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

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

The development of body representations: an associative learning account.

Representing one's own body is of fundamental importance to interact with our environment, yet little is known about how body representations develop. One account suggests that the ability to represent one's own body is present from birth and supports infants' ability to detect similarities between their own and others' bodies. However, in recent years evidence has been accumulating for alternative accounts that emphasize the role of multisensory experience obtained through acting and interacting with our own body in the development of body representations. Here, we review this evidence, and propose an integrative account that suggests that through experience, infants form multisensory associations that facilitate the development of body representations. This associative account provides a coherent explanation for previous developmental findings, and generates novel hypotheses for future research.

The developmental trajectory of fronto-temporoparietal connectivity as a proxy of the default mode network: a longitudinal fNIRS investigation.

The default mode network (DMN) is a network of brain regions that is activated while we are not engaged in any particular task. While there is a large volume of research documenting functional connectivity within the DMN in adults, knowledge of the development of this network is still limited. There is some evidence for a gradual increase in the functional connections within the DMN during the first 2 years of life, in contrast to other functional resting-state networks that support primary sensorimotor functions, which are online from very early in life. Previous studies that investigated the development of the DMN acquired data from sleeping infants using fMRI. However, sleep stages are known to affect functional connectivity. In the current longitudinal study, fNIRS was used to measure spontaneous fluctuations in connectivity within fronto-temporoparietal areas-as a proxy for the DMN-in awake participants every 6 months from 11 months till 36 months. This study validates a method for recording resting-state data from awake infants, and presents a data analysis pipeline for the investigation of functional connections with infant fNIRS data, which will be beneficial for researchers in this field. A gradual development of fronto-temporoparietal connectivity was found, supporting the idea that the DMN develops over the first years of life. Functional connectivity reached its maximum peak at about 24 months, which is consistent with previous findings showing that, by 2 years of age, DMN connectivity is similar to that observed in adults.

The role of sensorimotor experience in the development of mimicry in infancy.

During social interactions we often have an automatic and unconscious tendency to copy or 'mimic' others' actions. The dominant view on the neural basis of mimicry appeals to an automatic coupling between perception and action. It has been suggested that this coupling is formed through associative learning during correlated sensorimotor experience. Although studies with adult participants have provided support for this hypothesis, little is known about the role of sensorimotor experience in supporting the development of perceptual-motor couplings, and consequently mimicry behaviour, in infancy. Here we investigated whether the extent to which an observed action elicits mimicry depends on the opportunity an infant has had to develop perceptual-motor couplings for this action through correlated sensorimotor experience. We found that mothers' tendency to imitate their 4-month-olds' facial expressions during a parent-child interaction session was related to infants' facial mimicry as measured by electromyography. Maternal facial imitation was not related to infants' mimicry of hand actions, and instead we found preliminary evidence that infants' tendency to look at their own hands may be related to their tendency to mimic hand actions. These results are consistent with the idea that mimicry is supported by perceptual-motor couplings that are formed through correlated sensorimotor experience obtained by observing one's own actions and imitative social partners.

Selective facial mimicry of native over foreign speakers in preverbal infants.

Mimicry, the spontaneous copying of others' behaviors, plays an important role in social affiliation, with adults selectively mimicking in-group members over out-group members. Despite infants' early documented sensitivity to cues to group membership, previous work suggests that it is not until 4 years of age that spontaneous mimicry is modulated by group status. Here we demonstrate that mimicry is sensitive to cues to group membership at a much earlier age if the cues presented are more relevant to infants. 11-month-old infants observed videos of facial actions (e.g., mouth opening, eyebrow raising) performed by models who either spoke the infants' native language or an unfamiliar foreign language while we measured activation of the infants' mouth and eyebrow muscle regions using electromyography to obtain an index of mimicry. We simultaneously used functional near-infrared spectroscopy to investigate the neural mechanisms underlying differential mimicry responses. We found that infants showed greater facial mimicry of the native speaker compared to the foreign speaker and that the left temporal parietal cortex was activated more strongly during the observation of facial actions performed by the native speaker compared to the foreign speaker. Although the exact mechanisms underlying this selective mimicry response will need to be investigated in future research, these findings provide the first demonstration of the modulation of facial mimicry by cues to group status in preverbal infants and suggest that the foundations for the role that mimicry plays in facilitating social bonds seem to be present during the first year of life.

Dynamic causal modelling on infant fNIRS data: A validation study on a simultaneously recorded fNIRS-fMRI dataset.

Tracking the connectivity of the developing brain from infancy through childhood is an area of increasing research interest, and fNIRS provides an ideal method for studying the infant brain as it is compact, safe and robust to motion. However, data analysis methods for fNIRS are still underdeveloped compared to those available for fMRI. Dynamic causal modelling (DCM) is an advanced connectivity technique developed for fMRI data, that aims to estimate the coupling between brain regions and how this might be modulated by changes in experimental conditions. DCM has recently been applied to adult fNIRS, but not to infants. The present paper provides a proof-of-principle for the application of this method to infant fNIRS data and a demonstration of the robustness of this method using a simultaneously recorded fMRI-fNIRS single case study, thereby allowing the use of this technique in future infant studies. fMRI and fNIRS were simultaneously recorded from a 6-month-old sleeping infant, who was presented with auditory stimuli in a block design. Both fMRI and fNIRS data were preprocessed using SPM, and analysed using a general linear model approach. The main challenges that adapting DCM for fNIRS infant data posed included: (i) the import of the structural image of the participant for spatial pre-processing, (ii) the spatial registration of the optodes on the structural image of the infant, (iii) calculation of an accurate 3-layer segmentation of the structural image, (iv) creation of a high-density mesh as well as (v) the estimation of the NIRS optical sensitivity functions. To assess our results, we compared the values obtained for variational Free Energy (F), Bayesian Model Selection (BMS) and Bayesian Model Average (BMA) with the same set of possible models applied to both the fMRI and fNIRS datasets. We found high correspondence in F, BMS, and BMA between fMRI and fNIRS data, therefore showing for the first time high reliability of DCM applied to infant fNIRS data. This work opens new avenues for future research on effective connectivity in infancy by contributing a data analysis pipeline and guidance for applying DCM to infant fNIRS data.

Baby steps: investigating the development of perceptual-motor couplings in infancy.

There are cells in our motor cortex that fire both when we perform and when we observe similar actions. It has been suggested that these perceptual-motor couplings in the brain develop through associative learning during correlated sensorimotor experience. Although studies with adult participants have provided support for this hypothesis, there is no direct evidence that associative learning also underlies the initial formation of perceptual-motor couplings in the developing brain. With the present study we addressed this question by manipulating infants' opportunities to associate the visual and motor representation of a novel action, and by investigating how this influenced their sensorimotor cortex activation when they observed this action performed by others. Pre-walking 7-9-month-old infants performed stepping movements on an infant treadmill while they either observed their own real-time leg movements (Contingent group) or the previously recorded leg movements of another infant (Non-contingent control group). Infants in a second control group did not perform any steps and only received visual experience with the stepping actions. Before and after the training period we measured infants' sensorimotor alpha suppression, as an index of sensorimotor cortex activation, while they watched videos of other infants' stepping actions. While we did not find greater sensorimotor alpha suppression following training in the Contingent group as a whole, we nevertheless found that the strength of the visuomotor contingency experienced during training predicted the amount of sensorimotor alpha suppression at post-test in this group. We did not find any effects of motor experience alone. These results suggest that the development of perceptual-motor couplings in the infant brain is likely to be supported by associative learning during correlated visuomotor experience.

Face engagement during infancy predicts later face recognition ability in younger siblings of children with autism.

Face recognition difficulties are frequently documented in children with autism spectrum disorders (ASD). It has been hypothesized that these difficulties result from a reduced interest in faces early in life, leading to decreased cortical specialization and atypical development of the neural circuitry for face processing. However, a recent study by our lab demonstrated that infants at increased familial risk for ASD, irrespective of their diagnostic status at 3 years, exhibit a clear orienting response to faces. The present study was conducted as a follow-up on the same cohort to investigate how measures of early engagement with faces relate to face-processing abilities later in life. We also investigated whether face recognition difficulties are specifically related to an ASD diagnosis, or whether they are present at a higher rate in all those at familial risk. At 3 years we found a reduced ability to recognize unfamiliar faces in the high-risk group that was not specific to those children who received an ASD diagnosis, consistent with face recognition difficulties being an endophenotype of the disorder. Furthermore, we found that longer looking at faces at 7 months was associated with poorer performance on the face recognition task at 3 years in the high-risk group. These findings suggest that longer looking at faces in infants at risk for ASD might reflect early face-processing difficulties and predicts difficulties with recognizing faces later in life.

Fronto-temporoparietal connectivity and self-awareness in 18-month-olds: A resting state fNIRS study.

How and when a concept of the 'self' emerges has been the topic of much interest in developmental psychology. Self-awareness has been proposed to emerge at around 18 months, when toddlers start to show evidence of physical self-recognition. However, to what extent physical self-recognition is a valid indicator of being able to think about oneself, is debated. Research in adult cognitive neuroscience has suggested that a common network of brain regions called Default Mode Network (DMN), including the temporo-parietal junction (TPJ) and the medial prefrontal cortex (mPFC), is recruited when we are reflecting on the self. We hypothesized that if mirror self-recognition involves self-awareness, toddlers who exhibit mirror self-recognition might show increased functional connectivity between frontal and temporoparietal regions of the brain, relative to those toddlers who do not yet show mirror self-recognition. Using fNIRS, we collected resting-state data from 18 Recognizers and 22 Non-Recognizers at 18 months of age. We found significantly stronger fronto-temporoparietal connectivity in Recognizers compared to Non-Recognizers, a finding which might support the hypothesized relationship between mirror-self recognition and self-awareness in infancy.

Eye contact modulates facial mimicry in 4-month-old infants: An EMG and fNIRS study.

Mimicry, the tendency to spontaneously and unconsciously copy others' behaviour, plays an important role in social interactions. It facilitates rapport between strangers, and is flexibly modulated by social signals, such as eye contact. However, little is known about the development of this phenomenon in infancy, and it is unknown whether mimicry is modulated by social signals from early in life. Here we addressed this question by presenting 4-month-old infants with videos of models performing facial actions (e.g., mouth opening, eyebrow raising) and hand actions (e.g., hand opening and closing, finger actions) accompanied by direct or averted gaze, while we measured their facial and hand muscle responses using electromyography to obtain an index of mimicry (Experiment 1). In Experiment 2 the infants observed the same stimuli while we used functional near-infrared spectroscopy to investigate the brain regions involved in modulating mimicry by eye contact. We found that 4-month-olds only showed evidence of mimicry when they observed facial actions accompanied by direct gaze. Experiment 2 suggests that this selective facial mimicry may have been associated with activation over posterior superior temporal sulcus. These findings provide the first demonstration of modulation of mimicry by social signals in young human infants, and suggest that mimicry plays an important role in social interactions from early in life.

An EEG study on the somatotopic organisation of sensorimotor cortex activation during action execution and observation in infancy.

Previous studies have shown that sensorimotor cortex activation is somatotopically-organised during action execution and observation in adulthood. Here we aimed to investigate the development of this phenomenon in infancy. We elicited arm and leg actions from 12-month-old infants and presented them, and a control group of adults, with videos of arm and leg actions while we measured their sensorimotor alpha suppression using EEG. Sensorimotor alpha suppression during action execution was somatotopically organised in 12-month-old infants: there was more suppression over the arm areas when infants performed reaching actions, and more suppression over the leg area when they performed kicking actions. Adults also showed somatotopically-organised activation during the observation of reaching and kicking actions. In contrast, infants did not show somatotopically-organised activation during action observation, but instead activated the arm areas when observing both reaching and kicking actions. We suggest that the somatotopic organisation of sensorimotor cortex activation during action observation may depend on infants' understanding of the action goal and their expectations about how this goal will be achieved.