are recognised as beneficial for fostering communicative skills and social behaviour, social conversation, emotion recognition, imaginative skills, sensory integration and learning accounts in children with ASC (Grossard et al., 2017; Noor et al., 2012; Zakari et al., 2014). It has also been found that autistic children enjoy playing video games (Durkin, 2010) and engage with virtual/technically mediated
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environments well (Josman et al., 2008; Mitchell et al., 2007). Furthermore, serious games have the overall advantage of being easily applicable and integrable into daily routines and social environments of children with ASC.
Neurofeedback-based serious games constitute a subgroup of medical serious games. They combine the serious game with non-invasive brain computer interfaces (BCI). In those games, cortical activity has to be manipulated to reach a certain target within the game.
The underlying idea of neurofeedback is to illustrate brain activity, such as frequency, amplitude or coherence. It is illustrated in real time to eventually enable its voluntary modification. Mostly, the brain activity is not directly visually displayed (like e.g. when looking at EEG data) but translated into visual, auditory or tactile stimuli. Those stimuli are often embedded into a playful environment. A simple example is an image that appears blurry and turns clear when the brain activity is modified as requested. Or in a serious game, a car that only moves forward when the desired brain activity is measured.
1.3 Aim of this work
The realities of children with ASC are majorly influenced by difficulties in coping with, and successfully interacting in social environments. Yet, most theories as well as therapy approaches tend to focus merely on the autistic individual. In this work, I will review evidence as well as theoretical frameworks indicating the importance of interpersonal attunement, synchronisation and reciprocity in ASC. I will then review selected studies that assess the impact of neurofeedback therapy on social skills to elucidate its overall feasibility for autistic children. Moreover, I will introduce the method of interpersonal biofeedback with a focus on neural biofeedback, thus interpersonal neurofeedback. This will be followed by an overview of its previous applications and occurrences. Based on the steps described before, I will eventually discuss the possibility of researching interpersonal neurofeedback as an intervention for children on the autism spectrum.
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2. Literature review
2.1 Through others we become ourselves (Vygotsky, 1987): The role of
interpersonal attunement in social interactions
As outlined in the Introduction, many people with ASC have difficulties that result in challenging social situations. In those situations, social understanding remains unfulfilled. In the following sections, I will provide a short introduction to interpersonal synchrony and the methodology used to assess it. Based on this, I will give an overview of studies that assessed aspects of interpersonal synchrony in ASC. Lastly, I will introduce theoretical accounts that acknowledge interpersonal engagement in its reciprocity as source or part source of the social issues people with ASC face.
2.1.1 Interpersonal synchrony and its assessment
Interpersonal synchrony can be described as the dynamic and reciprocal adaptation of the temporal structure of behaviours and states between interactive partners (Delaherche et al., 2012). It is hypothesised to play a substantial role in the success of social understanding and interactions. Interpersonal synchrony can be understood as an adaptive mechanism that affords entrainment between two or more people (Wheatley et al., 2012). Previous research has suggested that it is beneficial for a variety of prosocial behaviours, such as fostering social bonds (Semin, 2007; Semin & Cacioppo, 2008), affiliation (Hove & Risen, 2009), rapport (Vacharkulksemsuk & Fredrickson, 2012) or emotional support satisfaction (Jones & Wirtz, 2007). Moreover, the ‘In-sync model’ (Koole & Tschacher, 2016) suggests that interpersonal synchrony is beneficial for the client’s emotion regulation in psychotherapy through enhancing client-therapist alliance.
Interpersonal synchrony is manifested in, but not reducible to, behavioural synchrony; synchronisation can arise at neural, perceptual, affective, and behavioural levels (Semin, 2007). In that, behavioural synchrony promotes neural synchrony and thereby social engagement. According to Wheatley et al. (2012), this ‘reverse-engineering’ of social
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connection is likely to underlie the distinctive human ability to create large-scale social coordination. To achieve the most comprehensive results, it can therefore be profitable to assess synchrony on a behavioural level (e.g. movement or posture) as well as taking into account physiological synchronisation (e.g. skin conductance or heart rate) and inter-brain coupling, thus neural synchronisation.
Interpersonal neural synchronisation can be assessed using hyperscanning techniques, the simultaneous neuroimaging of two or more people’s brain activity. Hyperscanning enables observing how two brains couple independently of external stimulation during social interaction. It thereby affords extended understanding of the neural underpinnings of cooperation. Interpersonal neural synchrony between two or more interacting agents has been found to enhance joint performance, attention or interaction. The assessment paradigms range from simple motor activities like pressing a button over conversational set-ups to more complex joint activities like playing music or interactive games (for reviews, see Babiloni & Astolfi, 2014; Czeszumski et al., 2020; Konvalinka & Roepstorff, 2012). Noteworthy, enhanced inter-brain coupling has been associated with improved joint action (Dumas et al., 2010), facilitated communication of affect through facial expression (Anders et al., 2011) and successful mother-infant interactions (Hirata et al., 2014; Levy et al., 2017). Similar resting state networks in caregivers and their children suggest similar day-to-day emotional synchrony and that being ‘neurally attuned’ to their parents entails emotional benefits for children (T.-H. Lee et al., 2017). Enhanced inter-brain coupling furthermore correlates with perspective sharing in consequence of simultaneously perceived emotionally valenced input (Lahnakoski et al., 2014). Such similar neural states are believed to allow individuals to connect and be attuned to their environment in a more harmonious way (Wheatley et al., 2012). Additionally, interpersonal neural synchrony has been found to predict communicative success (Stephens et al., 2010) and the engagement of students in class and social dynamics (Dikker et al., 2017). Accordingly, it is hypothesised to be a possible neural marker for dynamic social interaction which is assumed to be driven by shared attention mechanisms (Dikker et al., 2017). In sum, interpersonal neural synchrony assessed with hyperscanning has been associated with a wide range of positive outcomes in areas that are associated with socio-communicative difficulties in ASC.
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2.1.2 Interpersonal synchrony and interaction in ASC research
Unusual patterns in dynamic interaction and reciprocity as a marker of ASC have been reported as early as 1943 by Kanner (1943). Kanner illustrates the experience of a mother who expresses that her autistic child has lacked a sense of relationship for other persons from an early age on. This did for example show in not adjusting posture when being picked up to facilitate the process. In contrast, typically developing (TD) children show this facilitating behaviour when they anticipate being picked up (Reddy et al., 2013). However, the mother also points out that she feels restricted in her own behaviour when interacting with her autistic son. This observation draws attention to a reciprocal aspect in the interaction of an autistic and a non-autistic person. As described above, many areas that are known to be impacted in such interactions, such as shared attention, social decision making, verbal communication, action, movement and emotional alignment, have been associated with interpersonal (neural) synchrony. Subsequently, it has been suggested to study ASC using interactive approaches (Rolison et al., 2015).
In the following section, studies assessing inter-brain coupling and a selection of studies assessing other forms of interpersonal synchrony and dynamic interaction will be outlined. The dyads are mostly consisting of one autistic person and a non-autistic partner. For a comprehensive review on interpersonal synchrony in ASC, I refer to McNaughton and Redcay (2020). The authors summarize a variety of additional studies on diverging motor synchrony, conversational synchrony and physiological synchrony in ASC.
Inter-brain coupling
Tanabe et al. (2012) conducted a functional Magnetic Resonance Imaging (fMRI) hyperscanning study to assess how inter-brain coupling during eye contact correlates with eye cue detection in a joint attention task. ASC–neurotypical dyads were less accurate in detecting gaze direction than neurotypical–neurotypical dyads, performance was impaired in both members of the dyad. The findings suggest that inter-subject synchronisation during eye contact may be required for eye cue detection, which is assumed to play an important role in establishing joint attention and thus in overall successful social communication.
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In a Magnetoencephalography (MEG) hyperscanning study, Hasegawa et al. (2016) assessed the degree of mu-suppression during spontaneous, non-linguistic interactions in dyads consisting of mothers and their young children with ASC. Mu-suppression over sensory motor regions are assumed to be a neural marker for activity in a resonance system similar to the mirror neuron system. They are therefore, broadly speaking, estimated to represent ‘the social mind’. Significant correlations of mothers’ and children’s mu-suppression indices in the right precentral area and the degree of overall mu-suppression negatively correlated with autistic trait severity of the children. The authors conclude that enhanced synchronised mu-suppression is beneficial for autistic interaction.
Wang et al. (2020) conducted a functional Near InfraRed Spectroscopy (fNIRS) hyperscanning study in which children on the autism spectrum and their parents performed a simple button pressing task. Children’s performance was best when inter-brain coupling with parents was most enhanced as opposed to being in less synchrony with the parents or performing the task alone (but under observation of the parent). Those findings indicate a positive impact of interpersonal neural synchronisation on the child’s task performance ability. They furthermore found that the level of interpersonal synchrony correlates with autistic characteristics, in such a way that children with more pronounced autistic characteristics performed worse in the task and displayed a lower level of neural synchronisation with their parents during cooperation.
In sum, the results of these three studies indicate a correlation of the extent of interpersonal neural synchrony and the quality of social behaviours of autistic children in dynamic interactions.
Movement synchrony
Based on a study in which children with ASC and their caregivers were to synchronise rocking in a chair, Marsh et al. (2013) suggest that perceptual, attentional, and adaptive timing deficiencies directly impact the ability to socially connect to a ‘unit’ with others.
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Fitzpatrick, Romero and colleagues conducted a series of studies further assessing social motor coordination in dyads consisting of children and adolescents on the autism spectrum and either their caregiver or an experimenter. They implemented different action sequences, like e.g. tapping task or interpersonal hand clapping game, that involved the interpersonal coordination of objects, bodies and faces to evaluate imitation and synchronization abilities (Fitzpatrick et al., 2017; Romero et al., 2016) or a pendulum coordination paradigm to assess dynamic, process-oriented measures of social motor synchrony (Fitzpatrick et al., 2016). Autistic participants demonstrated disruption of spontaneous synchronisation and intentional synchronisation, decreased movement synchrony during implicit, dynamic movement coordination as well as during explicit, intentional movement matching. The authors suggest that socio-communicative difficulties of children with ASC are closely connected (co-dependent) to these difficulties in social motor synchronisation they found.
Koehne and colleagues (2016) found that when individuals with ASC produced more synchronous finger tapping movements with their partner, ratings of cognitive (but not affective) empathy increased. In a TD group, the level of cognitive empathy was also impacted by perceived synchrony, this mediating effect was not present in the ASC group. Those findings are indicative for a mediating role of interpersonal synchrony in cognitive empathy and an attenuated capacity to utilise it in ASC.
Taken together, these results suggest that the ability to synchronise movement correlates with social competence in ASC.
Synchrony in play interaction
Impairments in joint attention are widely recognized as a reliable early autistic trait (S. Baron-Cohen et al., 1996). Joint attention is presumed to be an essential skill in developing mentalizing capacities (Happé & Frith, 2014; Mundy & Stella, 2000; Soto-Icaza et al., 2015). It is furthermore one of the few cognitive abilities that is conventionally assumed to be impacted not only by individual autistic traits, but the context of a social interaction. Despite this, only a very limited number of studies assess both, the child’s and the interacting person’s behaviour.
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Siller and Sigman (2002) observed caregivers’ indicative behaviours and verbalisation with respect to their autistic children’s focus of attention during play interactions. More precisely, they assessed whether the caregiver’s behaviour was synchronised with their child’s focus of attention. It was found that children of caregivers who showed higher levels of synchronisation during play interactions developed superior joint attention and language over a long-term period (1,10 and 16 years).
Lee and Schertz (2020) assessed the relationship between turn taking and joint attention (responding to joint attention and initiating joint attention) during interaction of caregivers with their toddlers with ASC. A positive relationship between the two forms of social communication was found. This suggests that even before joint attention, the dynamic process of turn taking which is highly reciprocal, plays a role in the long-term development of more complex social abilities like mentalizing.
Those two studies imply that attentional synchronisation levels of autistic children and their caregivers can be associated with the capacity to develop advanced social abilities.
Non-verbal aspects and affective engagement
Non-verbal aspects of communication (durations of looks, numbers of head-shakes/nod episodes, and smiles) and intersubjective measures (affective engagement which was defined as the degree of emotional connectedness between the participant and the experimenter, rated using a one-to-five point scale, flow of interview) were observed during semi-structured interviews about self-concept with adolescents on the autism spectrum (García-Pérez et al., 2007). It was found that non-verbal aspects correlate with intersubjective measures, indicating an interpersonal, non-individualistic aspect to communicative difficulties.
2.1.3 Theories with emphasis on interpersonal factors in ASC
In the Introduction, I briefly introduced a few ‘unilateral explanations’ for autistic people’s difficulties in social competence. Those unilateral explanations assume that social
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difficulties merely or primarily derive from an intrapersonal deficit of the autistic person in processing, understanding and reacting to social stimuli. Yet, the evidence from studies provided in the section above, suggests that interpersonal aspects play a constitutive role in social behaviours in ASC. Accordingly, another way of approaching the emergence of socio-communicative difficulties in ASC, are accounts that see social difficulties as partly constituted through dynamic interaction between at least two agents. Thus, the person on the autism spectrum as well as the person(s) they are interacting with. Those approaches tie in with on the first sight unilateral approaches such as ToM, embodied resonance or general simulation difficulties, including the assumption of a deficient mirror neuron or resonance system. They don’t oppose but extend them and can help to better grasp the extent of social difficulties. A selection of those interpersonal approaches to ASC will be presented in the following sections.
The intersubjectivity approach to ASC as suggested by Hobson and Baron-Cohen (2002) originates from the idea that psychological social connectedness, or what they call intersubjective engagement, cannot be assessed objectively. Yet it needs to be considered in theorising autistic characteristics. Intersubjective engagement is established ‘before thought’, hence before any ‘higher order cognitive functions’ come into play, it is an experience, not a metacognitive function. This idea is in line with Gallese’s account of embodied resonance, which assumes an experiential aspect to be crucial for ToM. Hobson and Baron-Cohen point out that the atypical behaviour of people on the autism spectrum does not stand alone, but always unfolds in social interaction and yields in atypical reciprocity, despite neurotypical interaction partners.
Gallagher (2004) develops a neurophenomenological interaction theory of autism which opposes the conventional ToM account centering around conceptual, explanatory and predictive mentalizing. Gallagher develops his interaction theory based on the notions of primary and secondary intersubjectivity (Trevarthen, 1979). He points out that even though we might indeed possess sophisticated ways of theorising other minds (secondary intersubjectivity), we are not limited to this mentalistic understanding. In interaction theory, primary intersubjectivity, thus a common bodily intentionality, continues to play a crucial role in social understanding. Phenomenological evidence indicates that our interactive relations with others mainly involve modes of understanding that are pragmatic and evaluative, based
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on environmental and contextual factors. This means that ToM cannot account for realistic interaction. And therefore, a deficient ToM cannot be taken as the cause of difficulties in social skills of individuals with autism. Gallagher conclusively distances from an individualistic approach to autism which is centred around mentalistic, conceptual, explanatory or predictive attitudes.
De Jaegehr (2013) offers an enactive account of autism, on the basis of embodiment and sense making. Her approach integrates cognitive, social, communicative, embodied, interactive, experiential and affective aspects. Like Gallagher, she distances herself from accounts that focus on particular neurocognitive functioning (e.g. ToM). She points out the importance of considering autistic embodiment and how it connects with autistic psychology and offers an explanation for the whole range of autistic characteristics. Regarding social difficulties in ASC, De Jaegher denotes that the ability for sensorimotor interactional coordination is at the base of social connection. And since autistic individuals display sensorimotor differences, a different sense-making in autism is suggested. In turn, those differences in sense-making impact the ability of flexible engagement with a social partner, which is the base for participatory sense-making.
Léon (2019) develops an account based on the concept of minimal social acts (Reinach, 1989; von Hildebrand, 1975). The success of minimal social acts is built on responsiveness or repetitiveness from the receiver. In ASC, those minimal social acts could be flawed because the receiver (e.g. the person an autistic individual is interacting with) does not reciprocate the intention of the autistic person and the other way around. The response, which is constitutive in building up what we perceive as socially skilled behaviour, is lacking. Léon further brings up the phenomenon that individuals with so called ‘high-functioning autism’, who do not have intellectual or language deficits, still display deficits in social-emotional reciprocity. This might be due to the way they learn about the social world; they rely on intellectual and cognitive strategies which are insensitive to the dynamic changes of real-life social interactions. Léon concludes that socio-communicative difficulties in ASC can impossibly be understood in a unilateral fashion. Reciprocity in connectedness, unconscious alignment and communicative engagement are vital for their understanding.
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The dialectical misattunement hypothesis developed by Bolis and colleagues (2017) draws on accounts of predictive processing and active inference. ASC traits are not attributed to impaired neurocognitive functions (e.g. ToM) and/or specific brain areas (e.g. ‘the mirror neuron system’). Instead, ASC is revised as a different prediction and (inter-)action style. At a collective level, interpersonal incompatibilities in prediction and (inter-)action styles are induced by weak interpersonal coupling (under impact of sociocultural factors). At an individual level, the divergence between prediction and (inter-)action styles entails weak communicative coupling with others. Initially, differences at the individual level might be negligible. However, through feedback mechanisms created through constant social interaction, differences can cumulatively enhance or weaken interpersonal coupling and the other way around. Therefore, an initial communicative gap can yield incompatible prediction and (inter-)action styles and vice versa. Note that this assumption aligns with Léon’s account of flawed minimal social acts.
Based on this framework, Bolis and colleagues suggest new approaches to psychotherapy and education. Approaches that focus on tuning collective rather than individual behaviour. They bring up ‘sociofeedback’, thus interpersonal biofeedback, as a promising method.
Figure 1
Dialectical Misattunement
Note. Dialectical Misattunement. Increasing communicative gap (collective level) entails increasingly different prediction and (inter-)action styles (individual level) and vice versa. From “Beyond Autism: Introducing the Dialectical Misattunement Hypothesis and a Bayesian Account of Intersubjectivity “, by D. Bolis et al., 2017, Psychopathology, 50(6), 355-372 (http://dx.doi.org/10.1159/000484353).
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Shamay-Tsoory and colleagues (2019) offer a multilevel model of social alignment. The model theorises movement synchrony, emotional contagion and social conformity as interrelated processes that rely on shared neural networks and feedback loops. The authors assume a predictive processing mechanism during social interaction to enable successful alignment in movement, emotion, and cognitions with others. Successful social alignment is based on the feedback loops of three networks: Firstly, the gap-detection system which monitors errors/misattunement. Secondly, the alignment/observation-execution system which accounts for the gaps detected and coordinates alignment in interpersonal motor synchrony, emotional contagion, and conformity. And thirdly, the alignment reward circuit which is activated when alignment is achieved.
Shamay-Tsoori and colleagues highlight that years of searching for atypical brain areas as neuromarkers for ASC did not yield any unambiguous results. Yet in ASC, all three levels of social alignment (movement synchrony, emotional contagion and social conformity) are affected behaviourally. Additionally, there are neuroimaging studies that show differences in Figure 2
Extended Integrative Model of Alignment
Note. Extended Integrative Model of Alignment. Feedback loops of three networks on which successful social alignment is based on: The gap-detection system (dorsomedial prefrontal cortex (dmPFC), dorsal anterior cingulate cortex (dACC), anterior insula (AI)), the alignment/observation-execution system (inferior frontal gyrus (IFG), inferior parietal lobule (IPL), premotor cortex (PC)). the alignment reward circuit orbitofrontal cortex (OFC), ventromedial PFC (vmPFC), and ventral striatum (VS)).
From “Herding Brains: A Core Neural Mechanism for Social Alignment”, by S. Shamay-Tsoory et al., 2019, Trends in Cognitive Sciences, 23(3), 174-186 (http://dx.doi.org/10.1016/j.tics.2019.01.002).
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cortical activity or connectivity. Therefore, the authors suggest deficiencies in the feedback loops introduced above as a reasonable source of ASC traits. The multilevel model of social alignment offers an integrative approach in line with Bayesian explanations and predictive coding accounts (see Bolis et al., 2017 or Pellicano & Burr, 2012 who assume attenuated prior predictions for alignment in the irregularities found in behaviour AND brain activity of autistic individuals).
2.2 Take a look inside the head: From intra- to interpersonal neurofeedback
So far, I have introduced interpersonal synchrony and presented evidence as well as theoretical frameworks which indicate the crucial role reciprocity plays in ASC. The following section is concerned with neurofeedback. Firstly, I will provide a brief explanation of neurofeedback to then elucidate its feasibility in use with autistic children by reviewing selected studies. Subsequently, I will illustrate previous applications of interpersonal neurofeedback/cross-brain biofeedback (as well as other forms of biofeedback).
2.2.1 Neurofeedback
The underlying idea of neurofeedback in therapeutic settings is, to enable self-regulation of brain activity and thereby support desired behaviour. Thus, neurofeedback can be described as a particular form of non-invasive BCI in which ‘‘the aim is not to control an external device but rather to use external feedback to modulate specific aspects of physiological signals intrinsic to the brain.” (Wood et al., 2014). When changes in cortical activity occur as requested, a reward within the application is dispensed. The direct goal of neurofeedback is teaching how to influence cortical activity. Its indirect goal is evoking positive effects on particular behaviours and daily functioning. EEG-based neurofeedback is the most common application of neurofeedback, as EEG has the advantage of a high temporal solution. It thereby allows for real time feedback to be integrated into, for example, an ongoing game. Mobile EEG devices are easily applicable. Additionally, relatively low-priced mobile devices forcommercial use exist.
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Neurofeedback has been used with neurotypical individuals to enhance cognitive abilities like attention and memory (Thomas et al., 2013). It has also been applied in a variety of medical and therapeutic contexts. Examples include therapy of Attention Deficit Disorders (Holtmann et al., 2014; Lofthouse et al., 2012; Van Doren et al., 2019), epilepsy (Monderer et al., 2002; Walker & Kozlowski, 2005), cognitive and motor impairments caused by stroke (Renton et al., 2017; T. Wang et al., 2018), depression disorders (Yadollahpour & Arani, 2014), post-traumatic stress disorders (Chiba et al., 2019) or eating disorders (Bartholdy et al., 2013).
2.2.2 Neurofeedback in ASC therapy
Evidence indicates that divergent social skills in ASC correlate with diverging functioning in brain areas that are associated with social cognition, social perception and social interaction (Hadjikhani et al., 2006; Misra, 2014; Pelphrey et al., 2005; Pelphrey & Carter, 2008). Additionally, resting state EEGs of autistic people exhibit deviations in power, an overall local overconnectivity and long-range underconnectivity, enhanced power in the left hemisphere (J. Wang et al., 2013). Hence derives the assumption that modulation of cortical activity through neurofeedback could be beneficial for addressing undesired ASC traits.
For a comprehensive review on neurofeedback training with autistic children, see Hoogdalem et al. (2020) who recently reviewed a variety of studies assessing different features, heterogeneous groups, different types and frequency of neurofeedback training. The authors conclude that neurofeedback impacts neurophysiological activity and enables transfer from learned skills to social interactions. Examples include improvement in social behaviour, attention and sensory-motor skills.
The focus of this work, however, is specifically on social aspects in ASC. Consequently, only studies that implement neurofeedback training with a focus on positive effects on social behaviour, like social awareness and communication, were selected for review.
Almost 20 years ago, Jarusiewicz (2002) conducted a pilot study assessing the efficiency of neurofeedback in ASC with 40 children with ASC. They were split into pairs, matching gender,
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age and the ‘extent of autism’ and randomly assigned to the intervention group or the wait list control group. Twelve out of twenty children completed the intervention with a mean of 36 neurofeedback sessions. The task consisted of adjusting activity at electrode site C4 to a 10-13 Hz (high alpha) range. Autism Treatment Evaluation Checklist (ATEC, Rimland & Edelson, 2000) levels of sociability, speech/language/communication, health and sensory/cognitive awareness improved significantly after neurofeedback training. Additionally, parents reported improvement in areas that they had identified as desirable for improvement (socialization, vocalization, school work, anxiety, tantrums and sleep) to varying degrees with an average of 5 (scale 0-10, 10 indicating the most improvement). This pilot study initially suggested the efficiency of neurofeedback training for autistic children. It thereby laid the foundation for further research.
Kouijzer et al. (2009) implemented 40 EEG neurofeedback sessions with seven children with ASC with an IQ above 70. They assessed social skills as well executive functioning pre- and post-intervention. Seven autistic children (age, IQ and sex matched) constituted the wait list control group. The task in this study was reducing theta activity (4-7 Hz), while increasing activity in the low beta band (12-15 Hz). The children received visual feedback in the form of bar graphs. If the amplitude criteria were met and maintained, a movie with sound played. If the criteria were not met, the movie stopped. Assessment of the Children's Communication Checklist (Geurts, 2007) indicated improvement of general communication, including non-verbal communication, in the intervention group as compared to the control group. No improvement was found in pragmatics. An evaluation of an adapted version of the AUTI-R (Van Berckelaer-Onnes & Hoekman, 1991) suggested improvements for children in the intervention group in social interaction, communication, and typical behaviour as compared to children in the control group. The study also found improvements in executive functioning (cognitive flexibility, attentional control, goal setting, speed and efficiency). Furthermore, the intervention group was reassessed after 12 months. Direct post-neurofeedback positive effects on social skills and executive functioning were maintained (Kouijzer, de Moor, Gerrits, Buitelaar, et al., 2009). One year later, Kouijzer et al. (2010) were able to replicate their findings indicating a positive effect of neurofeedback on executive functioning and socio-communicative skills using individualized or quantitative EEG (QEEG)-guided neurofeedback (Coben & Padolsky, 2007; Heinrich et al., 2007; Walker & Kozlowski, 2005). Frequency bands
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and electrode placement for treatment in this study were adjusted to the individual QEEG of each participant. Furthermore, they included children ‘from the full spectrum’ (with an IQ above 80), thus with a bigger variety in autistic traits, into the study. This way, they aimed to prove the applicability of their neurofeedback training to a more diverse group.
Pineda et al. (2014) conducted a study with 13 children with ASC and age matched TD controls. Both groups underwent 30 hours of neurofeedback training. The aim of this study was to induce neuroplastic changes that are beneficial to the mirror neuron system through regulating alpha mu rhythm (8-12Hz) (suppression or desynchronisation). Video clips depicting social interaction (cartoon or real life) were the reward in this study. They were only played when the power in the alpha mu band recorded at C4 electrode site was maintained above a pre-determined threshold for at least 1 second. Meanwhile, theta (4 –8 Hz) and beta (13 –30 Hz) activity had to remain below pre-determined thresholds. The study found a significant decrease in scores as a function of treatment on the social responsiveness scale (SRS, Constantino et al., 2003) and in ATEC (Rimland & Edelson, 2000) scores in the ASC group. No significant effects for Vineland adaptive behaviour scales (VABS, Sparrow et al., 1984) were found.
Friedrich and colleagues (2015) implemented a neurofeedback study with 13 autistic children. They received 16 sessions playing a neurofeedback social mirroring game including a social interaction sequence before each non-social game episode. The task was modulating mu (8– 12 Hz), theta (3–8 Hz) and high beta (18–30 Hz) bands. Before every non-social segment, the game involved a ‘social interaction’ sequence. In this sequence the child’s avatar imitates the facial expression of the non-player avatar in real-time as a reward for the desired frequency manipulation. Negative feedback yields in a sad face without any imitation behaviour. In the ‘non-social’ part of the game, participants had to increase mu power in order to receive reward and continue the journey in the game plot. Results of the Reading the Mind in the Eyes Test (RMET, Simon Baron-Cohen et al., 2001) to assess mentalizing abilities suggests significant improvement in emotion recognition as a function of training. Additionally, in an emotion imitation task, the children exhibited more appropriate spontaneous imitation behaviour post- than pre- neurofeedback training. Post-intervention results of VABS (Sparrow et al., 1984) , SRS (Constantino et al., 2003), ATEC (Rimland & Edelson, 2000) indicate
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significant improvements in autistic features, social responsiveness and adaptive behaviour. Furthermore, EEG measures displayed a higher mu suppression index after the training. According to the authors, this implies higher activity in the mirror neuron system.
Lastly, Datko et al. (2018) conducted a neurofeedback study modulating mu rhythms (8-12Hz) with 17 children with ASC and age matched TD controls. They completed 20 neurofeedback training sessions. The task was to increase mu rhythm while inhibiting theta and beta rhythms to either control the movement of a car in a game or enable a movie to continue playing. Pre- and post fMRI scans showed increased activity in the mirror neuron system. Furthermore, accuracy and reaction time improvements post neurofeedback during a finger lifting imitation task was found. Additionally, ATEC (Rimland & Edelson, 2000) and SRS (Constantino et al., 2003) scores significantly improved.
In sum, the studies reviewed here, strongly indicate a positive impact of neurofeedback training on autistic children’s social skills (measured with diagnostic tools and qualitative questionnaires filled out by caregivers).
2.2.3 Interpersonal neurofeedback in art contexts and games
Regarding the literature reviewed in 2.1, there is an interest in extending the focus from individual to interpersonal neurofeedback. Thus, neurofeedback that depicts the cortical activity of two or more agents and possibly involves voluntary modulation according to a certain, possibly shared, target. In the following sections, I will give an outline of its previous applications in art contexts and games.
Passive interpersonal neurofeedback in art contexts
In the art world, multi-person neurofeedback is not a newcomer. It has been used as early as in the 1960s to explore the possibility to extend musical interfaces (Rosenboom, 1999). As an example, John Lennon’s and Yoko Ono’ brain activity was simultaneously translated into sounds in a TV show in 1975 under supervision of neuroscientist and psychologist David Rosenboom. More previously, the music performance ‘The Space Between
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Us’ (Eaton et al., 2014) used a BCI music interface system which displays brain activity associated with emotional states of performers and members of the audience simultaneously. In the live brain-computer cinema performance ‘Enheduanna – A Manifesto of Falling’ (Zioga et al., 2018), EEG-based neurofeedback of a performer and several members of the audience is used. The feedback is given in the form of live visuals which are displayed during the performance. Findings from this project, among other things, indicate that the ability to identify moments of representation of one's own brain activity correlates with attention and engagement.
The projects described as of yet illustrate passive implementation of neurofeedback, as they do not involve voluntary control of brain activity but solely its display. The projects described hereafter, on the other hand, involve an active implementation of neurofeedback.
Active interpersonal neurofeedback in art contexts
In an exploratory experiment in an immersive art environment Kovacevic and colleagues (Kovacevic et al., 2015) collected data of more than 500 participants in a single night. The experiment consisted of a collective computer game played with 5 players simultaneously. The players manipulated mental states of relaxation and concentration through targeted modulation of alpha and beta frequency ranges. The study detected unprecedented learning speed in power spectrum regulation. It was also found that participants' baseline brain activity predicted the subsequent neurofeedback beta learning speed. The authors interpret the latter finding as indicative for state-dependent learning. Though this project involved a collective game, interpersonal synchrony was neither the target nor of particular interest when interpreting the results.
Art installations with a focus on and interest in interpersonal neural synchrony include Mariko Mori’s ‘Wave UFO’ (Mori et al., 2003). It involves the projection of real-time imagery of EEG data recorded from three participants. The different frequencies are visualised in form of different coloured rings. They move closer to each other and eventually fuse when the participant’s EEGs progress to being in synchrony.
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Likewise, interpersonal synchrony was the centrepiece of a series of interactive art projects using interpersonal neurofeedback realised by Dikker and colleagues. Those projects share the purpose to investigate the relationship between human connectedness and brainwave synchronisation (Dikker, Montgomery, et al., 2019). ‘Measuring the Magic of Mutual Gaze’ (2011), is restaging Marina Abramovic’s project ‘The Artist is Present’ (2010). Participants look into each other’s eyes while their brain activity is visualised for the audience in form of two brains moving closer together the more the participants’ cortical activity is synchronised. ‘The Compatibility Racer’ (2012) is an interactive brain-robotics installation which translates frequency synchronisation into the speed of a cart the participants sit in. The more the cortical activity of the two participants synchronises, the faster the cart moves along a track.
Results from data acquired in ‘The Mutual Wave Machine’ (2013) were published in a research paper (Dikker, Michalareas, et al., 2019). Over the course of five years the ‘Mutual Wave Machine’ was exhibited at festivals and in museums, resulting in a high number of participants (726 after excluding non-usable data sets based on strict criteria) (Dikker, Michalareas, et al., 2019). In this project, two participants sit in a capsule surrounded by an audio-visual environment which is modified by their brain activity. With enhancing synchrony, the audio and visuals become more vivid. Additionally, a projection of one's own face becomes more visible behind the partner when synchrony enhances. The latter constituent of the installation is playing with the idea of ‘seeing oneself in another person’ when feeling socially connected. It was found that inter-brain synchrony was positively related to the dyads’ social closeness, certain personality traits, focus level, and their motivation to connect. Alpha synchrony modulations co-varied with changes in beta coherence, suggesting a relationship between lower and higher frequency inter-brain coupling. Based on their findings, the authors propose implications for shared attention/engagement. Namely that shared attention, as expressed in alpha synchrony, provides an opportunity for establishing shared motor, perceptual and cognitive representations. Overall, ‘The Mutual Wave Machine’ illustrates that interpersonal neurofeedback setups in combination with behavioural measures and careful analysis provide an opportunity to assess face-to-face interaction and social connectedness outside the laboratory. Additionally, the high number and variety of participants with different interpersonal relations suggest a broad feasibility of interpersonal neurofeedback.
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Interpersonal neurofeedback in serious games
Interactive forms of new media and performance art using multi-brain neurofeedback as presented above, share a common goal with computer and serious games using BCI. Specifically, the goal of achieving a level of shared understanding of ideas and the shared reflection upon certain notions (Zioga et al., 2015). Bonnet and colleagues (2013) implemented a study in which participants played a BCI video game. Single and multiplayer conditions were compared with regard to motivation and performance of the participants. They found that the multi-user interactive condition yielded higher motivation and better
Figure 3
The Mutual Wave Machine
Note. The Mutual Wave Machine. By Suzanne Dikker, Matthias Oostrik, Peter Burr, Diederik Schoorl and Pandelis Diamantides. From “Using synchrony-based neurofeedback in search of human connectedness”, by S. Dikker et al., 2019, Brain Art: Brain-Computer Interfaces for Artistic Expression, Chapter 6, 161-206 (https://doi.org/10.1007/978-3-030-14323-7_6)
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performance. The authors conclude, that multiplayer BCI applications can be operational, effective, and more engaging for participants.
Multi-player brain games range from games that require two players to cooperate by communicating through modulating their brain activity while being located in the same room, e.g. Mind The Sheep (Gürkök, 2012). Over competitive multiplayer BCI games like Brainball (Hjelm & Browall, 2000), asking players to relax as much as possible as measured through alpha and beta activity modulation. Up to using motor imagery (imagine hand movements) to play Pong (Krepki et al., 2007).
In sum, interpersonal neurofeedback as realised in new media and performance art and multi-player brain games hold eminent potential for transferring interpersonal neurofeedback applications into therapeutic contexts as they already exist in several, functioning designs.
2.2.4 Interpersonal biofeedback in research
In the following section, I will present research from neuroscience and psychology that used interpersonal neurofeedback and/or other forms of interpersonal biofeedback.
Duan and colleagues (2013) conducted a study to validate a cross-brain fNIRS neurofeedback concept for the first time and establish an experimental platform. They used fNIRS based cross-brain neurofeedback in an interactive game in which the two participants competed against each other. The target was increasing one’s own brain activity in the left sensorimotor area higher than the opponent’s using kinesthetic motor imagery (in this case pulling a ribbon towards one direction). In this study, both participants had undergone individual neurofeedback training in which they learned how to apply different motor imagery methods. Based on their findings, the authors planned to conduct another cross-brain neurofeedback study to assess the impact of voluntary modulated motor system synchronisation on social behaviour and motor coordination and imitation. However, to date, there is no such study publicly available.
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Salminen et al. (2019) conducted a study in a social biofeedback virtual reality environment. The purpose was to assess how interpersonal respiratory and neural biofeedback during a compassion meditation exercise impacts perceived empathy and interpersonal synchrony. 36 dyads participated in the study. The participant’s empathy-related approach motivation towards the other participant (expressed in frontal asymmetry between EEGs) were depicted. Furthermore, their respiration rates were visualised in different conditions. The two types of biofeedback were either provided isolated (thus only respiratory or only neural) or simultaneously. To assess perceived empathy, the participants rated how much they felt sympathetic, compassionate, soft-hearted, warm, tender, and moved after each condition. The combination condition, hence when provided with respiratory and EEG biofeedback, yielded the biggest impact on empathy ratings. The isolated neurofeedback entailed a higher impact than isolated respiratory biofeedback. Additionally, synchronisation of the EEG frontal asymmetry activities between the two members of the dyad related to increased perceived empathy. These findings suggest that affective cues based on biofeedback yield enhanced empathy, emotional contagion and interpersonal synchronisation which in turn are beneficial for successful collaboration.
Figure 4
fNIRS Cross-Brain Neurofeedback Set-Up
Note. fNIRS Cross-Brain Neurofeedback Set-Up. A) illustration of the set up. B) depicts the experimental set-up with a dyad. From “Cross-brain neurofeedback: scientific concept and experimental platform”, by L. Duan et al., 2013, PLoS One, 8(5), e64590
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In her master thesis, Mende (2017) proposes a study combining EEG hyperscanning and neurofeedback (what I have been referring to as interpersonal neurofeedback) to assess whether brain activity of two participants can synchronise only based on neurofeedback, thus in absence of an additional joint task requiring motor synchrony. Such a study would basically enable to validate how impactful pure targeted interpersonal synchrony in absence of another task is. The proposed study has been conducted, but no results are publicly available as of today.
In a poster presentation, Kerr and colleagues (2020) introduce a study using fMRI based interpersonal neurofeedback with adolescents and a caregiver (see https://www.youtube.com/watch?v=MCOSntsmp6A&feature=youtu.be&ab_channel=klkerr for presentation). The neurofeedback in this pilot study is utilised in a unidirectional fashion. The goal here is for the parents to decrease the right anterior insula activation of their children. This area has been found to be hyperactive in adolescents with depression. While being in the scanner, the adolescent describes an emotionally valenced event and the parent responds while monitoring the right anterior insula activation of their child. So far, the study has been implemented with four dyads. Preliminary findings show an average downward trend of right anterior insula activity indicating emotion regulation in the adolescent generated by the parent’s neurofeedback-altered response.
In the last paper selected for this review, Tennant and colleagues (2019) point out the importance of assessing interpersonal synchrony overtly, thus by using interpersonal biofeedback. By doing so, insights on directionality between interpersonal synchrony and pro-social behaviour could be gained. They propose a study using an interpersonal biofeedback (heart-rate, skin conductance, respiratory activity) device using musical stimuli. They are planning to assess whether hearing biofeedback from the other participant improves the accuracy of emotional judgements. Additionally, they are interested in whether participants show patterns of interpersonal synchrony. And whether this synchrony enhances performance on emotional empathy. The authors suggest that if successful manipulations of synchrony affects empathy, this will support the hypothesis of a causal impact of interpersonal synchrony on prosocial behaviour and social cognition overall.
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The studies presented in this section can be seen as preliminary evidence for the feasibility of interpersonal neurofeedback in laboratory settings to answer specific questions.
3. Discussion
The provided literature compiles evidence and theoretical approaches which highlight the emphasis of interpersonal factors in ASC and illustrates different neurofeedback applications and their potential. To complete the line of argument, I will discuss the limitations of neurofeedback, how focussing on interpersonal synchrony could help solving what I call ‘the imitation issue’, some considerations concerning the application of interpersonal neurofeedback as well as the benefits of interpersonal approaches for the autistic self-image.
Limitations of neurofeedback
Most neurofeedback studies with autistic children reviewed in 2.2.2, lack indications of how many children did actually perform well in neurofeedback training. There is also no indication of whether those who did perform well are actually the ones exhibiting improvement in autistic behaviours. Rather than solely comparing means and standard deviations to control groups, the report of individual outcomes is important. In fact, there is evidence from neurofeedback research indicating that there are ‘regulators’ and ‘non-regulators’, meaning that being able to regulate brain activity using neurofeedback is not a given (Alkoby et al., 2018; Gruzelier, 2014). Furthermore, some studies that applied neurofeedback with autistic children reviewed in 2.2.2 did not assess changes in the children’s EEGs. But took behavioural measures/questionnaires as a mere indication of improvement. However, correlating behavioural measures with changes in EEG is essential to trace back the positive outcomes to neurofeedback training. Otherwise, it can easily be claimed that the positive outcome might as well have derived from being in a therapeutic context or the games played. Regarding these issues, an individual assessment of neurofeedback compatibility and response is crucial when interpreting results.
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As explained, neurofeedback methods might not be feasible for all autistic children. However, it might be possible to benefit from positive effects of modulating cortical activity despite that. Neuromodulatory techniques like transcranial direct current stimulation (tDCS) or transcranial altering current stimulation (tACS) could offer an alternative/addition to neurofeedback training. The evidence available suggests improvement of symptoms and supports tDCS as a feasible method for many neurodevelopmental disorders, in particular when combined with cognitive training (D’Urso et al., 2020). In a review looking at five studies applying tACS with children on the autism spectrum (Osório & Brunoni, 2019), the authors conclude that it is a promising method. In regard to this work’s interest in interpersonal methodology, it is worth mentioning that tASC has also tentatively been used to induce interpersonal neural synchrony. For example, to induce beta band oscillations in dyads performing a finger tapping task (Novembre et al., 2017) or to stimulate right frontal and parietal sites in theta band during dyadic drumming (Szymanski et al., 2017). However, although tASC and tDCS are non-invasive methods, they might leave a negative connotation of ‘electric stimulation of the brain’.
Overall, neurofeedback appears to be the more subtle neuromodulation method in ASC contexts. The active participation it requires furthermore affords a sense of control and agency. When applied interpersonally, it is a joint task to the core, whereas interpersonal tASC and tDCS are inducing interpersonal synchrony externally. But an individual assessment of neurofeedback compatibility should be part of any scientific or therapeutic application of it.
The imitation issue
So called coping mechanisms of individuals with ASC often involve imitating and adapting behaviours that account as socially acceptable. Naturally, social acceptance is something desirable. Caregivers want their children to fit in to prevent them from solitude. And growing up, most children also want to fit in. Therefore, it seems legit that developing coping mechanisms is part of many therapeutic inventions. Especially with autistic children that have regular or only slightly impaired intellectual ability.
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Mimicry is an example of an imitation behaviour that is often conceived as a beneficial coping mechanism. It has been found that automatic mimicry of facial expressions is impaired in ASC (McIntosh et al., 2006). Simple mimicry, thus behaviour that corresponds with and is elicited by observing another person’s behaviour (Hatfield et al., 1992), can be improved by explicit learning which relies on intellectual and metacognitive strategies. Improvement of simple mimicry has undoubtedly proven to help in daily functioning and being socially accepted. But it is automatic, especially emotional mimicry of facial expressions, that is assumed to entail affective empathy/internal simulation of an affective state of the other and emotional contagion. Processes that in turn foster better social understanding (Decety & Chaminade, 2003; Iacoboni, 2005; Oberman et al., 2007). Therefore, teaching coping mechanisms that involve mimicry is not without concern: Apparent social skills of people on the autism spectrum are often based on simple and voluntary mimicry. Thus, imitation that resembles simple copying of perceived acceptable or socially skilled behaviours. As a consequence, these social skills are superficial. Autistic people with higher cognitive abilities and especially females often display particularly strong imitation abilities (Attwood, 2006; Ehlers & Gillberg, 1993; Haney, 2016). Yet, under the surface, autistic individuals that cope well in social situations might experience high levels of subjective stress, anxiety and exhaustion that can lead to an active avoidance of social situations (Allely, 2019). The mismatch between surface imitation and the underlying condition can be referred to as ‘masking’ or ‘camouflaging’. To sum up, generically assuming that mimicry is a desirable ability for autistic people, is wrong and can be harmful.
Interpersonal synchrony can be seen as an alternative measure of social competence. Even if mimicry and interpersonal synchrony share many attributes, they are not the same. Mimicry comprises simple copying of perceived behaviour, it is in itself unilateral. Interpersonal synchrony on the other hand is the dynamic and reciprocal adaptation of the temporal structure of behaviours and states between interactive partners. It requires a constant loop of anticipation and updating those anticipations based on constant flow of input information on many levels (compare predictive processing account, updating priors). Synchronous behaviours are better indicators of similarity and better inducers of affiliation than mimicry (Hove & Risen, 2009).
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Hence, interpersonal synchrony (on several levels) offers a more authentic way of fostering prosocial behaviour, social alignment, interpersonal connectedness, affective empathy and embodied resonance. It can therefore also yield social acceptance but with a lower risk of masking or camouflaging.
Considerations for implementation
For future implementations of interpersonal neurofeedback that have the goal of enhancing social skills, it is important to carefully choose what should be synchronised and how. Findings from hyperscanning studies can be used as indications for target frequencies in interpersonal neurofeedback set-ups. Be it in cooperative games or tasks that comprise simple visual or auditory depiction of interpersonal synchrony.
In many hyperscanning studies, interpersonal synchrony in the alpha band was correlated with social activities or situations, e.g. in social interaction (Dumas et al., 2010), during speaking and listening (Pérez et al., 2018), during hand holding and associated pain reduction (Goldstein et al., 2018), in resting state EEG when being alone vs resting state EEGs recorded when being with another person (Verbeke et al., 2014) or in shared attention (Dikker, Michalareas, et al., 2019). Furthermore, alpha-mu band synchrony between the right centroparietal regions has been suggested to play an important role in social interaction
(Pfurtscheller et al., 2003; Tognoli et al., 2007).
Looking at higher frequencies, the gamma band is also a promising candidate for a synchronised target frequency. A recent EEG hyperscanning study found inter-brain coupling in the gamma band during cooperation. The authors assume synchronised gamma as a marker for shared intentionality (Barraza et al., 2020). Additionally, in an MEG study, mother-children dyads displayed enhanced gamma synchrony while watching previously taped positive natural interactions (Levy et al., 2017). Gamma band activity has also been associated with mentalizing (Cohen et al., 2009) as well as cognitive reappraisal (Kang et al., 2012). Cognitive reappraisal is an emotion regulation strategy that entails changing the affective impact of a stimulus (Naor et al., 2018). This process also plays a role when flexibly interacting with others.
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As emphasised throughout the course of this work, different levels of synchrony interact and impact each other. Thus, heart rate, skin conductance, respiratory activity and movement synchrony biofeedback applications should be considered to be investigated for ASC intervention as well. It is furthermore important to mention that interpersonal neurofeedback and games using multi-person BCIs should not be appraised as replacements for ‘conventional’ approaches to therapy, such as ABA or carefully administered pharmacological therapy. Those can easily be combined and extended with targeted application of interpersonal neurofeedback.
Defeat the narrative of self-responsibility
Unilateral approaches to ASC that emphasise deficient functioning in the individual are not only insufficient to account for real life experience of autistic people but also profoundly harmful for an autistic self-understanding. Children with ASC often grow up to believe that something is wrong with them Or if not wrong, at least special. But even this specialty comes with the idea that it is on them alone to deal with their ‘issues’. To find coping mechanisms and accept if their social environment cannot deal with them the way they deal with non-autistic people. Methods like interpersonal neurofeedback take the focus away from an individual ‘disorder’. When the involvement of the other (be it therapist, caregiver, classmate) is acknowledged, creating a safe, capacity promoting and comfortable social environment from early on becomes an obvious shared effort. Interpersonal approaches and methods offer room for change in therapeutic and educational contexts as well as in the general narrative of otherness. Especially for children, a way of actively working on what makes their lives difficult while acknowledging that it is not ‘just them’ can possibly be highly beneficial. Interpersonal neurofeedback is therefore a promising tool. It can be applied in therapeutic contexts and after training ,also at home with caregivers, siblings, friends etc. Ideally, it would also find a place in educational frameworks with classmates, starting in primary school reaching up to higher education institutions.
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4. Interdisciplinary reflection
The literature reviewed in this work originates from the disciplines cognitive neuroscience, psychiatry, psychology, psychotherapy, philosophy of cognition, art (music, visual art, performance, new media), and the gaming sector. Even though ASC has been a matter of interest for decades, its theorising and the search for neurocognitive markers and causes in psychiatry, psychology and neuroscience has not yielded unambiguous indications and much remains unknown. This is why opening up to theoretical frameworks with a philosophical influence like phenomenology or enactive, embodied, extended, embedded cognition as well as to Bayesian approaches to brain functions or predictive coding are promising ‘new’ additions to ASC research.
Hyperscanning methods and analysis techniques are rapidly advancing in neuroscience, there has been a swift increase of studies looking at more than one brain over the past 10 years. But in artistic contexts as well as in the gaming field, interpersonal neurofeedback set-ups are actually advanced through being more widespread. The combination of increasingly precise hyperscanning methods with interpersonal neurofeedback insights and set-ups from the art and gaming sector should therefore be encouraged. Art and gaming applications furthermore show that strictly structured lab settings are no necessity and thereby encourage the use of more ecological settings for research using neurofeedback. Overall, this work illustrates that it is important to acknowledge insights from different fields to progress, adapt and extend opportunities optimally.
5. Conclusion
The literature provided indicates that social difficulties observed in ASC cannot solely be explained in a unilateral way by divergences in the autistic individual’s behaviour or underlying neurocognitive functioning. Instead, socio-communicative difficulties are manifested in interaction with other people, who thereby play a mutually constitutive role. A lack of interpersonal neural synchronisation can be assumed to play a crucial role in diverging social competence in ASC.
