Actions chains and intention understanding in 3- to 6-year-old children.

In intentional behavior, the final goal of an action is crucial in determining the entire sequence of motor acts. Neurons have been described in the inferior parietal lobule of monkeys, which besides encoding a specific motor act (e.g., grasping), have their discharge modulated by the final goal of the intended action (e.g., grasping-to-eat). Many of these "action-constrained" neurons have mirror properties responding to the observation of the motor act they encode, provided that this is embedded in a specific action. Thanks to this mechanism, the observers have an internal copy of the whole action before its execution and may, in this way, understand the agent's intention. The chained organization of motor acts has been demonstrated in schoolchildren. Here, we examined whether this organization is already present in very young children. To this purpose, we recorded EMG from the mylohyoid (MH) muscle in the children aged 3 to 6 y. The results showed that preschoolers, like older children, possess the chained organization of motor acts in execution. Interestingly, in comparison to older children, they have a delayed ability to use this mechanism to infer others' intentions by observation. Finally, we found a significant negative association between the children's age and the activation of the MH muscle during the grasp-to-eat phase in the observation condition. We, tentatively, interpreted it as a sign of an immature control of motor acts.

Two distinct networks for encoding goals and forms of action: An effective connectivity study.

Goal-directed actions are characterized by two main features: the content (i.e., the action goal) and the form, called vitality forms (VF) (i.e., how actions are executed). It is well established that both the action content and the capacity to understand the content of another's action are mediated by a network formed by a set of parietal and frontal brain areas. In contrast, the neural bases of action forms (e.g., gentle or rude actions) have not been characterized. However, there are now studies showing that the observation and execution of actions endowed with VF activate, in addition to the parieto-frontal network, the dorso-central insula (DCI). In the present study, we established-using dynamic causal modeling (DCM)-the direction of information flow during observation and execution of actions endowed with gentle and rude VF in the human brain. Based on previous fMRI studies, the selected nodes for the DCM comprised the posterior superior temporal sulcus (pSTS), the inferior parietal lobule (IPL), the premotor cortex (PM), and the DCI. Bayesian model comparison showed that, during action observation, two streams arose from pSTS: one toward IPL, concerning the action goal, and one toward DCI, concerning the action vitality forms. During action execution, two streams arose from PM: one toward IPL, concerning the action goal and one toward DCI concerning action vitality forms. This last finding opens an interesting question concerning the possibility to elicit VF in two distinct ways: cognitively (from PM to DCI) and affectively (from DCI to PM).

Architectural experience influences the processing of others' body expressions.

The interplay between space and cognition is a crucial issue in Neuroscience leading to the development of multiple research fields. However, the relationship between architectural space and the movement of the inhabitants and their interactions has been too often neglected, failing to provide a unifying view of architecture's capacity to modulate social cognition broadly. We bridge this gap by requesting participants to judge avatars' emotional expression (high vs. low arousal) at the end of their promenade inside high- or low-arousing architectures. Stimuli were presented in virtual reality to ensure a dynamic, naturalistic experience. High-density electroencephalography (EEG) was recorded to assess the neural responses to the avatar's presentation. Observing highly aroused avatars increased Late Positive Potentials (LPP), in line with previous evidence. Strikingly, 250 ms before the occurrence of the LPP, P200 amplitude increased due to the experience of low-arousing architectures, reflecting an early greater attention during the processing of body expressions. In addition, participants stared longer at the avatar's head and judged the observed posture as more arousing. Source localization highlighted a contribution of the dorsal premotor cortex to both P200 and LPP. In conclusion, the immersive and dynamic architectural experience modulates human social cognition. In addition, the motor system plays a role in processing architecture and body expressions suggesting that the space and social cognition interplay is rooted in overlapping neural substrates. This study demonstrates that the manipulation of mere architectural space is sufficient to influence human social cognition.

Investigating form and content of emotional and non-emotional laughing.

As cold actions (i.e. actions devoid of an emotional content), also emotions are expressed with different vitality forms. For example, when an individual experiences a positive emotion, such as laughing as expression of happiness, this emotion can be conveyed to others by different intensities of face expressions and body postures. In the present study, we investigated whether the observation of emotions, expressed with different vitality forms, activates the same neural structures as those involved in cold action vitality forms processing. To this purpose, we carried out a functional magnetic resonance imaging study in which participants were tested in 2 conditions: emotional and non-emotional laughing both conveying different vitality forms. There are 3 main results. First, the observation of emotional and non-emotional laughing conveying different vitality forms activates the insula. Second, the observation of emotional laughing activates a series of subcortical structures known to be related to emotions. Furthermore, a region of interest analysis carried out in these structures reveals a significant modulation of the blood-oxygen-leveldependent (BOLD) signal during the processing of different vitality forms exclusively in the right amygdala, right anterior thalamus/hypothalamus, and periaqueductal gray. Third, in a subsequent electromyography study, we found a correlation between the zygomatic muscles activity and BOLD signal in the right amygdala only.

Observation of others' actions during limb immobilization prevents the subsequent decay of motor performance.

There is rich clinical evidence that observing normally executed actions promotes the recovery of the corresponding action execution in patients with motor deficits. In this study, we assessed the ability of action observation to prevent the decay of healthy individuals' motor abilities following upper-limb immobilization. To this end, upper-limb kinematics was recorded in healthy participants while they performed three reach-to-grasp movements before immobilization and the same movements after 16 h of immobilization. The participants were subdivided into two groups; the experimental group observed, during the immobilization, the same reach-to-grasp movements they had performed before immobilization, whereas the control group observed natural scenarios. After bandage removal, motor impairment in performing reach-to-grasp movements was milder in the experimental group. These findings support the hypothesis that action observation, via the mirror mechanism, plays a protective role against the decline of motor performance induced by limb nonuse. From this perspective, action observation therapy is a promising tool for anticipating rehabilitation onset in clinical conditions involving limb nonuse, thus reducing the burden of further rehabilitation.

The value of corticospinal excitability and intracortical inhibition in predicting motor skill improvement driven by action observation.

The observation of other's actions represents an essential element for the acquisition of motor skills. While action observation is known to induce changes in the excitability of the motor cortices, whether such modulations may explain the amount of motor improvement driven by action observation training (AOT) remains to be addressed. Using transcranial magnetic stimulation (TMS), we first assessed in 41 volunteers the effect of action observation on corticospinal excitability, intracortical inhibition, and transcallosal inhibition. Subsequently, half of the participants (AOT-group) were asked to observe and then execute a right-hand dexterity task, while the controls had to observe a no-action video before practicing the same task. AOT participants showed greater performance improvement relative to controls. More importantly, the amount of improvement in the AOT group was predicted by the amplitude of corticospinal modulation during action observation and, even more, by the amount of intracortical inhibition induced by action observation. These relations were specific for the AOT group, while the same patterns were not found in controls. Taken together, our findings demonstrate that the efficacy of AOT in promoting motor learning is rooted in the capacity of action observation to modulate the trainee's motor system excitability, especially its intracortical inhibition. Our study not only enriches the picture of the neurophysiological effects induced by action observation onto the observer's motor excitability, but linking them to the efficacy of AOT, it also paves the way for the development of models predicting the outcome of training procedures based on the observation of other's actions.

Neurotypical individuals fail to understand action vitality form in children with autism spectrum disorder.

Any defects of sociality in individuals diagnosed with autism spectrum disorder (ASD) are standardly explained in terms of those individuals' putative impairments in a variety of cognitive functions. Recently, however, the need for a bidirectional approach to social interaction has been emphasized. Such an approach highlights differences in basic ways of acting between ASD and neurotypical individuals which would prevent them from understanding each other. Here we pursue this approach by focusing on basic action features reflecting the agent's mood and affective states. These are action features Stern named "vitality forms," and which are widely assumed to substantiate core social interactions [D. N. Stern, The Interpersonal World of the Infant (1985); D. N. Stern, Forms of Vitality Exploring Dynamic Experience in Psychology, Arts, Psychotherapy, and Development (2010)]. Previously we demonstrated that, although ASD and typically developing (TD) children alike differentiate vitality forms when performing actions, ASD children express them in a way that is motorically dissimilar to TD children. To assess whether this motor dissimilarity may have consequences for vitality form recognition, we asked neurotypical participants to identify the vitality form of different types of action performed by ASD or TD children. We found that participants exhibited remarkable inaccuracy in identifying ASD children's vitality forms. Interestingly, their performance did not benefit from information feedback. This indicates that how people act matters for understanding others and for being understood by them. Because vitality forms pervade every aspect of daily life, our findings promise to open the way to a deeper comprehension of the bidirectional difficulties for both ASD and neurotypical individuals in interacting with one another.

Tonic somatosensory responses and deficits of tactile awareness converge in the parietal operculum.

Although clinical neuroscience and the neuroscience of consciousness have long sought mechanistic explanations of tactile-awareness disorders, mechanistic insights are rare, mainly because of the difficulty of depicting the fine-grained neural dynamics underlying somatosensory processes. Here, we combined the stereo-EEG responses to somatosensory stimulation with the lesion mapping of patients with a tactile-awareness disorder, namely tactile extinction. Whereas stereo-EEG responses present different temporal patterns, including early/phasic and long-lasting/tonic activities, tactile-extinction lesion mapping co-localizes only with the latter. Overlaps are limited to the posterior part of the perisylvian regions, suggesting that tonic activities may play a role in sustaining tactile awareness. To assess this hypothesis further, we correlated the prevalence of tonic responses with the tactile-extinction lesion mapping, showing that they follow the same topographical gradient. Finally, in parallel with the notion that visuotactile stimulation improves detection in tactile-extinction patients, we demonstrated an enhancement of tonic responses to visuotactile stimuli, with a strong voxel-wise correlation with the lesion mapping. The combination of these results establishes tonic responses in the parietal operculum as the ideal neural correlate of tactile awareness.

Supporting preschoolers' cognitive development: Short- and mid-term effects of fluid reasoning, visuospatial, and motor training.

Cognitive abilities are essential to children's overall growth; thus, the implementation of early and effective training interventions is a major challenge for developmental psychologists and teachers. This study explores whether an intervention simultaneously operating on fluid reasoning (FR), visuospatial, narrative, and motor abilities could boost these competencies in a group of Italian preschoolers (N = 108, 54 males 54 females, Agemean  = 4.04). FR and visuospatial abilities showed training-related increases at the end of the training and 1-year follow-up (moderate effect size). Interestingly, positive correlations with working memory and mathematical abilities were found. Beyond their scientific relevance, the short- and long-term effects provide fundamental indications for designing and implementing educational programs dedicated to preschoolers.

Action Observation and Motor Imagery administered the day before surgery enhance functional recovery in patients after total hip arthroplasty: A randomized controlled trial.

OBJECTIVE: To investigate the effects of Action Observation and Motor Imagery administered the day before surgery on functional recovery in patients after total hip arthroplasty. DESIGN: Randomised controlled trial. SETTING: Humanitas Clinical and Research Center, Milan, Italy. PARTICIPANTS: Eighty inpatients with end-stage hip osteoarthritis undergoing total hip arthroplasty. INTERVENTIONS: All patients followed a standardized postoperative rehabilitation program. Experimental group (AO + MI) performed two 12-minute Action Observation and Motor Imagery sessions on the preoperative day, whereas control group underwent usual care consisting of education without any additional preoperative activity. OUTCOME MEASURES: A blinded physiotherapist assessed participants for functional mobility (Timed Up and Go - TUG) (primary outcome), maximum walking speed (10-Meter Walk Test - 10MWT), pain (Numeric Pain Rating Scale - NPRS) and fear of movement (Tampa Scale of Kinesiophobia - TSK) the day before and at four days after surgery. RESULTS: No between-group differences were found at baseline. Although TUG and 10MWT worsened in both groups (p < 0.001), better TUG was found for AO + MI group at four days (mean difference -5.8 s, 95% confidence interval from -11.3 to -0.3 s, p = 0.039). NPRS (p < 0.001) and TSK (p = 0.036 for AO + MI group, p = 0.003 for control group) improved after surgery without between-group differences. CONCLUSIONS: Patients undergoing Action Observation and Motor Imagery on the day before surgery showed less functional decline than control group in the first days after total hip arthroplasty. This intervention may contribute to a safer discharge with higher functional abilities in patients hospitalized for total hip arthroplasty.

Agent-based representations of objects and actions in the monkey pre-supplementary motor area.

Information about objects around us is essential for planning actions and for predicting those of others. Here, we studied pre-supplementary motor area F6 neurons with a task in which monkeys viewed and grasped (or refrained from grasping) objects, and then observed a human doing the same task. We found "action-related neurons" encoding selectively monkey's own action [self-type (ST)], another agent's action [other-type (OT)], or both [self- and other-type (SOT)]. Interestingly, we found "object-related neurons" exhibiting the same type of selectivity before action onset: Indeed, distinct sets of neurons discharged when visually presented objects were targeted by the monkey's own action (ST), another agent's action (OT), or both (SOT). Notably, object-related neurons appear to signal self and other's intention to grasp and the most likely grip type that will be performed, whereas action-related neurons encode a general goal attainment signal devoid of any specificity for the observed grip type. Time-resolved cross-modal population decoding revealed that F6 neurons first integrate information about object and context to generate an agent-shared signal specifying whether and how the object will be grasped, which progressively turns into a broader agent-based goal attainment signal during action unfolding. Importantly, shared representation of objects critically depends upon their location in the observer's peripersonal space, suggesting an "object-mirroring" mechanism through which observers could accurately predict others' impending action by recruiting the same motor representation they would activate if they were to act upon the same object in the same context.

Cortical mechanisms underlying the organization of goal-directed actions and mirror neuron-based action understanding.

Our understanding of the functions of motor system evolved remarkably in the last 20 years. This is the consequence not only of an increase in the amount of data on this system but especially of a paradigm shift in our conceptualization of it. Motor system is not considered anymore just a "producer" of movements, as it was in the past, but a system crucially involved in cognitive functions. In the present study we review the data on the cortical organization underlying goal-directed actions and action understanding. Our review is subdivided into two major parts. In the first part, we review the anatomical and functional organization of the premotor and parietal areas of monkeys and humans. We show that the parietal and frontal areas form circuits devoted to specific motor functions. We discuss, in particular, the visuo-motor transformation necessary for reaching and for grasping. In the second part we show how a specific neural mechanism, the mirror mechanism, is involved in understanding the action and intention of others. This mechanism is located in the same parieto-frontal circuits that mediate goal-directed actions. We conclude by indicating future directions for studies on the mirror mechanism and suggest some major topics for forthcoming research.

The mirror mechanism: a basic principle of brain function.

The mirror mechanism is a basic brain mechanism that transforms sensory representations of others' behaviour into one's own motor or visceromotor representations concerning that behaviour. According to its location in the brain, it may fulfil a range of cognitive functions, including action and emotion understanding. In each case, it may enable a route to knowledge of others' behaviour, which mainly depends on one's own motor or visceromotor representations.

Motor and emotional behaviours elicited by electrical stimulation of the human cingulate cortex.

The cingulate cortex is a mosaic of different anatomical fields, whose functional characterization is still a matter of debate. In humans, one method that may provide useful insights on the role of the different cingulate regions, and to tackle the issue of the functional differences between its anterior, middle and posterior subsectors, is intracortical electrical stimulation. While previous reports showed that a variety of integrated behaviours could be elicited by stimulating the midcingulate cortex, little is known about the effects of the electrical stimulation of anterior and posterior cingulate regions. Moreover, the internal arrangement of different behaviours within the midcingulate cortex is still unknown. In the present study, we extended previous stimulation studies by retrospectively analysing all the clinical manifestations induced by intracerebral high frequency electrical stimulation (50 Hz, pulse width: 1 ms, 5 s, current intensity: average intensity of 2.7 ± 0.7 mA, biphasic) of the entire cingulate cortex in a cohort of 329 drug-resistant epileptic patients (1789 stimulation sites) undergoing stereo-electroencephalography for a presurgical evaluation. The large number of patients, on one hand, and the accurate multimodal image-based localization of stereo-electroencephalography electrodes, on the other hand, allowed us to assign specific functional properties to modern anatomical subdivisions of the cingulate cortex. Behavioural or subjective responses were elicited from the 32.3% of all cingulate sites, mainly located in the pregenual and midcingulate regions. We found clear functional differences between the pregenual part of the cingulate cortex, hosting the majority of emotional, interoceptive and autonomic responses, and the anterior midcingulate sector, controlling the majority of all complex motor behaviours. Particularly interesting was the 'actotopic' organization of the anterior midcingulate sector, arranged along the ventro-dorsal axis: (i) whole-body behaviours directed to the extra-personal space, such as getting-up impulses, were elicited ventrally, close to the corpus callosum; (ii) hand actions in the peripersonal space were evoked by the stimulation of the intermediate position; and (iii) body-directed actions were induced by the stimulation of the dorsal branch of the cingulate sulcus. The caudal part of the midcingulate cortex and the posterior cingulate cortex were, in contrast, poorly excitable, and mainly devoted to sensory modalities. In particular, the caudal part of the midcingulate cortex hosted the majority of vestibular responses, while posterior cingulate cortex was the principal recipient of visual effects. We will discuss our data in the light of current controversies on the role of the cingulate cortex in cognition and emotion.

Efficacy of a home-based platform for child-to-child interaction on hand motor function in unilateral cerebral palsy.

AIM: To evaluate the feasibility and effectiveness of an action observation treatment (AOT) home-based platform promoting child-to-child interaction to improve hand motor function in unilateral cerebral palsy (CP). METHOD: Twenty children (14 males, six females; mean age 6y 7mo, standard deviation 1y 7mo; range 5y 1mo-10y 6mo) with unilateral CP underwent 20 sessions where they had to observe and then imitate a wizard performing dexterity-demanding magic tricks; a child-to-child live video-session to practise the same exercise then took place. We assessed hand-motor skills with the Besta Scale, neurological motor impairment with Fugl-Meyer Assessment for upper extremity, as well as spasticity, muscle strength, visual analogue scale, and global impression of change 1-month before (T-1), at baseline (T0), and at the end of treatment (T1). RESULTS: We observed a T0 to T1 improvement in global hand-motor and bimanual skills, and a significant correlation between motor improvement and difference in hand motor skills relative to the peer (r=-0.519). INTERPRETATION: AOT associated with child-to-child interaction effectively improves hand motor function in unilateral CP. This improvement is linked to differences in hand motor ability among peers, suggesting that children should observe others with superior motor skills to their own. This study extends traditional AOT toward novel socially-enriched scenarios, where children might simultaneously be recipients and leaders within a motor learning process. WHAT THIS PAPER ADDS: Home-based action observation treatment (AOT) based on child-to-child interaction improves hand motor function in children with unilateral cerebral palsy. Interaction with a more capable peer increases the chances of positive outcome in child-to-child AOT.

Four-dimensional maps of the human somatosensory system.

A fine-grained description of the spatiotemporal dynamics of human brain activity is a major goal of neuroscientific research. Limitations in spatial and temporal resolution of available noninvasive recording and imaging techniques have hindered so far the acquisition of precise, comprehensive four-dimensional maps of human neural activity. The present study combines anatomical and functional data from intracerebral recordings of nearly 100 patients, to generate highly resolved four-dimensional maps of human cortical processing of nonpainful somatosensory stimuli. These maps indicate that the human somatosensory system devoted to the hand encompasses a widespread network covering more than 10% of the cortical surface of both hemispheres. This network includes phasic components, centered on primary somatosensory cortex and neighboring motor, premotor, and inferior parietal regions, and tonic components, centered on opercular and insular areas, and involving human parietal rostroventral area and ventral medial-superior-temporal area. The technique described opens new avenues for investigating the neural basis of all levels of cortical processing in humans.

Expressing our internal states and understanding those of others.

Vitality form is a term that describes the style with which motor actions are performed (e.g., rude, gentle, etc.). They represent one characterizing element of conscious and unconscious bodily communication. Despite their importance in interpersonal behavior, vitality forms have been, until now, virtually neglected in neuroscience. Here, using the functional MRI (fMRI) technique, we investigated the neural correlates of vitality forms in three different tasks: action observation, imagination, and execution. Conjunction analysis showed that, in all three tasks, there is a common, consistent activation of the dorsocentral sector of the insula. In addition, a common activation of the parietofrontal network, typically active during arm movements production, planning, and observation, was also found. We conclude that the dorsocentral part of the insula is a key element of the system that modulates the cortical motor activity, allowing individuals to express their internal states through action vitality forms. Recent monkey anatomical data show that the dorsocentral sector of the insula is, indeed, connected with the cortical circuit involved in the control of arm movements.

The extended object-grasping network.

Grasping is the most important skilled motor act of primates. It is based on a series of sensorimotor transformations through which the affordances of the objects to be grasped are transformed into appropriate hand movements. It is generally accepted that a circuit formed by inferior parietal areas AIP and PFG and ventral premotor area F5 represents the core circuit for sensorimotor transformations for grasping. However, selection and control of appropriate grip should also depend on higher-order information, such as the meaning of the object to be grasped, and the overarching goal of the action in which grasping is embedded. In this review, we describe recent findings showing that specific sectors of the ventrolateral prefrontal cortex are instrumental in controlling higher-order aspects of grasping. We show that these prefrontal sectors control the premotor cortex through two main gateways: the anterior subdivision of ventral area F5-sub-area F5a-, and the pre-supplementary area (area F6). We then review functional studies showing that both F5a and F6, besides being relay stations of prefrontal information, also play specific roles in grasping. Namely, sub-area F5a is involved in stereoscopic analysis of 3D objects, and in planning cue-dependent grasping activity. As for area F6, this area appears to play a crucial role in determining when to execute the motor program encoded in the parieto-premotor circuit. The recent discovery that area F6 contains a set of neurons encoding specific grip types suggests that this area, besides controlling "when to go", also may control the grip type, i.e., "how to go". We conclude by discussing clinical syndromes affecting grasping actions and their possible mechanisms.

Extending the Cortical Grasping Network: Pre-supplementary Motor Neuron Activity During Vision and Grasping of Objects.

Grasping relies on a network of parieto-frontal areas lying on the dorsolateral and dorsomedial parts of the hemispheres. However, the initiation and sequencing of voluntary actions also requires the contribution of mesial premotor regions, particularly the pre-supplementary motor area F6. We recorded 233 F6 neurons from 2 monkeys with chronic linear multishank neural probes during reaching-grasping visuomotor tasks. We showed that F6 neurons play a role in the control of forelimb movements and some of them (26%) exhibit visual and/or motor specificity for the target object. Interestingly, area F6 neurons form 2 functionally distinct populations, showing either visually-triggered or movement-related bursts of activity, in contrast to the sustained visual-to-motor activity displayed by ventral premotor area F5 neurons recorded in the same animals and with the same task during previous studies. These findings suggest that F6 plays a role in object grasping and extend existing models of the cortical grasping network.