Relations between infants’ emerging reach‐grasp competence and event‐related desynchronization in EEG

Recent reports of similar patterns of brain electrical activity (electroencephalogram: EEG) during action execution and observation, recorded from scalp locations over motor‐related regions in infants and adults, have raised the possibility that two foundational abilities – controlling one's own intentional actions and perceiving others’ actions – may be integrally related during ontogeny. However, to our knowledge, there are no published reports of the relations between developments in motor skill (i.e. recording actual motor skill performance) and EEG during both action execution and action observation. In the present study we collected EEG from 21 9‐month‐olds who were given opportunities to reach for toys and who also observed an experimenter reach for toys. Event‐related desynchronization (ERD) was computed from the EEG during the reaching events. We assessed infants’ reaching‐grasping competence, including reach latency, errors, preshaping of the hand, and bimanual reaches, and found that desynchronization recorded in scalp electrodes over motor‐related regions during action observation was associated with action competence during execution. Infants who were more competent reachers, compared to less competent reachers, exhibited greater ERD while observing reaching‐grasping. These results provide initial evidence for an early emerging neural system integrating one's own actions with the perception of others’ actions.     

Development of infant sustained attention and its relation to EEG oscillations: an EEG and cortical source analysis study

The current study examined the relation between infant sustained attention and infant EEG oscillations. Fifty‐nine infants were tested at 6 (N = 15), 8 (N = 17), 10 (N = 14), and 12 (N = 13) months. Three attention phases, stimulus orienting, sustained attention, and attention termination, were defined based on infants' heart rate changes. Frequency analysis using simultaneously recorded EEG focused on infant theta (2–6 Hz), alpha (6–9 Hz), and beta (9–14 Hz) rhythms. Cortical source analysis of EEG oscillations was conducted with realistic infant MRI models. Theta synchronization was found over fontal pole, temporal, and parietal electrodes during infant sustained attention for 10 and 12 months. Alpha desynchronization was found over frontal, central and parietal electrodes during sustained attention. This alpha effect started to emerge at 10 months and became well established by 12 months. No difference was found for the beta rhythm between different attention phases. The theta synchronization effect was localized to the orbital frontal, temporal pole, and ventral temporal areas. The alpha desynchronization effect was localized to the brain regions composing the default mode network including the posterior cingulate cortex and precuneus, medial prefrontal cortex, and inferior parietal gyrus. The alpha desynchronization effect was also localized to the pre‐ and post‐central gyri. The present study demonstrates a connection between infant sustained attention and EEG oscillatory activities.     

Using mu rhythm desynchronization to measure mirror neuron activity in infants

The Mirror Neuron System hypothesis stating that observed actions are projected onto the observer’s own action system assigns an important role to development, because only actions mastered by the observer can be mirrored. The purpose of the present study was to investigate whether there is evidence of a functioning mirror neuron system (MNS) in 8-month-old infants. High-density EEG was used to assess the mu rhythm desynchronization in an action observation task where the infants observed a live model. To reduce noise, ICA decompositions were used. The results show a higher desynchronization of the mu rhythm when infants observed a goal-directed action than when they observed a spatially similar non-goal-directed movement. The localizations of the sources are in agreement with those proposed by the MNS hypothesis. This indicates that the MNS is functioning at this age.     

Infants’ grip strength predicts mu rhythm attenuation during observation of lifting actions with weighted blocks

Research has established that the body is fundamentally involved in perception: bodily experience influences activation of the shared neural system underlying action perception and production during action observation, and bodily characteristics influence perception of the spatial environment. However, whether bodily characteristics influence action perception and its underlying neural system is unknown, particularly in early ontogeny. We measured grip strength in 12‐month‐old infants and investigated relations with mu rhythm attenuation, an electroencephalographic correlate of the neural system underlying action perception, during observation of lifting actions performed with differently weighted blocks. We found that infants with higher grip strength exhibited significant mu attenuation during observation of lifting actions, whereas infants with lower grip strength did not. Moreover, a progressively strong relation between grip strength and mu attenuation during observation of lifts was found with increased block weight. We propose that this relation is attributable to differences in infants’ ability to recognize the effort associated with lifting objects of different weights, as a consequence of their developing strength. Together, our results extend the body's role in perception by demonstrating that bodily characteristics influence action perception by shaping the activation of its underlying neural system.     

EEG mu rhythm and imitation impairments in individuals with autism spectrum disorder

Imitation ability has consistently been shown to be impaired in individuals with autism. A dysfunctional execution/observation matching system has been proposed to account for this impairment. The EEG mu rhythm is believed to reflect an underlying execution/observation matching system. This study investigated evidence of differential mu rhythm attenuation during the observation, execution, and imitation of movements and examined its relation to behaviorally assessed imitation abilities. Fourteen high-functioning adults with autism spectrum disorder (ASD) and 15 IQ- and age-matched typical adults participated. On the behavioral imitation task, adults with ASD demonstrated significantly poorer performance compared to typical adults in all domains of imitation ability. On the EEG task, both groups demonstrated significant attenuation of the mu rhythm when executing an action. However, when observing movement, the individuals with ASD showed significantly reduced attenuation of the mu wave. Behaviorally assessed imitation skills were correlated with degree of mu wave attenuation during observation of movement. These findings suggest that there is execution/observation matching system dysfunction in individuals with autism and that this matching system is related to degree of impairment in imitation abilities.     

Development of frontal electroencephalogram (EEG) and heart rate (ECG) responses to affective musical stimuli during the first 12 months of post-natal life

We examined the development of infants' regional electrocortical (EEG) and heart rate (ECG) responses to affective musical stimuli during the first 12 months of post-natal life. Separate groups of infants were seen at 3 (n=33), 6 (n=42), 9 (n=52), and 12 (n=40) months of age at which time regional EEG and ECG responses were continuously recorded during a baseline condition and during the presentation of three orchestral pieces that were known to vary in affective valence and intensity (happy, sad, fear). Overall, there were two important findings. First, we found that although the overall amount of EEG 4-8 Hz power increased between 3 and 12 months, the distribution of EEG power changed across age, with the younger infants (3- and 6-month-olds) showing no difference between frontal and parietal regions, but the older infants (9- and 12-month-olds) showing relatively more activation at frontal than at parietal sites. This development likely reflects the maturation of frontal lobe function. Second, we found that the presentation of affective music significantly increased brain activity at 3 months of age, had seemingly little effect at 6 and 9 months, and significantly attenuated brain activity at 12 months. Findings suggest that there is a clear developmental change in the effect of music on brain activity in the first year, with music having a "calming" influence on infants by the end of the first year of life.     

人类镜像系统参与音乐情绪的自动加工：来自EEG的证据

大脑中线电极诱发的μ抑制波(包括α和β频段)是人类镜像系统活动的电生理指标。尽管音乐情绪表现被认为是通过模仿个体的心理状态来实现的, 但是尚未有研究探讨人类镜像系统与音乐情绪加工的关系。本研究通过EEG技术, 采用跨通道情绪启动范式, 探究人类镜像系统是否参与和弦情绪的自动加工。愉悦或不愉悦的和弦启动情绪一致与不一致的目标面孔。行为结果显示, 被试对情绪一致面孔的反应显著快于情绪不一致面孔的反应。EEG结果显示, 在听觉刺激出现后的500~650 ms之间, 与情绪一致条件相比, 情绪不一致条件诱发了β频段的去同步化。在听觉刺激出现后的300~450 ms, 无论是情绪一致, 还是不一致条件, 都诱发了α频段的去同步化。源分析结果显示, μ抑制波主要出现在人类镜像系统的相关脑区。这些结果表明, 音乐情绪的自动加工与人类镜像系统的活动密切相关。     

Infants' mu suppression during the observation of real and mimicked goal‐directed actions

Since their discovery in the early 1990s, mirror neurons have been proposed to be related to many social‐communicative abilities, such as imitation. However, research into the early manifestations of the putative neural mirroring system and its role in early social development is still inconclusive. In the current EEG study, mu suppression, generally thought to reflect activity in neural mirroring systems was investigated in 18‐ to 30‐month‐olds during the observation of object manipulations as well as mimicked actions. EEG power data recorded from frontal, central, and parietal electrodes were analysed. As predicted, based on previous research, mu wave suppression was found over central electrodes during action observation and execution. In addition, a similar suppression was found during the observation of intransitive, mimicked hand movements. To a lesser extent, the results also showed mu suppression at parietal electrode sites, over all three conditions. Mu wave suppression during the observation of hand movements and during the execution of actions was significantly correlated with quality of imitation, but not with age or language level.     

The 'like me' framework for recognizing and becoming an intentional agent

Infant imitation demonstrates that the perception and production of human action are closely linked by a 'supramodal' representation of action. This action representation unites observation and execution into a common framework, and it has far-reaching implications for the development of social cognition. It allows infants to see the behaviors of others as commensurate with their own-as 'like me.' Based on the 'like me' perception of others, social encounters are interpretable and informative. Infants can use themselves as a framework for understanding others and can learn about the possibilities and consequences of their own potential acts by observing the behavior of others. Through social interaction with other intentional agents who are viewed as 'like me,' infants develop a richer social cognition. This paper explores the early manifestations and cascading developmental effects of the 'like me' conception.     

Longitudinal study of perception of structured optic flow and random visual motion in infants using high‐density EEG

Electroencephalogram (EEG) was used in infants at 3–4 months and 11–12 months to longitudinally study brain electrical activity as the infants were exposed to structured forwards and reversed optic flow, and non‐structured random visual motion. Analyses of visual evoked potential (VEP) and temporal spectral evolution (TSE, time‐dependent amplitude changes) were performed on EEG data recorded with a 128‐channel sensor array. VEP results showed infants to significantly differentiate between the radial motion conditions, but only at 11–12 months where they showed shortest latency for forwards optic flow and longest latency for random visual motion. When the TSE results of the motion conditions were compared with those of a static non‐flow dot pattern, infants at 3–4 and 11–12 months both showed significant differences in induced activity. A decrease in amplitudes at 5–7 Hz was observed as desynchronized theta‐band activity at both 3–4 and 11–12 months, while an increase in amplitudes at 9–13 Hz was observed as synchronized alpha‐band activity only at 11–12 months. It was concluded that brain electrical activities related to visual motion perception change during the first year of life, and these changes can be observed both in the VEP and induced activities of EEG. With adequate neurobiological development and locomotor experience infants around 1 year of age rely, more so than when they were younger, on structured optic flow and show a more adult‐like specialization for motion where faster oscillating cell assemblies have fewer but more specialized neurons, resulting in improved visual motion perception.     

Infants show enhanced neural responses to musical meter frequencies beyond low-level features

Music listening often entails spontaneous perception and body movement to a periodic pulse-like meter. There is increasing evidence that this cross-cultural ability relates to neural processes that selectively enhance metric periodicities, even when these periodicities are not prominent in the acoustic stimulus. However, whether these neural processes emerge early in development remains largely unknown. Here, we recorded the electroencephalogram (EEG) of 20 healthy 5- to 6-month-old infants, while they were exposed to two rhythms known to induce the perception of meter consistently across Western adults. One rhythm contained prominent acoustic periodicities corresponding to the meter, whereas the other rhythm did not. Infants showed significantly enhanced representations of meter periodicities in their EEG responses to both rhythms. This effect is unlikely to reflect the tracking of salient acoustic features in the stimulus, as it was observed irrespective of the prominence of meter periodicities in the audio signals. Moreover, as previously observed in adults, the neural enhancement of meter was greater when the rhythm was delivered by low-pitched sounds. Together, these findings indicate that the endogenous enhancement of metric periodicities beyond low-level acoustic features is a neural property that is already present soon after birth. These high-level neural processes could set the stage for internal representations of musical meter that are critical for human movement coordination during rhythmic musical behavior.

Research Highlights

• 5- to 6-month-old infants were presented with auditory rhythms that induce the perception of a periodic pulse-like meter in adults.
• Infants showed selective enhancement of EEG activity at meter-related frequencies irrespective of the prominence of these frequencies in the stimulus.
• Responses at meter-related frequencies were boosted when the rhythm was conveyed by bass sounds.
• High-level neural processes that transform rhythmic auditory stimuli into internal meter templates emerge early after birth.

     

Action experience in infancy predicts visual-motor functional connectivity during action anticipation

Despite substantial evidence indicating a close link between action production and perception in early child development, less is known about how action experience shapes the processes of perceiving and anticipating others’ actions. Here, we developed a novel approach to capture functional connectivity specific to certain brain areas to investigate how action experience changes the networks involved in action perception and anticipation. Nine- and-12-month-old infants observed familiar (grasping) and novel (tool-use) actions while their brain activity was measured using EEG. Infants’ motor competence of both actions was assessed. A link between action experience and connectivity patterns was found, particularly during the anticipation period. During action anticipation, greater motor competence in grasping predicted greater functional connectivity between visual (occipital alpha) and motor (central alpha) regions relative to global levels of whole-brain EEG connectivity. Furthermore, visual and motor regions tended to be more coordinated in response to familiar versus novel actions and for older than younger participants. Critically, these effects were not found in the control networks (frontal-central; frontal-occipital; parietal-central; parietal-occipital), suggesting a unique role of visual-motor networks on the link between motor skills and action encoding.

Highlights

• Infants’ motor development predicted functional connectivity patterns during action anticipation.
• Faster graspers, and older infants, showed a stronger ratio of visual-motor neural coherence.
• Overall whole-brain connectivity was modulated by age and familiarity with the actions.
• Measuring inter-site relative to whole-brain connectivity can capture specific brain-behavior links.
• Measures of phase-based connectivity over time are sensitive to anticipatory action.

     

Delta and spindle components in the integrated EEG during nocturnal sleep for infants with developmental disabilities

The delta and spindle components in the integrated EEG for 121 infants with developmental disabilities (from 4 mo. to 6 yr. of age: M=1.79, SD=0.14; 57 girls and 64 boys) were studied throughout nocturnal sleep. In 80 (66.1%, Group A) of 121 subjects, periodic changes of delta and spindle rhythm powers were noted in measurements of EEG made during sleep. In 28 (23.1%, Group B), delta but not spindle rhythm powers were found, and in the remaining 13 subjects (10.7%, Group C) neither delta nor spindle rhythm powers were found throughout measurements of EEG made during sleep. The Tsumori-Inage Questionnaire for Infants was administered to the parents to estimate subjects' behavioral developmental level as Developmental Quotients. Significantly lower mean Developmental Quotients were found for Groups B and C than Group A. These findings suggested that the presence or absence of delta and spindle rhythm powers in EEG measurements made during nocturnal sleep could be taken as an index of the severity of developmental disorders in infants with developmental disabilities.     

Mechanisms behind hazard perception of warning signs: An EEG study

Warning signs are the most effective way to alert people to hazards in the industries, architecture, and transportation. To better understand how these warning signs prompted hazard, this study investigated the intrinsic mechanism of hazard perception of warning signs, including warning words (low versus high hazard levels) and surrounding shapes (upright triangle versus circle). We recruited 18 participants and recorded electroencephalogram (EEG). We found that a combination of high-hazard-level words and an upright triangle shape significantly elicited more negative N300 and increased theta-band (3–8 Hz) synchronization, but reduced beta-band (15–30 Hz) desynchronization. The N300 component represented the emotional arousal strength, theta oscillations reflected the engagement of retrieval of emotional experiences from episodic memory, and beta oscillation connoted the semantic encoding. Thus, these findings suggested that a high-hazard-level combination had the ability to obtain high priority in cognitive processing. The EEG pattern changes allowed us to assess whether the hazard perception of warning signs was high or low, which could be an accurate indicator to better evaluate the design of warning signs.     

Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory

Metabotropic glutamate receptors (mGluRs) are known to play a role in synaptic plasticity and learning. We have previously shown that mGluR7 deletion in mice produces a selective working memory (WM) impairment, while other types of memory such as reference memory remain unaffected. Since WM has been associated with Theta activity (6-12 Hz) in EEGs, and since EEG abnormalities have been observed in these mice before, we studied the effect of mGluR7 gene ablation on EEG activity in the hippocampus, in particular in the Theta range, during performance of a WM task. In an eight-arm maze with four arms baited, mGluR7 knock-out (KO) and wild-type mice committed the same number of reference memory errors, whereas KOs committed more WM errors. While performing the task, KO mice showed substantially higher Theta amplitudes, and the ratio of Theta to overall EEG power was much increased. No change was seen in the Delta (0-5 Hz), or Gamma (30-40 Hz) EEG bands compared with controls. When recording EEGs during periods of rest in the home cages, no difference was seen between groups. These findings suggest that mGluR7 is important for modulation and control of Theta activity. Since only WM was affected, and only the Theta range of EEG activity was altered, these results show a correlation between Theta rhythm and WM performance, and therefore support the concept that Theta activity in the hippocampus is involved in WM storage.     

Perception and production of object-related grasping in 6-month-olds

In this study, 6-month-olds’ perception of an object-related human grasping action was compared with their level of grasping performance using a within-participants design. In the action perception task, infants were presented with the video of an actor’s grasping movement toward an occluded target object. Subsequently, an expected and an unexpected final state of this grasping movement were presented simultaneously, and infants’ looking times were measured. In the action production task, infants were presented with three graspable objects. Infants’ grasping behavior was coded to be either palmar or thumb-opposite grasping. Results indicate that infants who were already able to perform a thumb-opposite grasp differentiated between the two final states in the action perception task by looking longer toward the unexpected final state. In contrast, infants who showed only palmar grasps looked equally long toward both final states. This finding supports the assumption that action perception and action control are already closely related in infants as young as 6 months.     

Event-related Desynchronization of Mu Rhythms During Concentric and Eccentric Contractions

The purpose of this study was to compare the electroencephalographic (EEG) patterns and reaction times (RTs) of muscle activation between concentric and eccentric biceps brachii contractions under the RT paradigm and to evaluate how the EEG patterns and RTs changed with practice. Sixteen subjects performed 3 sets of 30 repetitions of submaximal voluntary concentric and eccentric biceps contractions. RT, event-related desynchronization (ERD) patterns of mu rhythm onset, and ERD amplitudes were selectively analyzed. Mental demand decreased as familiarity with the motor action increased due to practice regardless of contraction type. However, the 2 types of muscle contractions still have differences in brain activity regardless of decreased mental demand: eccentric contractions require earlier preparation than concentric contractions.     

Electroencephalogram and heart rate measures of working memory at 5 and 10 months of age

We recorded electroencephalogram (EEG; 6-9 Hz) and heart rate (HR) from infants at 5 and 10 months of age during baseline and performance on the looking A-not-B task of infant working memory (WM). Longitudinal baseline-to-task comparisons revealed WM-related increases in EEG power (all electrodes) and EEG coherence (medial frontal-occipital electrode pairs) at both ages. WM-related decreases in HR were only present at 5 months, and WM-related increases in EEG coherence became more localized by 10 months. Regression analyses revealed that baseline-to-task changes in psychophysiology accounted for variability in WM performance at 10 but not 5 months. HR and EEG power (medial frontal and lateral frontal electrodes) were unique predictors of variability in 10-month WM performance. These findings are discussed in relation to frontal lobe development and represent the first comprehensive longitudinal analysis of age-related changes in the behavioral and psychophysiological correlates of WM.     

The early development of human mirror mechanisms: evidence from electromyographic recordings at 3 and 6 months

In primates and adult humans direct understanding of others' action is provided by mirror mechanisms matching action observation and action execution (e.g. Casile, Caggiano & Ferrari, 2011). Despite the growing body of evidence detailing the existence of these mechanisms in the adult human brain, their origins and early development are largely unknown. In this study, for the first time, electromyographic (EMG) measures were used to shed light on the emergence of mirror motor mechanisms in infancy. EMG activity was recorded while 6‐ and 3‐month‐old infants watched two videos displaying an agent reaching for, grasping and bringing an object either to the mouth or to the head. Results indicate that the motor system of 6‐month‐olds, but not 3‐month‐olds, was recruited and selectively modulated during observation of the goal‐directed actions, favoring the idea that mirror mechanisms driving action understanding gradually emerge during early development.     

Action mechanisms for social cognition: behavioral and neural correlates of developing Theory of Mind

Many psychological theories posit foundational links between two fundamental constructs: (1) our ability to produce, perceive, and represent action; and (2) our ability to understand the meaning and motivation behind the action (i.e. Theory of Mind; ToM). This position is contentious, however, and long‐standing competing theories of social‐cognitive development debate roles for basic action‐processing in ToM. Developmental research is key to investigating these hypotheses, but whether individual differences in neural and behavioral measures of motor action relate to social‐cognitive development is unknown. We examined 3‐ to 5‐year‐old children's (N = 26) EEG mu‐desynchronization during production of object‐directed action, and explored associations between mu‐desynchronization and children's behavioral motor skills, behavioral action‐representation abilities, and behavioral ToM. For children with high (but not low) mu‐desynchronization, motor skill related to action‐representation abilities, and action‐representation mediated relations between motor skill and ToM. Results demonstrate novel foundational links between action‐processing and ToM, suggesting that basic motor action may be a key mechanism for social‐cognitive development, thus shedding light on the origins and emergence of higher social cognition.