Modulation of the mirror neuron system during action observation: neuroimaging evidence for experience-dependent motor resonance in healthy humans and children with Unilateral celebran Palsy

Abstract

It is now a well-accepted notion in neurophysiology that the observation of actions performed by others activates in the perceiver a set of neural structures responsible for the actual execution of those same actions. Indeed, action observation is believed to activate the mirror neuron system (MNS), formed by visuomotor neurons which fire both when individuals perform a goal-directed action or when they observe a similar act, performed by another individual. The function of this network is to transform the sensory representations of observed motor acts into the corresponding motor representations. Overall, action observation is considered an effective tool to enhance motor learning in healthy people and patients with stroke or Parkinson disease. The action observation therapy has been also used in children with Unilateral Cerebral Palsy (UCP). An important assumption for an observation-based therapy/training is the plasticity of the MNS. Several studies indicate a strong role of the MNS in representing previously acquired motor skills, showing that, during action observation, observers tend to “resonate” more strongly with observed actions already embodied in their own motor repertoire. Here, we hypothesized that the MNS could be better activated: 1) in healthy humans by the observation of a model with a motor repertoire similar to that of the observer; 2) in UCP children by a paretic hand model as compared to a healthy one. The first fMRI study concerns the role of motor experience in the modulation of MNS in healthy humans observing complex manipulative actions performed with different levels of expertise. The hypothesis was that the MNS is more active when the observed hand actions correspond to the own motor expertise. Eighteen healthy volunteers, without particular hand motor skills, observed video-clips displaying hand-object manipulation performed with the right hand, in a first person perspective. The manipulation was performed by an expert with a high level of manual/fingers dexterity, by an actor with an intermediate ability or by a naïve subject. The most important result was that the observation of actions performed by a naïve model produced a stronger activation in a dorsal parieto-premotor network of areas, mostly lateralized to the left hemisphere. Secondly, the results showed that the superior parietal lobule was functionally coupled with bilateral parietal and frontal areas including the dorsal premotor cortex. This could suggest that this dorsal circuit, possibly involved in the processing of kinematic proprieties of the observed action, tends to resonate strongly with actions already embodied in the personal motor repertoire. In the second fMRI study, a group of UCP children, homogeneous for type of hand impairment and lesion side, observed grasping actions performed by a healthy or a paretic hand and their brain activations were compared with that of a group of typically developing (TD) children matched by age. The results showed that the MNS areas were activated not only in TD, but also in UCP children, in spite of the presence of extended lesions. According with the hypothesis, the main result was that in UCP children the MNS was more activated during observation of actions performed by the paretic hand model with respect to the healthy one, suggesting that this neural system was modulated by the degree of similarity between observer’s motor repertoire and observed model. A possible explanation is that in UCP children the MNS is sensitive not only to the goal of the action but also to observed action kinematics. In situations in which the observed action does not belong to the personal motor repertoire, deviation in kinematics could be fundamental to explain a decreased motor resonance with the observed model. In a translational medicine perspective, these results could allow the therapy to achieve a greater motor improvement and to better adapt it to individual upper limb clinical characteristics.