Re-examination of Oostenbroek et al. (2016): evidence for neonatal imitation of tongue protrusion.

The meaning, mechanism, and function of imitation in early infancy have been actively discussed since Meltzoff and Moore's (1977) report of facial and manual imitation by human neonates. Oostenbroek et al. (2016) claim to challenge the existence of early imitation and to counter all interpretations so far offered. Such claims, if true, would have implications for theories of social-cognitive development. Here we identify 11 flaws in Oostenbroek et al.'s experimental design that biased the results toward null effects. We requested and obtained the authors' raw data. Contrary to the authors' conclusions, new analyses reveal significant tongue-protrusion imitation at all four ages tested (1, 3, 6, and 9 weeks old). We explain how the authors missed this pattern and offer five recommendations for designing future experiments. Infant imitation raises fundamental issues about action representation, social learning, and brain-behavior relations. The debate about the origins and development of imitation reflects its importance to theories of developmental science.

Perception-action coupling and imitation in autism spectrum disorder.

This paper focuses on the key function of imitation in motor and social development of typically developing infants and low-functioning children with autism spectrum disorder (ASD). We suggest that it might also be a developmental cornerstone for other neurodevelopmental disorders. Why this suggestion? First, imitation just requires relating one's motor patterns to perceived motor patterns. This is always possible if the actions seen are not beyond the individual's motor scope; for instance, newborn infants can already imitate tongue protrusion, eye blinking, or mouth opening, because these movements are part of their foetal repertoire. Second, imitation is a 'use it or lose it' capacity: the more it is used, the more the repertoire grows (plasticity). Finally, imitation is an efficient tool for two main adaptive functions: learning and communication. Imitation-based communication is available through the use of the two facets of imitation: imitating and being imitated. The two facets afford two roles that the partners can exchange as a turn-taking while they synchronize matched activities. Neuroimaging studies of interactive imitation have shown that such communicative systems involve a coordination of bottom-up and top-down processes. In this line, imitation is a booster of development that can also be of benefit for children with neurodevelopmental disorders.

Mirror Neuron System and Mentalizing System connect during online social interaction.

Two sets of brain areas are repeatedly reported in neuroimaging studies on social cognition: the Mirror Neuron System and the Mentalizing System. The Mirror System is involved in goal understanding and has been associated with several emotional and cognitive functions central to social interaction, ranging from empathy to gestural communication and imitation. The Mentalizing System is recruited in tasks requiring cognitive processes such as self-reference and understanding of other's intentions. Although theoretical accounts for an interaction between the two systems have been proposed, little is known about their synergy during social exchanges. In order to explore this question, we have recorded brain activity by means of functional MRI during live social exchanges based on reciprocal imitation of hand gestures. Here, we investigate, using the method of psychophysiological interaction, the changes in functional connectivity of the Mirror System due to the conditions of interest (being imitated, imitating) compared with passive observation of hand gestures. We report a strong coupling between the Mirror System and the Mentalizing System during the imitative exchanges. Our findings suggest a complementary role of the two networks during social encounters. The Mirror System would engage in the preparation of own actions and the simulation of other's actions, while the Mentalizing System would engage in the anticipation of the other's intention and thus would participate to the co-regulation of reciprocal actions. Beyond a specific effect of imitation, the design used offers the opportunity to tackle the role of role-switching in an interpersonal account of social cognition.

Distinct social behavior and inter-brain connectivity in Dyads with autistic individuals.

Autism Spectrum Disorder (ASD) is defined by distinctive socio-cognitive behaviors that deviate from typical patterns. Notably, social imitation skills appear to be particularly impacted, manifesting early on in development. This paper compared the behavior and inter-brain dynamics of dyads made up of two typically developing (TD) participants with mixed dyads made up of ASD and TD participants during social imitation tasks. By combining kinematics and EEG-hyperscanning, we show that individuals with ASD exhibited a preference for the follower rather than the lead role in imitating scenarios. Moreover, the study revealed inter-brain synchrony differences, with low-alpha inter-brain synchrony differentiating control and mixed dyads. The study's findings suggest the importance of studying interpersonal phenomena in dynamic and ecological settings and using hyperscanning methods to capture inter-brain dynamics during actual social interactions.

Reciprocal imitation: toward a neural basis of social interaction.

Social interaction is a coregulated coupling activity that involves at least 2 autonomous agents. Numerous methodological and technical challenges impede the production of natural social interaction within an Magnetic Resonance Imaging environment under controlled conditions. To overcome the obstacle, we chose a simple format of social interaction, namely "interactive imitation" through a double-video system. We registered blood oxygen level-dependent activity of 23 participants during 2 imitative conditions: free (F) and instructed (I) episodes of imitating (i) and of being imitated (bi). In addition to the areas classically reported in instructed imitation tasks, 2 activation patterns were found, which differentiate the subconditions. Firstly, brain areas involved during decisional and attentional processes (dorsolateral prefrontal cortex , dorsal part of anterior cingulate gyrus [dACC], pre-SMA) were activated during all conditions except for instructed imitation-classically used in neuroimaging studies of imitation. Second, a greater activation in dACC and insula combined with an increased deactivation in the default mode network was observed when subjects were imitated compared with when they imitated. We suggest that these 2 patterns reflect the anticipation of the other's behavior and the engagement with others required by social interaction.

Human newborns match tongue protrusion of disembodied human and robotic mouths.

No evidence had been provided so far of newborns' capacity to give a matching response to 2D stimuli. We report evidence from 18 newborns who were presented with three types of stimuli on a 2D screen. The stimuli were video-recorded displays of tongue protrusion shown by: (a) a human face, (b) a human tongue from a disembodied mouth, and (c) an artificial tongue from a robotic mouth. Compared to a baseline condition, neonates increased significantly their tongue protrusion when seeing disembodied human and artificial tongue movements, but not when seeing a 2D full-face protruding tongue. This result was interpreted as revealing the exploration of top-heavy patterns of the 2D face that distracted infants' attention from the tongue. Results also showed progressively more accurate matching (full tongue protrusion) throughout repeated exposure to each kind of stimulus. Such findings are not in line with the predictions of the innate releasing mechanism (IRM) model or of the oral exploration hypothesis. They support the active intermodal mapping (AIM) hypothesis that emphasizes not only the importance of repeated experience, as would the associative sequence learning (ASL) hypothesis, but also predicts a differential learning and progressive correction of the response adapted to each stimulus.

Shall We Play the Same? Pedagogical Perspectives on Infants' and Children's Imitation of Musical Gestures.

Imitation, both gestural and vocal, has been acknowledged to be at the origin of human communication (Donald, 1991). Music is often considered to be the first means of communication of emotion via both vocal and gestural synchronization (Malloch, 1999; Malloch and Trevarthen, 2009). Instrumental music is part of the human heritage for more than 35,000 years before our era (Aimé et al., 2020). However, very little is known about the acquisition of gestures that produce sounds (i.e., musical gestures) and their role in the development of music and musicality. In the present paper, we propose that studying early synchronous imitation of musical gestures is essential both for investigating the development of the early action-perception system and for outlining early music interventions during infancy. We designed double musical objects which can be used in preschool music education for prompting synchronic imitation of musical gestures between adult and child, and between dyads of infants. We conclude by proposing a novel pedagogical perspective in music education for the early years which links the privileged orientation of infants and children towards sound discoveries with the development of perception-action coupling via imitation of musical gestures.

Building Robota, a mini-humanoid robot for the rehabilitation of children with autism.

The Robota project constructs a series of multiple-degrees-of-freedom, doll-shaped humanoid robots, whose physical features resemble those of a human baby. The Robota robots have been applied as assistive technologies in behavioral studies with low-functioning children with autism. These studies investigate the potential of using an imitator robot to assess children's imitation ability and to teach children simple coordinated behaviors. In this article, the authors review the recent technological developments that have made the Robota robots suitable for use with children with autism. They critically appraise the main outcomes of two sets of behavioral studies conducted with Robota and discuss how these results inform future development of the Robota robots and robots in general for the rehabilitation of children with complex developmental disabilities.

Morphing technique reveals intact perception of object motion and disturbed perception of emotional expressions by low-functioning adolescents with Autism Spectrum Disorder.

A morphing procedure has been designed to compare directly the perception of emotional expressions and of moving objects. Morphing tasks were presented to 12 low-functioning teenagers with Autism Spectrum Disorder (LF ASD) compared to 12 developmental age-matched typical children and a group presenting ceiling performance. In a first study, when presented with morphed stimuli of objects and emotional faces, LF ASD showed an intact perception of object change of state together with an impaired perception of emotional facial change of state. In a second study, an eye-tracker recorded visual exploration of morphed emotional stimuli displayed by a human face and a robotic set-up. Facing the morphed robotic stimuli, LF ASD displayed equal duration of fixations toward emotional regions and toward mechanical sources of motion, while the typical groups tracked the emotional regions only. Altogether the findings of the two studies suggest that individuals with ASD process motion rather than emotional signals when facing facial expressions.

Brief report: imitation effects on children with autism.

Twenty children with autism (mean age, 5 years) were recruited for the study from a school for children with autism. The children were randomly assigned to an imitation (n = 10) or contingently responsive (n = 10) interaction group based on a stratification table for gender and developmental and chronological age. The sessions consisted of four phases, with each phase lasting 3 minutes. In the first phase, the child walked into a room that was furnished with a sofa, a table, chairs, and two sets of identical toys. An adult was in the room sitting very still like a statue (first still-face condition). In the second phase, the adult either imitated the child or was contingently responsive to the child. In the third phase, the adult sat still again (second still-face condition), and in the fourth phase, the adult engaged in a spontaneous interaction. During the third phase (the second still-face condition), the children in the imitation group spent less time in gross motor activity and more time touching the adult, as if attempting to initiate an interaction. The contingency condition appeared to be a more effective way to facilitate a distal social behavior (attention), whereas the imitative condition was a more effective way to facilitate a proximal social behavior (touching).

An eye-tracking method to reveal the link between gazing patterns and pragmatic abilities in high functioning autism spectrum disorders.

The present study illustrates the potential advantages of an eye-tracking method for exploring the association between visual scanning of faces and inferences of mental states. Participants watched short videos involving social interactions and had to explain what they had seen. The number of cognition verbs (e.g., think, believe, know) in their answers were counted. Given the possible use of peripheral vision that could confound eye-tracking measures, we added a condition using a gaze-contingent viewing window: the entire visual display is blurred, expect for an area that moves with the participant's gaze. Eleven typical adults and eleven high functioning adults with Autism Spectrum Disorders (ASD) were recruited. The condition employing the viewing window yielded strong correlations between the average duration of fixations, the ratio of cognition verbs and standard measures of social disabilities.

Revisiting mu suppression in autism spectrum disorder.

Two aspects of the EEG literature lead us to revisit mu suppression in Autism Spectrum Disorder (ASD). First and despite the fact that the mu rhythm can be functionally segregated in two discrete sub-bands, 8-10 Hz and 10-12/13 Hz, mu-suppression in ASD has been analyzed as a homogeneous phenomenon covering the 8-13 Hz frequency. Second and although alpha-like activity is usually found across the entire scalp, ASD studies of action observation have focused on the central electrodes (C3/C4). The present study was aimed at testing on the whole brain the hypothesis of a functional dissociation of mu and alpha responses to the observation of human actions in ASD according to bandwidths. Electroencephalographic (EEG) mu and alpha responses to execution and observation of hand gestures were recorded on the whole scalp in high functioning subjects with ASD and typical subjects. When two bandwidths of the alpha-mu 8-13 Hz were distinguished, a different mu response to observation appeared for subjects with ASD in the upper sub-band over the sensorimotor cortex, whilst the lower sub-band responded similarly in the two groups. Source reconstructions demonstrated that this effect was related to a joint mu-suppression deficit over the occipito-parietal regions and an increase over the frontal regions. These findings suggest peculiarities in top-down response modulation in ASD and question the claim of a global dysfunction of the MNS in autism. This research also advocates for the use of finer grained analyses at both spatial and spectral levels for future directions in neurophysiological accounts of autism.

Understanding goals and intentions in low-functioning autism.

We investigated ability to understand goals and attribute intentions in the context of two imitation studies in low-functioning, nonverbal children with autism (L-F CWA), a population that is rarely targeted by research in the domain. Down syndrome children (DSC) and typically developing children (TDC) were recruited to form matched comparison groups. In the two sets of simple action demonstrations only contextual indicators of the model's intentions were manipulated. In the Head touch experiment the model activated a button on a toy by pushing it with the forehead, whereas in the Hidden box experiment the model used a ball with a magnet to lift a box out of its container. Both actions were unusual and non-affordant with regards to the objects involved, none of the children in the baseline condition produced them. L-F CWA imitated the experimenter exactly, regardless of the model's intention. TDC showed appreciation of the model's intention by imitating her actions selectively. DSC reproduced only the intentional action as often as they imitated the experimenter exactly. It is concluded that L-F CWA attributed goals to the observed model, but did not show an appreciation of the model's intentions even in these simplified, nonverbal contexts.

Social orienting of children with autism to facial expressions and speech: a study with a wearable eye-tracker in naturalistic settings.

This study investigates attention orienting to social stimuli in children with Autism Spectrum Conditions (ASC) during dyadic social interactions taking place in real-life settings. We study the effect of social cues that differ in complexity and distinguish between social cues produced by facial expressions of emotion and those produced during speech. We record the children's gazes using a head-mounted eye-tracking device and report on a detailed and quantitative analysis of the motion of the gaze in response to the social cues. The study encompasses a group of children with ASC from 2 to 11-years old (n = 14) and a group of typically developing (TD) children (n = 17) between 3 and 6-years old. While the two groups orient overtly to facial expressions, children with ASC do so to a lesser extent. Children with ASC differ importantly from TD children in the way they respond to speech cues, displaying little overt shifting of attention to speaking faces. When children with ASC orient to facial expressions, they show reaction times and first fixation lengths similar to those presented by TD children. However, children with ASC orient to speaking faces slower than TD children. These results support the hypothesis that individuals affected by ASC have difficulties processing complex social sounds and detecting intermodal correspondence between facial and vocal information. It also corroborates evidence that people with ASC show reduced overt attention toward social stimuli.

Investigating gaze of children with ASD in naturalistic settings.

BACKGROUND: Visual behavior is known to be atypical in Autism Spectrum Disorders (ASD). Monitor-based eye-tracking studies have measured several of these atypicalities in individuals with Autism. While atypical behaviors are known to be accentuated during natural interactions, few studies have been made on gaze behavior in natural interactions. In this study we focused on i) whether the findings done in laboratory settings are also visible in a naturalistic interaction; ii) whether new atypical elements appear when studying visual behavior across the whole field of view. METHODOLOGY/PRINCIPAL FINDINGS: Ten children with ASD and ten typically developing children participated in a dyadic interaction with an experimenter administering items from the Early Social Communication Scale (ESCS). The children wore a novel head-mounted eye-tracker, measuring gaze direction and presence of faces across the child's field of view. The analysis of gaze episodes to faces revealed that children with ASD looked significantly less and for shorter lapses of time at the experimenter. The analysis of gaze patterns across the child's field of view revealed that children with ASD looked downwards and made more extensive use of their lateral field of view when exploring the environment. CONCLUSIONS/SIGNIFICANCE: The data gathered in naturalistic settings confirm findings previously obtained only in monitor-based studies. Moreover, the study allowed to observe a generalized strategy of lateral gaze in children with ASD when they were looking at the objects in their environment.

Investigating social gaze as an action-perception online performance.

Gaze represents a major non-verbal communication channel in social interactions. In this respect, when facing another person, one's gaze should not be examined as a purely perceptive process but also as an action-perception online performance. However, little is known about processes involved in the real-time self-regulation of social gaze. The present study investigates the impact of a gaze-contingent viewing window on fixation patterns and the awareness of being the agent moving the window. In face-to-face scenarios played by a virtual human character, the task for the 18 adult participants was to interpret an equivocal sentence which could be disambiguated by examining the emotional expressions of the character speaking. The virtual character was embedded in naturalistic backgrounds to enhance realism. Eye-tracking data showed that the viewing window induced changes in gaze behavior, notably longer visual fixations. Notwithstanding, only half of the participants ascribed the window displacements to their eye movements. These participants also spent more time looking at the eyes and mouth regions of the virtual human character. The outcomes of the study highlight the dissociation between non-volitional gaze adaptation and the self-ascription of agency. Such dissociation provides support for a two-step account of the sense of agency composed of pre-noetic monitoring mechanisms and reflexive processes, linked by bottom-up and top-down processes. We comment upon these results, which illustrate the relevance of our method for studying online social cognition, in particular concerning autism spectrum disorders (ASD) where the poor pragmatic understanding of oral speech is considered linked to visual peculiarities that impede facial exploration.

Does the brain know who is at the origin of what in an imitative interaction?

Brain correlates of the sense of agency have recently received increased attention. However, the explorations remain largely restricted to the study of brains in isolation. The prototypical paradigm used so far consists of manipulating visual perception of own action while asking the subject to draw a distinction between self- versus externally caused action. However, the recent definition of agency as a multifactorial phenomenon combining bottom-up and top-down processes suggests the exploration of more complex situations. Notably there is a need of accounting for the dynamics of agency in a two-body context where we often experience the double faceted question of who is at the origin of what in an ongoing interaction. In a dyadic context of role switching indeed, each partner can feel body ownership, share a sense of agency and altogether alternate an ascription of the primacy of action to self and to other. To explore the brain correlates of these different aspects of agency, we recorded with dual EEG and video set-ups 22 subjects interacting via spontaneous versus induced imitation (II) of hand movements. The differences between the two conditions lie in the fact that the roles are either externally attributed (induced condition) or result from a negotiation between subjects (spontaneous condition). Results demonstrate dissociations between self- and other-ascription of action primacy in delta, alpha and beta frequency bands during the condition of II. By contrast a similar increase in the low gamma frequency band (38-47 Hz) was observed over the centro-parietal regions for the two roles in spontaneous imitation (SI). Taken together, the results highlight the different brain correlates of agency at play during live interactions.

Anatomical connectivity influences both intra- and inter-brain synchronizations.

Recent development in diffusion spectrum brain imaging combined to functional simulation has the potential to further our understanding of how structure and dynamics are intertwined in the human brain. At the intra-individual scale, neurocomputational models have already started to uncover how the human connectome constrains the coordination of brain activity across distributed brain regions. In parallel, at the inter-individual scale, nascent social neuroscience provides a new dynamical vista of the coupling between two embodied cognitive agents. Using EEG hyperscanning to record simultaneously the brain activities of subjects during their ongoing interaction, we have previously demonstrated that behavioral synchrony correlates with the emergence of inter-brain synchronization. However, the functional meaning of such synchronization remains to be specified. Here, we use a biophysical model to quantify to what extent inter-brain synchronizations are related to the anatomical and functional similarity of the two brains in interaction. Pairs of interacting brains were numerically simulated and compared to real data. Results show a potential dynamical property of the human connectome to facilitate inter-individual synchronizations and thus may partly account for our propensity to generate dynamical couplings with others.