Bursting with Potential: How Sensorimotor Beta Bursts Develop from Infancy to Adulthood.

Beta activity is thought to play a critical role in sensorimotor processes. However, little is known about how activity in this frequency band develops. Here, we investigated the developmental trajectory of sensorimotor beta activity from infancy to adulthood. We recorded EEG from 9-month-old, 12-month-old, and adult humans (male and female) while they observed and executed grasping movements. We analyzed "beta burst" activity using a novel method that combines time-frequency decomposition and principal component analysis. We then examined the changes in burst rate and waveform motifs along the selected principal components. Our results reveal systematic changes in beta activity during action execution across development. We found a decrease in beta burst rate during movement execution in all age groups, with the greatest decrease observed in adults. Additionally, we identified three principal components that defined waveform motifs that systematically changed throughout the trial. We found that bursts with waveform shapes closer to the median waveform were not rate-modulated, whereas those with waveform shapes further from the median were differentially rate-modulated. Interestingly, the decrease in the rate of certain burst motifs occurred earlier during movement and was more lateralized in adults than in infants, suggesting that the rate modulation of specific types of beta bursts becomes increasingly refined with age.SIGNIFICANCE STATEMENT We demonstrate that, like in adults, sensorimotor beta activity in infants during reaching and grasping movements occurs in bursts, not oscillations like thought traditionally. Furthermore, different beta waveform shapes were differentially modulated with age, including more lateralization in adults. Aberrant beta activity characterizes various developmental disorders and motor difficulties linked to early brain injury, so looking at burst waveform shape could provide more sensitivity for early identification and treatment of affected individuals before any behavioral symptoms emerge. More generally, comparison of beta burst activity in typical versus atypical motor development will also be instrumental in teasing apart the mechanistic functional roles of different types of beta bursts.

Bayesian multilevel hidden Markov models identify stable state dynamics in longitudinal recordings from macaque primary motor cortex.

Neural populations, rather than single neurons, may be the fundamental unit of cortical computation. Analysing chronically recorded neural population activity is challenging not only because of the high dimensionality of activity but also because of changes in the signal that may or may not be due to neural plasticity. Hidden Markov models (HMMs) are a promising technique for analysing such data in terms of discrete latent states, but previous approaches have not considered the statistical properties of neural spiking data, have not been adaptable to longitudinal data, or have not modelled condition-specific differences. We present a multilevel Bayesian HMM addresses these shortcomings by incorporating multivariate Poisson log-normal emission probability distributions, multilevel parameter estimation and trial-specific condition covariates. We applied this framework to multi-unit neural spiking data recorded using chronically implanted multi-electrode arrays from macaque primary motor cortex during a cued reaching, grasping and placing task. We show that, in line with previous work, the model identifies latent neural population states which are tightly linked to behavioural events, despite the model being trained without any information about event timing. The association between these states and corresponding behaviour is consistent across multiple days of recording. Notably, this consistency is not observed in the case of a single-level HMM, which fails to generalise across distinct recording sessions. The utility and stability of this approach is demonstrated using a previously learned task, but this multilevel Bayesian HMM framework would be especially suited for future studies of long-term plasticity in neural populations.

Detection and analysis of cortical beta bursts in developmental EEG data.

Developmental EEG research often involves analyzing signals within various frequency bands, based on the assumption that these signals represent oscillatory neural activity. However, growing evidence suggests that certain frequency bands are dominated by transient burst events in single trials rather than sustained oscillations. This is especially true for the beta band, with adult 'beta burst' timing a better predictor of motor behavior than slow changes in average beta amplitude. No developmental research thus far has looked at beta bursts, with techniques used to investigate frequency-specific activity structure rarely even applied to such data. Therefore, we aimed to: i) provide a tutorial for developmental EEG researchers on the application of methods for evaluating the rhythmic versus transient nature of frequency-specific activity; and ii) use these techniques to investigate the existence of sensorimotor beta bursts in infants. We found that beta activity in 12-month-olds did occur in bursts, however differences were also revealed in terms of duration, amplitude, and rate during grasping compared to adults. Application of the techniques illustrated here will be critical for clarifying the functional roles of frequency-specific activity across early development, including the role of beta activity in motor processing and its contribution to differing developmental motor trajectories.

Social touch alters newborn monkey behavior.

In humans, infants respond positively to slow, gentle stroking-processed by C-tactile (CT) nerve fibers-by showing reductions in stress and increases in eye contact, smiling, and positive vocalizations. More frequent maternal touch is linked to greater activity and connectivity strength in social brain regions, and increases children's attention to and learning of faces. It has been theorized that touch may prime children for social interactions and set them on a path towards healthy social cognitive development. However, less is known about the effects of touch on young infants' psychological development, especially in the newborn period, a highly sensitive period of transition with rapid growth in sensory and social processing. It remains untested whether newborns can distinguish CT-targeted touch from other types of touch, or whether there are benefits of touch for newborns' social, emotional, or cognitive development. In the present study, we experimentally investigated the acute effects of touch in newborn monkeys, a common model for human social development. Rhesus macaques (Macaca mulatta), like humans, are highly social, have complex mother-infant interactions with frequent body contact for the first weeks of life, making them an excellent model of infant sociality. Infant monkeys in the present study were reared in a neonatal nursery, enabling control over their early environment, including all caregiver interactions. One-week-old macaque infants (N = 27) participated in three 5-minute counter-balanced caregiver interactions, all with mutual gaze: stroking head and shoulders (CT-targeted touch), stroking palms of hands and soles of feet (Non-CT touch), or no stroking (No-touch). Immediately following the interaction, infants watched social and nonsocial videos and picture arrays including faces and objects, while we tracked their visual attention with remote eye tracking. We found that, during the caregiver interactions, infants behaved differently while being touched compared to the no-touch condition, irrespective of the body part touched. Most notably, in both touch conditions, infants exhibited fewer stress-related behaviors-self-scratching, locomotion, and contact time with a comfort object-compared to when they were not touched. Following CT-targeted touch, infants were faster to orient to the picture arrays compared to the other interaction conditions, suggesting CT-targeted touch may activate or prime infants' attentional orienting system. In the No-touch condition infants attended longer to the nonsocial compared to the social video, possibly reflecting a baseline preference for nonsocial stimuli. In contrast, in both touch conditions, infants' looked equally to the social and nonsocial videos, suggesting that touch may influence the types of visual stimuli that hold infants' attention. Collectively, our results reveal that newborn macaques responded positively to touch, and touch appeared to influence some aspects of their subsequent attention, although we found limited evidence that these effects are mediated by CT fibers. These findings suggest that newborn touch may broadly support infants' psychological development, and may have early evolutionary roots, shared across primates. This study illustrates the unique insight offered by nonhuman primates for exploring early infant social touch, revealing that touch may positively affect emotional and attentional development as early as the newborn period.

Building blocks of joint attention: Early sensitivity to having one's own gaze followed.

Detecting when one's own gaze has been followed is a critical component of joint attention, but little is known about its development. To address this issue, we used electroencephalography (EEG) to record infant neural responses at 6.5 and 9.5 months during observation of an adult either turning to look at the same object as the infant (congruent actor), or turning to look at a different object (incongruent actor). We also used a preferential looking paradigm to investigate whether infants would demonstrate a preference for the congruent versus incongruent actor. Greater suppression of alpha band activity in the congruent compared to incongruent condition was revealed at both ages in central and parietal regions. However, the effect of congruency on alpha suppression was stronger at 9.5 months, and only at this age did infants demonstrate a preference towards looking at the congruent actor. Together, these results suggest that although infants are sensitive to others' gaze following from early on, important neural and behavioural developments occur between 6.5 and 9.5 months.

Auditory-Motor Matching in Vocal Recognition and Imitative Learning.

Songbirds possess mirror neurons (MNs) activating during the perception and execution of specific features of songs. These neurons are located in high vocal center (HVC), a premotor nucleus implicated in song perception, production and learning, making worth to inquire their properties and functions in vocal recognition and imitative learning. By integrating a body of brain and behavioral data, we discuss neurophysiology, anatomical, computational properties and possible functions of songbird MNs. We state that the neurophysiological properties of songbird MNs depends on sensorimotor regions that are outside the auditory neural system. Interestingly, songbirds MNs can be the result of the specific type of song representation possessed by some songbird species. At the functional level, we discuss whether songbird MNs are involved in others' song recognition, by dissecting the function of recognition in various different but possible overlapping processes: action-oriented perception, discriminative-oriented perception and identification of the signaler. We conclude that songbird MNs may be involved in recognizing other singer's vocalizations, while their role in imitative learning still require to solve how auditory feedback are used to correct own vocal performance to match the tutor song. Finally, we compare songbird and human mirror responses, hypothesizing a case of convergent evolution, and proposing new experimental directions.

Handling newborn monkeys alters later exploratory, cognitive, and social behaviors.

Touch is one of the first senses to develop and one of the earliest modalities for infant-caregiver communication. While studies have explored the benefits of infant touch in terms of physical health and growth, the effects of social touch on infant behavior are relatively unexplored. Here, we investigated the influence of neonatal handling on a variety of domains, including memory, novelty seeking, and social interest, in infant monkeys (Macaca mulatta; n=48) from 2 to 12 weeks of age. Neonates were randomly assigned to receive extra holding, with or without accompanying face-to-face interactions. Extra-handled infants, compared to standard-reared infants, exhibited less stress-related behavior and more locomotion around a novel environment, faster approach of novel objects, better working memory, and less fear towards a novel social partner. In sum, infants who received more tactile stimulation in the neonatal period subsequently demonstrated more advanced motor, social, and cognitive skills-particularly in contexts involving exploration of novelty-in the first three months of life. These data suggest that social touch may support behavioral development, offering promising possibilities for designing future early interventions, particularly for infants who are at heightened risk for social disorders.

Visual preferences for direct-gaze faces in infant macaques (Macaca mulatta) with limited face exposure.

From birth, human and nonhuman primates attend more to faces with direct gaze compared with averted gaze, and previous studies report that attention to the eyes is linked to the emergence of later social skills. Here, we explored whether early experiences influence attraction to eye contact in infant macaques by examining their attention to face pairs varying in their gaze direction across the first 13 weeks of life. Infants raised by human caretakers had limited conspecific interactions (nursery-reared; N = 16) and were compared to infants raised in rich social environments (mother-reared; N = 20). Both groups looked longer to faces and the eyes of direct compared to averted-gaze faces. Looking to all faces and eyes also increased with age. Nursery-reared infants did not display age-associated increases in attention to direct-gaze faces specifically, suggesting that, while there may be an initial preference for direct-gaze faces from birth, social experiences may support its early development.

The role of the motor system in action understanding and communication: Evidence from human infants and non-human primates.

There is growing evidence that activation of the motor system during observation of actions, a phenomenon first observed in non-human primates, underlies action understanding and even communication. This review (a) examines the evidence on motor system activity as an underlying neural correlate of action understanding; (b) reviews the theoretical and empirical work linking action understanding and the development of communication, with a specific focus on the role that gestures play as an intermediary; and (c) discusses the research on and existing opportunities for understanding the link between the motor system and communication in both humans and non-human primates, through the lens of action perception. Bringing together findings and perspectives from developmental social cognition in both humans and non-human primates and applying recent neuroscientific perspectives will help to elucidate the processes underlying the ability to understand and communicate with others.

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.

Face Detection and the Development of Own-Species Bias in Infant Macaques.

In visually complex environments, numerous items compete for attention. Infants may exhibit attentional efficiency-privileged detection, attention capture, and holding-for face-like stimuli. However, it remains unknown when these biases develop and what role, if any, experience plays in this emerging skill. Here, nursery-reared infant macaques' (Macaca mulatta; n = 10) attention to faces in 10-item arrays of nonfaces was measured using eye tracking. With limited face experience, 3-week-old monkeys were more likely to detect faces and looked longer at faces compared to nonfaces, suggesting a robust face detection system. By 3 months, after peer exposure, infants looked faster to conspecific faces but not heterospecific faces, suggesting an own-species bias in face attention capture, consistent with perceptual attunement.

Mirror neurons in the tree of life: mosaic evolution, plasticity and exaptation of sensorimotor matching responses.

Considering the properties of mirror neurons (MNs) in terms of development and phylogeny, we offer a novel, unifying, and testable account of their evolution according to the available data and try to unify apparently discordant research, including the plasticity of MNs during development, their adaptive value and their phylogenetic relationships and continuity. We hypothesize that the MN system reflects a set of interrelated traits, each with an independent natural history due to unique selective pressures, and propose that there are at least three evolutionarily significant trends that gave raise to three subtypes: hand visuomotor, mouth visuomotor, and audio-vocal. Specifically, we put forward a mosaic evolution hypothesis, which posits that different types of MNs may have evolved at different rates within and among species. This evolutionary hypothesis represents an alternative to both adaptationist and associative models. Finally, the review offers a strong heuristic potential in predicting the circumstances under which specific variations and properties of MNs are expected. Such predictive value is critical to test new hypotheses about MN activity and its plastic changes, depending on the species, the neuroanatomical substrates, and the ecological niche.

Acute oxytocin improves memory and gaze following in male but not female nursery-reared infant macaques.

RATIONALE: Exogenous oxytocin administration is widely reported to improve social cognition in human and nonhuman primate adults. Risk factors of impaired social cognition, however, emerge in infancy. Early interventions-when plasticity is greatest-are critical to reverse negative outcomes. OBJECTIVE: We tested the hypothesis that oxytocin may exert similar positive effects on infant social cognition, as in adults. To test this idea, we assessed the effectiveness of acute, aerosolized oxytocin on two foundational social cognitive skills: working memory (i.e., ability to briefly hold and process information) and social gaze (i.e., tracking the direction of others' gaze) in 1-month-old nursery-reared macaque monkeys (Macaca mulatta). We did not predict sex differences, but we included sex as a factor in our analyses to test whether our effects would be generalizable across both males and females. RESULTS: In a double-blind, placebo-controlled design, we found that females were more socially skilled at baseline compared to males, and that oxytocin improved working memory and gaze following, but only in males. CONCLUSIONS: These sex differences, while unexpected, may be due to interactions with gonadal steroids and may be relevant to sexually dimorphic disorders of social cognition, such as male-biased autism spectrum disorder, for which oxytocin has been proposed as a potential treatment. In sum, we report the first evidence that oxytocin may influence primate infant cognitive abilities. Moreover, these behavioral effects appear sexually dimorphic, highlighting the importance of considering sex differences. Oxytocin effects observed in one sex may not be generalizable to the other sex.

Animal studies help clarify misunderstandings about neonatal imitation.

Empirical studies are incompatible with the proposal that neonatal imitation is arousal driven or declining with age. Nonhuman primate studies reveal a functioning brain mirror system from birth, developmental continuity in imitation and later sociability, and the malleability of neonatal imitation, shaped by the early environment. A narrow focus on arousal effects and reflexes may grossly underestimate neonatal capacities.

The Emotional Modulation of Facial Mimicry: A Kinematic Study.

It is well-established that the observation of emotional facial expression induces facial mimicry responses in the observers. However, how the interaction between emotional and motor components of facial expressions can modulate the motor behavior of the perceiver is still unknown. We have developed a kinematic experiment to evaluate the effect of different oro-facial expressions on perceiver's face movements. Participants were asked to perform two movements, i.e., lip stretching and lip protrusion, in response to the observation of four meaningful (i.e., smile, angry-mouth, kiss, and spit) and two meaningless mouth gestures. All the stimuli were characterized by different motor patterns (mouth aperture or mouth closure). Response Times and kinematics parameters of the movements (amplitude, duration, and mean velocity) were recorded and analyzed. Results evidenced a dissociated effect on reaction times and movement kinematics. We found shorter reaction time when a mouth movement was preceded by the observation of a meaningful and motorically congruent oro-facial gesture, in line with facial mimicry effect. On the contrary, during execution, the perception of smile was associated with the facilitation, in terms of shorter duration and higher velocity of the incongruent movement, i.e., lip protrusion. The same effect resulted in response to kiss and spit that significantly facilitated the execution of lip stretching. We called this phenomenon facial mimicry reversal effect, intended as the overturning of the effect normally observed during facial mimicry. In general, the findings show that both motor features and types of emotional oro-facial gestures (conveying positive or negative valence) affect the kinematics of subsequent mouth movements at different levels: while congruent motor features facilitate a general motor response, motor execution could be speeded by gestures that are motorically incongruent with the observed one. Moreover, valence effect depends on the specific movement required. Results are discussed in relation to the Basic Emotion Theory and embodied cognition framework.

Neonatal imitation predicts infant rhesus macaque (Macaca mulatta) social and anxiety-related behaviours at one year.

The identification of early markers that predict the development of specific social trajectories is critical to understand the developmental and neurobiological underpinnings of healthy social development. We investigated, in infant rhesus macaques (Macaca mulatta), whether newborns' capacity to imitate facial gestures is a valid predictive marker for the emergence of social competencies later in development, at one year of age. Here we first assessed whether infant macaques (N = 126) imitate lipsmacking gestures (a macaque affiliative expression) performed by a human experimenter in their first week of life. We then collected data on infants' social interactions (aggression, grooming, and play) and self-scratching (a proxy indicator of anxiety) at 11-14 months when infants were transferred into a new enclosure with a large social group. Our results show that neonatal imitators exhibit more dominant behaviours, are less anxious, and, for males only, spend more time in play at one year old. These findings suggest that neonatal imitation may be an early predictor of infant sociality and may help identify infants at risk of neurodevelopmental social deficits.

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys.

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competency.

Motor System Activation Predicts Goal Imitation in 7-Month-Old Infants.

The current study harnessed the variability in infants' neural and behavioral responses as a novel method for evaluating the potential relations between motor system activation and social behavior. We used electroencephalography (EEG) to record neural activity as 7-month-old infants observed and responded to the actions of an experimenter. To determine whether motor system activation predicted subsequent imitation behavior, we assessed event-related desynchronization (ERD) at central sites during action observation as a function of subsequent behavior. Greater mu desynchronization over central sites was observed when infants subsequently reproduced the experimenter's goal than when they did not reproduce the goal and instead selected the nongoal object. We also found that mu desynchronization during action execution predicted the infants' later propensity to reproduce the experimenter's goal-directed behavior. These results provide the first evidence that motor system activation predicts the imitation of other individuals' goals during infancy.