An embodied approach to fetal and newborn perceptual and sensorimotor development.

The embodied approach argues that interaction with the environment plays a crucial role in brain development and that the presence of sensory effects generated by movements is fundamental. The movement of the fetus is initially random. Then, the repeated execution of the movement creates a link between it and its sensory effects, allowing the selection of movements that produce expected sensations. During fetal life, the brain develops from a transitory fetal circuit to the permanent cortical circuit, which completes development after birth. Accordingly, this process must concern the interaction of the fetus with the intrauterine environment and of the newborn with the new aerial environment, which provides a new sensory stimulation, light. The goal of the present review is to provide suggestions for neuroscientific research capable of shedding light on brain development process by describing from a functional point of view the relationship between the motor and sensory abilities of fetuses and newborns and the increasing complexity of their interaction with objects in the womb and outside of it.

Effects of a Robot-Assisted Arm Training Plus Hand Functional Electrical Stimulation on Recovery After Stroke: A Randomized Clinical Trial.

OBJECTIVE: To compare the effects of unilateral, proximal arm robot-assisted therapy combined with hand functional electrical stimulation with intensive conventional therapy for restoring arm function in survivors of subacute stroke. DESIGN: This was a single-blinded, randomized controlled trial. SETTING: Inpatient rehabilitation university hospital. PARTICIPANTS: Patients (N=40) diagnosed as having ischemic stroke (time since stroke <8wk) and upper limb impairment were enrolled. INTERVENTIONS: Participants randomized to the experimental group received 30 sessions (5 sessions/wk) of robot-assisted arm therapy and hand functional electrical stimulation (RAT+FES). Participants randomized to the control group received a time-matched intensive conventional therapy. MAIN OUTCOME MEASURES: The primary outcome was arm motor recovery measured with the Fugl-Meyer Motor Assessment. Secondary outcomes included motor function, arm spasticity, and activities of daily living. Measurements were performed at baseline, after 3 weeks, at the end of treatment, and at 6-month follow-up. Presence of motor evoked potentials (MEPs) was also measured at baseline. RESULTS: Both groups significantly improved all outcome measures except for spasticity without differences between groups. Patients with moderate impairment and presence of MEPs who underwent early rehabilitation (<30d post stroke) demonstrated the greatest clinical improvements. CONCLUSIONS: RAT+FES was no more effective than intensive conventional arm training. However, at the same level of arm impairment and corticospinal tract integrity, it induced a higher level of arm recovery.

Bilateral M1 anodal transcranial direct current stimulation in post traumatic chronic minimally conscious state: a pilot EEG-tDCS study.

OBJECTIVE: We tested the preliminary effects of bilateral anodal transcranial direct current stimulation (tDCS) in patients with disorders of consciousness. DESIGN: Open label pilot study. SUBJECTS: Ten chronic (greater than 12 months) patients in a minimally conscious state (MCS) following severe traumatic brain injury. METHODS: The patients received 10 sessions of bilateral M1 anodal tDCS. Behavioural changes were assessed with the Coma Recovery Scale-Revised (CRS-R) before stimulation (T-1, T0), after five sessions (T1), at the end of the stimulation (T2), after two weeks (T3) and after three months (T4). Moreover, an EEG assessment was conducted. RESULTS: Eight out of 10 patients showed new clinical signs of consciousness; specifically, a 2-point CRS-R improvement was detected in the last follow-up (p = 0.004). EEG upper α bandwidth was greater in the parietal site at T1 (p < 0.034). In addition, we found a significant correlation between behavioral and EEG indices at T1 (r =  0.89; p =  0.001). CONCLUSION: This preliminary study presents several limitations (small sample size and no control group). However, it provides important initial data that can be used to design randomized clinical trials testing this novel approach in MCS and to further explore EEG as a neural marker for the effects of tDCS.

Facial expressions as a model to test the role of the sensorimotor system in the visual perception of the actions.

A long-term debate concerns whether the sensorimotor coding carried out during transitive actions observation reflects the low-level movement implementation details or the movement goals. On the contrary, phonemes and emotional facial expressions are intransitive actions that do not fall into this debate. The investigation of phonemes discrimination has proven to be a good model to demonstrate that the sensorimotor system plays a role in understanding actions acoustically presented. In the present study, we adapted the experimental paradigms already used in phonemes discrimination during face posture manipulation, to the discrimination of emotional facial expressions. We submitted participants to a lower or to an upper face posture manipulation during the execution of a four alternative labelling task of pictures randomly taken from four morphed continua between two emotional facial expressions. The results showed that the implementation of low-level movement details influence the discrimination of ambiguous facial expressions differing for a specific involvement of those movement details. These findings indicate that facial expressions discrimination is a good model to test the role of the sensorimotor system in the perception of actions visually presented.

Digital Intentions in the Fingers: I Know What You Are Doing with Your Smartphone.

Every day, we make thousands of finger movements on the touchscreen of our smartphones. The same movements might be directed at various distal goals. We can type "What is the weather in Rome?" in Google to acquire information from a weather site, or we may type it on WhatsApp to decide whether to visit Rome with a friend. In this study, we show that by watching an agent's typing hands, an observer can infer whether the agent is typing on the smartphone to obtain information or to share it with others. The probability of answering correctly varies with age and typing style. According to embodied cognition, we propose that the recognition process relies on detecting subtle differences in the agent's movement, a skill that grows with sensorimotor competence. We expect that this preliminary work will serve as a starting point for further research on sensorimotor representations of digital actions.

Evidence of motor resonance in stroke patients with severe upper limb function impairments.

For the past fifteen years, observation of actions has proved to be effective in the motor rehabilitation of stroke. Despite this, no evidence has ever been provided that this practice is able to activate the efferent motor system of a limb unable to perform the observed action due to stroke. In fact, transcranial magnetic stimulation cannot easily be used in these patients, and the fMRI evidence is inconclusive. This creates a logical problem, as the effectiveness of action observation in functional recovery is attributed to its ability to evoke action simulation, up to sub-threshold muscle activation (i.e., motor resonance), in healthy individuals. To provide the necessary proof-of-concept, patients with severe upper limb function impairments and matched control participants were submitted to a verified action prediction paradigm. They were asked to watch videos showing gripping movements towards a graspable or an ungraspable object, and to press a button the instant the agent touched the object. The presence of more accurate responses for the graspable object trials is considered an indirect evidence of motor resonance. Participants were required to perform the task in two sessions which differed in the hand used to respond. Despite the serious difficulty of movement, 8 out of 18 patients were able to perform the task with their impaired hand. We found that the responses given by the paretic hand showed a modulation of the action prediction time no different from that showed by the non-paretic hand, which, in turn, did not differ from that showed by the matched control participants. The present proof-of-concept study shows that action observation involves the efferent motor system even when the hand used to respond is unable to perform the observed action due to a cortical lesion, providing the missing evidence to support the already established use of Action Observation Training (AOT) in motor rehabilitation of stroke.

Effects of movement congruence on motor resonance in early Parkinson's disease.

The observation of action seems to involve the generation of the internal representation of that same action in the observer, a process named motor resonance (MR). The objective of this study was to verify whether an experimental paradigm of action observation in a laboratory context could elicit cortical motor activation in 21 early Parkinson's disease (PD) patients compared to 22 controls. Participants were instructed to simply observe (observation-only session) or to respond (Time-to-contact detection session) at the instant the agent performed a grasping action toward a graspable or ungraspable object. We used functional near-infrared spectroscopy with 20 channels on the motor and premotor brain areas and event-related desynchronization of alpha-mu rhythm. In both groups, response times were more accurate in graspable than ungraspable object trials, suggesting that motor resonance is present in PD patients. In the Time-to-contact detection session, the oxyhemoglobin levels and alpha-mu desynchronization prevailed in the graspable object trials rather than in the ungraspable ones. This study demonstrates the preservation of MR mechanisms in early PD patients. The action observation finalized to a consequent movement can activate cortical networks in patients with early PD, suggesting early rehabilitation interventions taking into account specific observation paradigms preceding motor production.

The Role of the Sensorimotor System in Cognitive Functions.

The discovery of neurons with sensory properties in frontal motor circuits, and the discovery that these circuits send modulatory signals to the sensory parietal areas, strongly challenged the classical idea of a motor system as a mere executor of commands, and suggested that the sensorimotor system may contribute to the cognitive processes necessary for interaction with the world [...].

Movement observation activates motor cortex in fibromyalgia patients: a fNIRS study.

Scientific evidence points to a shared neural representation between performing and observing an action. The action observation notoriously determines a modulation of the observer's sensorimotor system, a phenomenon called Motor Resonance (MR). Fibromyalgia (FM) patients suffer from a condition characterized by generalized musculoskeletal pain in which even simple movement can exacerbate their symptoms. Maladaptive functioning of the primary motor cortex is a common finding in patients with chronic pain. Activation of the motor cortex is known to induce an analgesic effect in patients with chronic pain. In this exploratory study, we intend to verify if the mere observation of a movement could elicit activation of the motor cortical areas in patients with FM. Therefore, the purpose of this study was to examine the presence of MR in patients affected by fibromyalgia. We adopted a behavioral paradigm known for detecting the presence of MR and a neurophysiological experiment. Participants watched videos showing gripping movements towards a graspable or an ungraspable object, respectively, and were asked to press a button the instant the agent touched the object (Time-to-contact detection session). In a different experimental session, participants were only requested to observe and pay attention to the videos (Observation-only session). During each experimental session, the participants' cerebral hemodynamic activity was recorded using the functional Near-Infrared Spectroscopy method. The behavioral task analysis revealed the presence of MR in both FM patients and healthy controls. Moreover, neurophysiological findings suggested that the observation of movement during the Observation-only session provoked activation and modulation of the cortical motor networks of FM patients. These results could represent evidence of the possible beneficial effects of movement observation in restarting motor activation, notoriously reduced, in FM patients.

Grasping the semantic of actions: a combined behavioral and MEG study.

There is experimental evidence that the brain systems involved in action execution also play a role in action observation and understanding. Recently, it has been suggested that the sensorimotor system is also involved in language processing. Supporting results are slower response times and weaker motor-related MEG Beta band power suppression in semantic decision tasks on single action verbs labels when the stimulus and the motor response involve the same effector. Attenuated power suppression indicates decreased cortical excitability and consequent decreased readiness to act. The embodied approach forwards that the simultaneous involvement of the sensorimotor system in the processing of the linguistic content and in the planning of the response determines this language-motor interference effect. Here, in a combined behavioral and MEG study we investigated to what extent the processing of actions visually presented (i.e., pictures of actions) and verbally described (i.e., verbs in written words) share common neural mechanisms. The findings demonstrated that, whether an action is experienced visually or verbally, its processing engages the sensorimotor system in a comparable way. These results provide further support to the embodied view of semantic processing, suggesting that this process is independent from the modality of presentation of the stimulus, including language.

Effect of weight-related labels on corticospinal excitability during observation of grasping: a TMS study.

Recent studies of corticospinal excitability during observation of grasping and lifting of objects of different weight have highlighted the role of agent's kinematics in modulating observer's motor excitability. Here, we investigate whether explicit weight-related information, provided by written labels on the objects, modulate the excitability of the observer's motor system and how this modulation is affected when there is a conflict between label and object's weight. We measured TMS-evoked motor potentials (MEPs) from right hand intrinsic muscles, while subjects were observing an actor lifting objects of different weights, in some trials labeled (heavy/light) in congruent or incongruent way. Results confirmed a weight-related modulation of MEPs based on kinematic cues. Interestingly, any conflict between the labels and the actual weight (i.e., explicit versus implicit information), although never consciously noticed by the observer, deeply affected the mirroring of others' actions. Our findings stress the automatic involvement of the mirror-neuron system.

Proactive gaze is present during biological and non-biological motion observation.

Others' action observation activates in the observer a coordinated hand-eye motor program, covert for the hand (i.e. motor resonance), and overt for the eye (i.e. proactive gaze), similar to that of the observed agent. The biological motion hypothesis of action anticipation claims that proactive gaze occurs only in the presence of biological motion, and that kinematic information is sufficient to determine the anticipation process. The results of the present study did not support the biological motion hypothesis of action anticipation. Specifically, proactive gaze was present during observation of both a biological accelerated-decelerated motion and a non-biological constant velocity motion (Experiment 1), in the presence of a barrier able to restrict differences between the two kinematics to the motion profile of individual markers prior to contact (Experiment 2), but only if an object was present at the end point of the movement trajectory (Experiment 3). Furthermore, proactive gaze was found independently of the presence of end effects temporally congruent with the instant in which the movement stopped (Experiments 4, and 5). We propose that the involvement of the observer's motor system is not restricted to when the agent moves with natural kinematics, and it is mandatory whenever the presence of an agent or a goal is evident, regardless of physical appearance, natural kinematics, and the possibility to identify the action behind the stimulus.

Implicit Associations between Adverbs of Place and Actions in the Physical and Digital Space.

Neuropsychological, behavioral, and neurophysiological evidence indicates that the coding of space as near and far depends on the involvement of different neuronal circuits. These circuits are recruited on the basis of functional parameters, not of metrical ones, reflecting a general distinction of human behavior, which alternatively attributes to the individual the role of agent or observer. Although much research in cognitive psychology was devoted to demonstrating that language and concepts are rooted in the sensorimotor system, no study has investigated the presence of implicit associations between different adverbs of place (far vs. near) and actions with different functional characteristics. Using a series of Implicit Association Test (IAT) experiments, we tested this possibility for both actions performed in physical space (grasp vs. look at) and those performed when using digital technology (content generation vs. content consumption). For both the physical and digital environments, the results showed an association between the adverb near and actions related to the role of agent, and between the adverb far and actions related to the role of observer. Present findings are the first experimental evidence of an implicit association between different adverbs of place and different actions and of the fact that adverbs of place also apply to the digital environment.

Efficacy of Facial Exercises in Facial Expression Categorization in Schizophrenia.

Embodied cognition theories suggest that observation of facial expression induces the same pattern of muscle activation, and that this contributes to emotion recognition. Consequently, the inability to form facial expressions would affect emotional understanding. Patients with schizophrenia show a reduced ability to express and perceive facial emotions. We assumed that a physical training specifically developed to mobilize facial muscles could improve the ability to perform facial movements, and, consequently, spontaneous mimicry and facial expression recognition. Twenty-four inpatient participants with schizophrenia were randomly assigned to the experimental and control group. At the beginning and at the end of the study, both groups were submitted to a facial expression categorization test and their data compared. The experimental group underwent a training period during which the lip muscles, and the muscles around the eyes were mobilized through the execution of transitive actions. Participants were trained three times a week for five weeks. Results showed a positive impact of the physical training in the recognition of others' facial emotions, specifically for the responses of "fear", the emotion for which the recognition deficit in the test is most severe. This evidence suggests that a specific deficit of the sensorimotor system may result in a specific cognitive deficit.

Force requirements of observed object lifting are encoded by the observer's motor system: a TMS study.

Several transcranial magnetic stimulation (TMS) studies have reported facilitation of the primary motor cortex (M1) during the mere observation of actions. This facilitation was shown to be highly congruent, in terms of somatotopy, with the observed action, even at the level of single muscles. With the present study, we investigated whether this muscle-specific facilitation of the observer's motor system reflects the degree of muscular force that is exerted in an observed action. Two separate TMS experiments are reported in which corticospinal excitability was measured in the hand area of M1 while subjects observed the lifting of objects of different weights. The type of action 'grasping-and-lifting-the-object' was always identical, but the grip force varied according to the object's weight. In accordance to previous findings, excitability of M1 was shown to modulate in a muscle-specific way, such that only the cortical representation areas in M1 that control the specific muscles used in the observed lifting action became increasingly facilitated. Moreover, muscle-specific M1 facilitation was shown to modulate to the force requirements of the observed actions, such that M1 excitability was considerably higher when observing heavy object lifting compared with light object lifting. Overall, these results indicate that different levels of observed grip force are mirrored onto the observer's motor system in a highly muscle-specific manner. The measured force-dependent modulations of corticospinal excitability in M1 are hypothesized to be functionally relevant for scaling the observed grip force in the observer's own motor system. In turn, this mechanism may contribute, at least partly, to the observer's ability to infer the weight of the lifted object.

Encoding of human action in Broca's area.

Broca's area has been considered, for over a century, as the brain centre responsible for speech production. Modern neuroimaging and neuropsychological evidence have suggested a wider functional role is played by this area. In addition to the evidence that it is involved in syntactical analysis, mathematical calculation and music processing, it has recently been shown that Broca's area may play some role in language comprehension and, more generally, in understanding actions of other individuals. As shown by functional magnetic resonance imaging, Broca's area is one of the cortical areas activated by hand/mouth action observation and it has been proposed that it may form a crucial node of a human mirror-neuron system. If, on the one hand, neuroimaging studies use a correlational approach which cannot offer a final proof for such claims, available neuropsychological data fail to offer a conclusive demonstration for two main reasons: (i) they use tasks taxing both language and action systems; and (ii) they rarely consider the possibility that Broca's aphasics may also be affected by some form of apraxia. We administered a novel action comprehension test--with almost no linguistic requirements--on selected frontal aphasic patients lacking apraxic symptoms. Patients, as well as matched controls, were shown short movies of human actions or of physical events. Their task consisted of ordering, in a temporal sequence, four pictures taken from each movie and randomly presented on the computer screen. Patient's performance showed a specific dissociation in their ability to re-order pictures of human actions (impaired) with respect to physical events (spared). Our study provides a demonstration that frontal aphasics, not affected by apraxia, are specifically impaired in their capability to correctly encode observed human actions.

Two-day-old newborns learn to discriminate accelerated-decelerated biological kinematics from constant velocity motion.

Already in uterus the hand moves with the typical accelerated-decelerated kinematics of goal-directed actions and, from the twenty-second week of pregnancy, the unborn shows the ability to modulate the velocity of the movement depending on the nature of the target. According to the direct matching hypothesis, this motor knowledge may be sufficient to attune neonates' motion perception-like adults'-to biological kinematics. Using dots configuration motions which varied with respect to the kinematics of goal-directed actions, we observed that two-day-old human newborns did not show any spontaneous preference for either biological accelerated-decelerated motion or non-biological constant velocity motion when these were simultaneously presented in a standard preferential looking paradigm. In contrast, newborns preferred the biological kinematics after the repeated visual presentation of the different motions in a standard infant-control visual habituation paradigm. We propose that present results indicate that the relationship between perception and action does not require only action development but also the accumulation of sufficient perceptual experience. They also suggest a fast plasticity of the sensorimotor system in linking an already acquired motor knowledge with a newly experienced congruent visual stimulation.

Observation of the point-light animation of a grasping hand activates sensorimotor cortex in nine-month-old infants.

Measuring changes in sensorimotor alpha band activity in nine-month-old infants we sought to understand the involvement of the sensorimotor cortex during observation of the Point-Light (PL) animation of a grasping hand. Attenuation of alpha activity was found both when the PL display moved towards the to-be-grasped object and when the object was deleted from the video. Before the beginning of the movement of the PL stimuli, only in the presence of the object evoked attenuation of sensorimotor alpha activity was documented, possibly interpreted either as movement prediction or as graspable object perception. Our main findings demonstrate that, during observation of stimuli moving with biological kinematics, the infants' sensorimotor system is activated when the pictorial information is absent or highly reduced, and independently of the presence of the goal-directed object. The possible compensatory function of the sensorimotor system during observation of highly degraded moving stimuli is discussed.

Phonological and lexical motor facilitation during speech listening: a transcranial magnetic stimulation study.

In the present study, we used transcranial magnetic stimulation (TMS) to investigate the influence of phonological and lexical properties of verbal items on the excitability of the tongue's cortical motor representation during passive listening. In particular, we aimed to clarify if the difference in tongue motor excitability found during listening to words and pseudo-words [Fadiga, L., Craighero, L., Buccino, G., Rizzolatti, G., 2002. Speech listening specifically modulates the excitability of tongue muscles: a TMS study. European Journal of Neuroscience 15, 399-402] is due to lexical frequency or to the presence of a meaning per se. In order to do this, we investigated the time-course of tongue motor-evoked potentials (MEPs) during listening to frequent words, rare words, and pseudo-words embedded with a double consonant requiring relevant tongue movements for its pronunciation. Results showed that at the later stimulation intervals (200 and 300 ms from the double consonant) listening to rare words evoked much larger MEPs than listening to frequent words. Moreover, by comparing pseudo-words embedded with a double consonant requiring or not tongue movements, we found that a pure phonological motor resonance was present only 100 ms after the double consonant. Thus, while the phonological motor resonance appears very early, the lexical-dependent motor facilitation takes more time to appear and depends on the frequency of the stimuli. The present results indicate that the motor system responsible for phonoarticulatory movements during speech production is also involved during speech listening in a strictly specific way. This motor facilitation reflects both the difference in the phonoarticulatory characteristics and the difference in the frequency of occurrence of the verbal material.