What are you doing? How active and observational experience shape infants' action understanding

From early in life, infants watch other people''s actions. How do young infants come to make sense of actions they observe? Here, we review empirical findings on the development of action understanding in infancy. Based on this review, we argue that active action experience is crucial for infants'' developing action understanding. When infants execute actions, they form associations between motor acts and the sensory consequences of these acts. When infants subsequently observe these actions in others, they can use their motor system to predict the outcome of the ongoing actions. Also, infants come to an understanding of others’ actions through the repeated observation of actions and the effects associated with them. In their daily lives, infants have plenty of opportunities to form associations between observed events and learn about statistical regularities of others’ behaviours. We argue that based on these two forms of experience—active action experience and observational experience—infants gradually develop more complex action understanding capabilities.     

Favouritism in the motor system: social interaction modulates action simulation

The ability to anticipate others'' actions is crucial for social interaction. It has been shown that this ability relies on motor areas of the human brain that are not only active during action execution and action observation, but also during anticipation of another person''s action. Recording electroencephalograms during a triadic social interaction, we assessed whether activation of motor areas pertaining to the human mirror-neuron system prior to action observation depends on the social relationship between the actor and the observer. Anticipatory motor activation was stronger when participants expected an interaction partner to perform a particular action than when they anticipated that the same action would be performed by a third person they did not interact with. These results demonstrate that social interaction modulates action simulation.     

An interference effect of observed biological movement on action

It has been proposed that actions are intrinsically linked to perception and that imagining, observing, preparing, or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that certain brain regions involved in executing actions are activated by the mere observation of action (the so-called "mirror system;" ). However, it is unknown whether this mirror system causes interference between observed and simultaneously executed movements. In this study we test the hypothesis that, because of the overlap between action observation and execution, observed actions should interfere with incongruous executed actions. Subjects made arm movements while observing either a robot or another human making the same or qualitatively different arm movements. Variance in the executed movement was measured as an index of interference to the movement. The results demonstrate that observing another human making incongruent movements has a significant interference effect on executed movements. However, we found no evidence that this interference effect occurred when subjects observed a robotic arm making incongruent movements. These results suggest that the simultaneous activation of the overlapping neural networks that process movement observation and execution infers a measurable cost to motor control.     

Making Smart Social Judgments Takes Time: Infants' Recruitment of Goal Information When Generating Action Predictions

Previous research has shown that young infants perceive others'' actions as structured by goals. One open question is whether the recruitment of this understanding when predicting others'' actions imposes a cognitive challenge for young infants. The current study explored infants'' ability to utilize their knowledge of others'' goals to rapidly predict future behavior in complex social environments and distinguish goal-directed actions from other kinds of movements. Fifteen-month-olds (N = 40) viewed videos of an actor engaged in either a goal-directed (grasping) or an ambiguous (brushing the back of her hand) action on a Tobii eye-tracker. At test, critical elements of the scene were changed and infants'' predictive fixations were examined to determine whether they relied on goal information to anticipate the actor''s future behavior. Results revealed that infants reliably generated goal-based visual predictions for the grasping action, but not for the back-of-hand behavior. Moreover, response latencies were longer for goal-based predictions than for location-based predictions, suggesting that goal-based predictions are cognitively taxing. Analyses of areas of interest indicated that heightened attention to the overall scene, as opposed to specific patterns of attention, was the critical indicator of successful judgments regarding an actor''s future goal-directed behavior. These findings shed light on the processes that support “smart” social behavior in infants, as it may be a challenge for young infants to use information about others'' intentions to inform rapid predictions.     

Sex hormone influence on human infants' sound characteristics: melody in spontaneous crying

The specific impact of sex hormones on brain development and acoustic communication is known from animal models. Sex steroid hormones secreted during early development play an essential role in hemispheric organization and the functional lateralization of the brain, e.g. language. In animals, these hormones are well-known regulators of vocal motor behaviour. Here, the association between melody properties of infants'' sounds and serum concentrations of sex steroids was investigated. Spontaneous crying was sampled in 18 healthy infants, averaging two samples taken at four and eight weeks, respectively. Blood samples were taken within a day of the crying samples. The fundamental frequency contour (melody) was analysed quantitatively and the infants'' frequency modulation skills expressed by a melody complexity index (MCI). These skills provide prosodic primitives for later language. A hierarchical, multiple regression approach revealed a significant, robust relationship between the individual MCIs and the unbound, bioactive fraction of oestradiol at four weeks as well as with the four-to-eight-week difference in androstenedione. No robust relationship was found between the MCI and testosterone. Our findings suggest that oestradiol may have effects on the development and function of the auditory–vocal system in human infants that are as powerful as those in vocal-learning animals.     

Action observation treatment: a novel tool in neurorehabilitation

This review focuses on a novel rehabilitation approach known as action observation treatment (AOT). It is now a well-accepted notion in neurophysiology that the observation of actions performed by others activates in the perceiver the same neural structures responsible for the actual execution of those same actions. Areas endowed with this action observation–action execution matching mechanism are defined as the mirror neuron system. AOT exploits this neurophysiological mechanism for the recovery of motor impairment. During one typical session, patients observe a daily action and afterwards execute it in context. So far, this approach has been successfully applied in the rehabilitation of upper limb motor functions in chronic stroke patients, in motor recovery of Parkinson''s disease patients, including those presenting with freezing of gait, and in children with cerebral palsy. Interestingly, this approach also improved lower limb motor functions in post-surgical orthopaedic patients. AOT is well grounded in basic neuroscience, thus representing a valid model of translational medicine in the field of neurorehabilitation. Moreover, the results concerning its effectiveness have been collected in randomized controlled studies, thus being an example of evidence-based clinical practice.     

Infants’ Somatotopic Neural Responses to Seeing Human Actions: I’ve Got You under My Skin

Human infants rapidly learn new skills and customs via imitation, but the neural linkages between action perception and production are not well understood. Neuroscience studies in adults suggest that a key component of imitation–identifying the corresponding body part used in the acts of self and other–has an organized neural signature. In adults, perceiving someone using a specific body part (e.g., hand vs. foot) is associated with activation of the corresponding area of the sensory and/or motor strip in the observer’s brain–a phenomenon called neural somatotopy. Here we examine whether preverbal infants also exhibit somatotopic neural responses during the observation of others’ actions. 14-month-old infants were randomly assigned to watch an adult reach towards and touch an object using either her hand or her foot. The scalp electroencephalogram (EEG) was recorded and event-related changes in the sensorimotor mu rhythm were analyzed. Mu rhythm desynchronization was greater over hand areas of sensorimotor cortex during observation of hand actions and was greater over the foot area for observation of foot actions. This provides the first evidence that infants’ observation of someone else using a particular body part activates the corresponding areas of sensorimotor cortex. We hypothesize that this somatotopic organization in the developing brain supports imitation and cultural learning. The findings connect developmental cognitive neuroscience, adult neuroscience, action representation, and behavioral imitation.     

FMRI supports the sensorimotor theory of motor resonance

The neural mechanisms mediating the activation of the motor system during action observation, also known as motor resonance, are of major interest to the field of motor control. It has been proposed that motor resonance develops in infants through Hebbian plasticity of pathways connecting sensory and motor regions that fire simultaneously during imitation or self movement observation. A fundamental problem when testing this theory in adults is that most experimental paradigms involve actions that have been overpracticed throughout life. Here, we directly tested the sensorimotor theory of motor resonance by creating new visuomotor representations using abstract stimuli (motor symbols) and identifying the neural networks recruited through fMRI. We predicted that the network recruited during action observation and execution would overlap with that recruited during observation of new motor symbols. Our results indicate that a network consisting of premotor and posterior parietal cortex, the supplementary motor area, the inferior frontal gyrus and cerebellum was activated both by new motor symbols and by direct observation of the corresponding action. This tight spatial overlap underscores the importance of sensorimotor learning for motor resonance and further indicates that the physical characteristics of the perceived stimulus are irrelevant to the evoked response in the observer.     

Disrupting the experience of control in the human brain: pre-supplementary motor area contributes to the sense of agency

The feeling of controlling events through one''s actions is fundamental to human experience, but its neural basis remains unclear. This ‘sense of agency’ (SoA) can be measured quantitatively as a temporal linkage between voluntary actions and their external effects. We investigated the brain areas underlying this aspect of action awareness by using theta-burst stimulation to locally and reversibly disrupt human brain function. Disruption of the pre-supplementary motor area (pre-SMA), a key structure for preparation and initiation of a voluntary action, was shown to reduce the temporal linkage between a voluntary key-press action and a subsequent electrocutaneous stimulus. In contrast, disruption of the sensorimotor cortex, which processes signals more directly related to action execution and sensory feedback, had no significant effect. Our results provide the first direct evidence of a pre-SMA contribution to SoA.     

Neural mirroring mechanisms and imitation in human infants

Studying human infants will increase our understanding of the nature, origins and function of neural mirroring mechanisms. Human infants are prolific imitators. Infant imitation indicates observation–execution linkages in the brain prior to language and protracted learning. Investigations of neural aspects of these linkages in human infants have focused on the sensorimotor mu rhythm in the electroencephalogram, which occurs in the alpha frequency range over central electrode sites. Recent results show that the infant mu rhythm is desynchronized during action execution as well as action observation. Current work is elucidating properties of the infant mu rhythm and how it may relate to prelinguistic action processing and social understanding. Here, we consider this neuroscience research in relation to developmental psychological theory, particularly the ‘Like-Me’ framework, which holds that one of the chief cognitive tasks of the human infant is to map the similarity between self and other. We elucidate the value of integrating neuroscience findings with behavioural studies of infant imitation, and the reciprocal benefit of examining mirroring mechanisms from an ontogenetic perspective.     

Somatic and motor components of action simulation

Seminal studies in monkeys report that the viewing of actions performed by other individuals activates frontal and parietal cortical areas typically involved in action planning and execution. That mirroring actions might rely on both motor and somatosensory components is suggested by reports that action observation and execution increase neural activity in motor and in somatosensory areas. This occurs not only during observation of naturalistic movements but also during the viewing of biomechanically impossible movements that tap the afferent component of action, possibly by eliciting strong somatic feelings in the onlooker. Although somatosensory feedback is inherently linked to action execution, information on the possible causative role of frontal and parietal cortices in simulating motor and sensory action components is lacking. By combining low-frequency repetitive and single-pulse transcranial magnetic stimulation, we found that virtual lesions of ventral premotor cortex (vPMc) and primary somatosensory cortex (S1) suppressed mirror motor facilitation contingent upon observation of possible and impossible movements, respectively. In contrast, virtual lesions of primary motor cortex did not influence mirror motor facilitation. The reported double dissociation suggests that vPMc and S1 play an active, differential role in simulating efferent and afferent components of observed actions.     

Automatic Imitation in Rhythmical Actions: Kinematic Fidelity and the Effects of Compatibility,Delay, and Visual Monitoring

We demonstrate that observation of everyday rhythmical actions biases subsequent motor execution of the same and of different actions, using a paradigm where the observed actions were irrelevant for action execution. The cycle time of the distractor actions was subtly manipulated across trials, and the cycle time of motor responses served as the main dependent measure. Although distractor frequencies reliably biased response cycle times, this imitation bias was only a small fraction of the modulations in distractor speed, as well as of the modulations produced when participants intentionally imitated the observed rhythms. Importantly, this bias was not only present for compatible actions, but was also found, though numerically reduced, when distractor and executed actions were different (e.g., tooth brushing vs. window wiping), or when the dominant plane of movement was different (horizontal vs. vertical). In addition, these effects were equally pronounced for execution at 0, 4, and 8 s after action observation, a finding that contrasts with the more short-lived effects reported in earlier studies. The imitation bias was also unaffected when vision of the hand was occluded during execution, indicating that this effect most likely resulted from visuomotor interactions during distractor observation, rather than from visual monitoring and guidance during execution. Finally, when the distractor was incompatible in both dimensions (action type and plane) the imitation bias was not reduced further, in an additive way, relative to the single-incompatible conditions. This points to a mechanism whereby the observed action’s impact on motor processing is generally reduced whenever this is not useful for motor planning. We interpret these findings in the framework of biased competition, where intended and distractor actions can be represented as competing and quasi-encapsulated sensorimotor streams.     

Positive Facial Affect – An fMRI Study on the Involvement of Insula and Amygdala

Imitation of facial expressions engages the putative human mirror neuron system as well as the insula and the amygdala as part of the limbic system. The specific function of the latter two regions during emotional actions is still under debate. The current study investigated brain responses during imitation of positive in comparison to non-emotional facial expressions. Differences in brain activation of the amygdala and insula were additionally examined during observation and execution of facial expressions. Participants imitated, executed and observed happy and non-emotional facial expressions, as well as neutral faces. During imitation, higher right hemispheric activation emerged in the happy compared to the non-emotional condition in the right anterior insula and the right amygdala, in addition to the pre-supplementary motor area, middle temporal gyrus and the inferior frontal gyrus. Region-of-interest analyses revealed that the right insula was more strongly recruited by (i) imitation and execution than by observation of facial expressions, that (ii) the insula was significantly stronger activated by happy than by non-emotional facial expressions during observation and imitation and that (iii) the activation differences in the right amygdala between happy and non-emotional facial expressions were increased during imitation and execution, in comparison to sole observation. We suggest that the insula and the amygdala contribute specifically to the happy emotional connotation of the facial expressions depending on the task. The pattern of the insula activity might reflect increased bodily awareness during active execution compared to passive observation and during visual processing of the happy compared to non-emotional facial expressions. The activation specific for the happy facial expression of the amygdala during motor tasks, but not in the observation condition, might reflect increased autonomic activity or feedback from facial muscles to the amygdala.     

How frontoparietal brain regions mediate imitative and complementary actions: an FMRI study

The 'mirror neuron system' (MNS), located within inferior parietal lobe (IPL) and inferior frontal gyrus (IFG), creates an internal motor representation of the actions we see and has been implicated in imitation. Recently, the MNS has been implicated in non-identical responses: when the actions we must execute do not match those that we observe. However, in such conflicting situations non action-specific cognitive control networks also located in frontoparietal regions may be involved. In the present functional magnetic resonance imaging (fMRI) study participants made both similar and dissimilar actions within two action contexts: imitative and complementary. We aimed to determine whether activity within IPL/IFG depends on (i) responding under an imitative versus complementary context (ii) responding with similar versus dissimilar responses, and (iii) observing hand actions versus symbolic arrow cue stimuli. Activity within rIPL/rIFG regions was largest during observation of hand actions compared with arrow cues. Specifically, rIPL/rIFG were recruited only during the imitative context, when participants responded with similar actions. When responding to symbolic arrow cues, rIPL/rIFG activity increased during dissimilar responses, reflecting increased demands placed on general cognitive control mechanisms. These results suggest a specific role of rIPL/rIFG during imitation of hand actions, and also a general role of frontoparietal areas in mediating dissimilar responses to both hand actions and symbolic stimuli. We discuss our findings in relation to recent work that has examined the role of frontoparietal brain structures in joint-actions and inter-actor cooperation. We conclude that the specific brain regions identified here to show increased activation during action observation conditions are likely to form part of a mechanism specifically involved in matching observed actions directly with internal motor plans. Conversely, observation of arrow cues recruited part of a wider cognitive control network involved in the rapid remapping of stimulus-response associations.     

Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation

Mirror neurons are single cells found in macaque premotor and parietal cortices that are active during action execution and observation. In non-human primates, mirror neurons have only been found in relation to object-directed movements or communicative gestures, as non-object directed actions of the upper limb are not well characterized in non-human primates. Mirror neurons provide important evidence for motor simulation theories of cognition, sometimes referred to as the direct matching hypothesis, which propose that observed actions are mapped onto associated motor schemata in a direct and automatic manner. This study, for the first time, directly compares mirror responses, defined as the overlap between action execution and observation, during object directed and meaningless non-object directed actions. We present functional MRI data that demonstrate a clear dissociation between object directed and non-object directed actions within the human mirror system. A premotor and parietal network was preferentially active during object directed actions, whether observed or executed. Moreover, we report spatially correlated activity across multiple voxels for observation and execution of an object directed action. In contrast to predictions made by motor simulation theory, no similar activity was observed for non-object directed actions. These data demonstrate that object directed and meaningless non-object directed actions are subserved by different neuronal networks and that the human mirror response is significantly greater for object directed actions. These data have important implications for understanding the human mirror system and for simulation theories of motor cognition. Subsequent theories of motor simulation must account for these differences, possibly by acknowledging the role of experience in modulating the mirror response.     

Human primary motor cortex is both activated and stabilized during observation of other person's phasic motor actions

When your favourite athlete flops over the high-jump bar, you may twist your body in front of the TV screen. Such automatic motor facilitation, ‘mirroring’ or even overt imitation is not always appropriate. Here, we show, by monitoring motor-cortex brain rhythms with magnetoencephalography (MEG) in healthy adults, that viewing intermittent hand actions of another person, in addition to activation, phasically stabilizes the viewer''s primary motor cortex, with the maximum of half a second after the onset of the seen movement. Such a stabilization was evident as enhanced cortex–muscle coherence at 16–20 Hz, despite signs of almost simultaneous suppression of rolandic rhythms of approximately 7 and 15 Hz as a sign of activation of the sensorimotor cortex. These findings suggest that inhibition suppresses motor output during viewing another person''s actions, thereby withholding unintentional imitation.     

Neural mechanisms of infant learning: differences in frontal theta activity during object exploration modulate subsequent object recognition

Investigating learning mechanisms in infancy relies largely on behavioural measures like visual attention, which often fail to predict whether stimuli would be encoded successfully. This study explored EEG activity in the theta frequency band, previously shown to predict successful learning in adults, to directly study infants'' cognitive engagement, beyond visual attention. We tested 11-month-old infants (N = 23) and demonstrated that differences in frontal theta-band oscillations, recorded during infants'' object exploration, predicted differential subsequent recognition of these objects in a preferential-looking test. Given that theta activity is modulated by motivation to learn in adults, these findings set the ground for future investigation into the drivers of infant learning.     

Neuronal chains for actions in the parietal lobe: a computational model

The inferior part of the parietal lobe (IPL) is known to play a very important role in sensorimotor integration. Neurons in this region code goal-related motor acts performed with the mouth, with the hand and with the arm. It has been demonstrated that most IPL motor neurons coding a specific motor act (e.g., grasping) show markedly different activation patterns according to the final goal of the action sequence in which the act is embedded (grasping for eating or grasping for placing). Some of these neurons (parietal mirror neurons) show a similar selectivity also during the observation of the same action sequences when executed by others. Thus, it appears that the neuronal response occurring during the execution and the observation of a specific grasping act codes not only the executed motor act, but also the agent's final goal (intention).In this work we present a biologically inspired neural network architecture that models mechanisms of motor sequences execution and recognition. In this network, pools composed of motor and mirror neurons that encode motor acts of a sequence are arranged in form of action goal-specific neuronal chains. The execution and the recognition of actions is achieved through the propagation of activity bursts along specific chains modulated by visual and somatosensory inputs.The implemented spiking neuron network is able to reproduce the results found in neurophysiological recordings of parietal neurons during task performance and provides a biologically plausible implementation of the action selection and recognition process.Finally, the present paper proposes a mechanism for the formation of new neural chains by linking together in a sequential manner neurons that represent subsequent motor acts, thus producing goal-directed sequences.     

Corticospinal mirror neurons

Here, we report the properties of neurons with mirror-like characteristics that were identified as pyramidal tract neurons (PTNs) and recorded in the ventral premotor cortex (area F5) and primary motor cortex (M1) of three macaque monkeys. We analysed the neurons’ discharge while the monkeys performed active grasp of either food or an object, and also while they observed an experimenter carrying out a similar range of grasps. A considerable proportion of tested PTNs showed clear mirror-like properties (52% F5 and 58% M1). Some PTNs exhibited ‘classical’ mirror neuron properties, increasing activity for both execution and observation, while others decreased their discharge during observation (‘suppression mirror-neurons’). These experiments not only demonstrate the existence of PTNs as mirror neurons in M1, but also reveal some interesting differences between M1 and F5 mirror PTNs. Although observation-related changes in the discharge of PTNs must reach the spinal cord and will include some direct projections to motoneurons supplying grasping muscles, there was no EMG activity in these muscles during action observation. We suggest that the mirror neuron system is involved in the withholding of unwanted movement during action observation. Mirror neurons are differentially recruited in the behaviour that switches rapidly between making your own movements and observing those of others.     

Motor Contagion during Human-Human and Human-Robot Interaction

Motor resonance mechanisms are known to affect humans'' ability to interact with others, yielding the kind of “mutual understanding” that is the basis of social interaction. However, it remains unclear how the partner''s action features combine or compete to promote or prevent motor resonance during interaction. To clarify this point, the present study tested whether and how the nature of the visual stimulus and the properties of the observed actions influence observer''s motor response, being motor contagion one of the behavioral manifestations of motor resonance. Participants observed a humanoid robot and a human agent move their hands into a pre-specified final position or put an object into a container at various velocities. Their movements, both in the object- and non-object- directed conditions, were characterized by either a smooth/curvilinear or a jerky/segmented trajectory. These trajectories were covered with biological or non-biological kinematics (the latter only by the humanoid robot). After action observation, participants were requested to either reach the indicated final position or to transport a similar object into another container. Results showed that motor contagion appeared for both the interactive partner except when the humanoid robot violated the biological laws of motion. These findings suggest that the observer may transiently match his/her own motor repertoire to that of the observed agent. This matching might mediate the activation of motor resonance, and modulate the spontaneity and the pleasantness of the interaction, whatever the nature of the communication partner.