Actual and Imagined Movements Reveal a Dual Role of the Insular Cortex for Motor Control.

Movements rely on a mixture of feedforward and feedback mechanisms. With experience, the brain builds internal representations of actions in different contexts. Many factors are taken into account in this process among which is the immutable presence of gravity. Any displacement of a massive body in the gravitational field generates forces and torques that must be predicted and compensated by appropriate motor commands. The insular cortex is a key brain area for graviception. However, no attempt has been made to address whether the same internal representation of gravity is shared between feedforward and feedback mechanisms. Here, participants either mentally simulated (only feedforward) or performed (feedforward and feedback) vertical movements of the hand. We found that the posterior part of the insular cortex was engaged when feedback was processed. The anterior insula, however, was activated only in mental simulation of the action. A psychophysical experiment demonstrates participants' ability to integrate the effects of gravity. Our results point toward a dual internal representation of gravity within the insula. We discuss the conceptual link between these two dualities.

Cerebellar damage affects the inference of human motion.

The present study aims at the cerebellum's role in prediction mechanisms triggered by action observation. Five cerebellar patients and six age-paired control subjects were asked to estimate the occluded end point position of the shoulder's trajectories in Sit-to-Stand (STS) or Back-to-Sit (BTS) conditions, following or not biological rules. Contrarily to the control group, the prediction accuracy of the end point position in cerebellar patients did not depend on biological rules. Interestingly, both groups presented similar results when estimating the vanishing position of the target. Taken together, these results suggest that cerebellar damage affectsthe capacity of predicting upcoming actions by observation.

Mirror neurons and their relationship with neurodegenerative disorders.

The finding of mirror neurons (MNs) has provided a biological substrate to a new concept of cognition, relating data on actions and perceptions not only to integrate perception in action planning and execution but also as a neural mechanism supporting a wide range of cognitive functions. Here we first summarize data on MN localization and role in primates, then we report findings in normal human subjects: functional magnetic resonance imaging and neurophysiological studies sustain that MNs have a role in motor learning and recognizing actions and intentions of others, and they also support an embodied view of language, empathy, and memory. Then, we detail the results of literature searching on MNs and embodied cognition in Parkinson's disease (PD), frontotemporal dementia (FTD)/amyotrophic lateral sclerosis (ALS), and in mild cognitive impairment (MCI)/Alzheimer's disease (AD). In PD the network of MN could be altered, but its hyperactivation might support motor and cognitive performances at least in early stages. In the ALS/FTD continuum, preliminary evidence points out to an involvement of the MN network, which could explain language and inter-subjectivity deficits shown in patients affected by these clinical entities. In the MCI/AD spectrum, a few recent studies suggest a possible progressive involvement from posterior to anterior areas of the MN network, with the brain putting in place compensatory mechanisms in early stages. Reinterpreting neurodegenerative diseases at the light of the new views about brain organization stemming from the discovery of MN could help to better comprehend clinical manifestations and open new pathways to rehabilitation.

Ipsilesional functional recruitment within lower mu band in children with unilateral cerebral palsy, an event-related desynchronization study.

Cerebral palsy (CP) is a group of non-progressive developmental movement disorders inducing a strong brain reorganization in primary and secondary motor areas. Nevertheless, few studies have been dedicated to quantify brain pattern changes and correlate them with motor characteristics in CP children. In this context, it is very important to identify feasible and complementary tools able to enrich the description of motor impairments by considering their neural correlates. To this aim, we recorded the electroencephalographic activity and the corresponding event-related desynchronization (ERD) of a group of mild-to-moderate affected unilateral CP children while performing unilateral reach-to-grasp movements with both their paretic and non-paretic arms. During paretic arm movement execution, we found a reduced ERD in the upper µ band (10-12.5 Hz) over central electrodes, preceded by an increased fronto-central ERD in the lower µ band (7.5-10 Hz) during movement preparation. These changes positively correlated, respectively, with the Modified House Classification scale and the Manual Ability Classification System. The fronto-central activation likely represents an ipsilesional plastic compensatory reorganization, confirming that in not-severely affected CP, the lesioned hemisphere is able to compensate part of the damage effects. These results highlight the importance of analyzing different sub-bands within the classical mu band and suggest that in similar CP population, the lesioned hemisphere should be the target of specific intensive rehabilitation programs.

Temporal binding effect in the action observation domain: Evidence from an action-based somatosensory paradigm.

Temporal binding is understood as an effect in which a temporal interval between a voluntary action and its consequent effect is perceived as compressed. It denotes an implicit measure of a sense of agency. When people observe someone else performing an action that generates an effect, temporal binding also takes place. We aimed to test whether the interaction between observed actions and tactile sensation influences temporal binding. Participants observed finger tapping movements (of a human or wooden hand), in parallel to receiving tactile stimulations on their fingertip. These stimulations were either congruent or incongruent with the tactile consequences of the observed movement. The finger tapping movement was followed by a tone. Participants estimated the intervals between the observed action and the tone. We found that temporal binding for observed actions depends on the congruency between the perceived touch and tactile consequences of observed actions restricted to intentional actors.

The action congruency effect on the feelings of agency.

Previous studies suggest that the sense of agency (SoA), the feeling of control about one's own actions and ensuing effects is also generated during action selection processes. We investigate whether the conflict at the action selection stage induced by a supraliminal stimulus, modulates an implicit measure of SoA, namely intentional binding. Furthermore, we were interested to investigate the influence of different types of stimulus-response compatibility on SoA. To this aim we compared the influence of an automatic imitation task and a stroop-like task on intentional binding. In both tasks participants performed congruent and incongruent fingers movements (key release) in response to an external stimulus. Their movements caused an effect and participants estimated the time between their action and the ensuing effect. We found a reduced intentional binding effect in incongruent compared to congruent conditions in both tasks. The results are discussed within the theoretical framework of the fluency of action.

Initial information prior to movement onset influences kinematics of upward arm pointing movements.

To elaborate a motor plan and perform online control in the gravity field, the brain relies on priors and multisensory integration of information. In particular, afferent and efferent inputs related to the initial state are thought to convey sensorimotor information to plan the upcoming action. Yet it is still unclear to what extent these cues impact motor planning. Here we examined the role of initial information on the planning and execution of arm movements. Participants performed upward arm movements around the shoulder at three speeds and in two arm conditions. In the first condition, the arm was outstretched horizontally and required a significant muscular command to compensate for the gravitational shoulder torque before movement onset. In contrast, in the second condition the arm was passively maintained in the same position with a cushioned support and did not require any muscle contraction before movement execution. We quantified differences in motor performance by comparing shoulder velocity profiles. Previous studies showed that asymmetric velocity profiles reflect an optimal integration of the effects of gravity on upward movements. Consistent with this, we found decreased acceleration durations in both arm conditions. However, early differences in kinematic asymmetries and EMG patterns between the two conditions signaled a change of the motor plan. This different behavior carried on through trials when the arm was at rest before movement onset and may reveal a distinct motor strategy chosen in the context of uncertainty. Altogether, we suggest that the information available online must be complemented by accurate initial information.

Tactile perception during action observation.

It has been suggested that tactile perception becomes less acute during movement to optimize motor control and to prevent an overload of afferent information generated during action. This empirical phenomenon, known as "tactile gating effect," has been associated with mechanisms of sensory feedback prediction. However, less attention has been given to the tactile attenuation effect during the observation of an action. The aim of this study was to investigate whether and how the observation of a goal-directed action influences tactile perception as during overt action. In a first experiment, we recorded vocal reaction times (RTs) of participants to tactile stimulations during the observation of a reach-to-grasp action. The stimulations were delivered on different body parts that could be either congruent or incongruent with the observed effector (the right hand and the right leg, respectively). The tactile stimulation was contrasted with a no body-related stimulation (an auditory beep). We found increased RTs for tactile congruent stimuli compared to both tactile incongruent and auditory stimuli. This effect was reported only during the observation of the reaching phase, whereas RTs were not modulated during the grasping phase. A tactile two-alternative forced-choice (2AFC) discrimination task was then conducted in order to quantify the changes in tactile sensitivity during the observation of the same goal-directed actions. In agreement with the first experiment, the tactile perceived intensity was reduced only during the reaching phase. These results suggest that tactile processing during action observation relies on a process similar to that occurring during action execution.

Visuomotor adaptation to a visual rotation is gravity dependent.

Humans perform vertical and horizontal arm motions with different temporal patterns. The specific velocity profiles are chosen by the central nervous system by integrating the gravitational force field to minimize energy expenditure. However, what happens when a visuomotor rotation is applied, so that a motion performed in the horizontal plane is perceived as vertical? We investigated the dynamic of the adaptation of the spatial and temporal properties of a pointing motion during prolonged exposure to a 90° visuomotor rotation, where a horizontal movement was associated with a vertical visual feedback. We found that participants immediately adapted the spatial parameters of motion to the conflicting visual scene in order to keep their arm trajectory straight. In contrast, the initial symmetric velocity profiles specific for a horizontal motion were progressively modified during the conflict exposure, becoming more asymmetric and similar to those appropriate for a vertical motion. Importantly, this visual effect that increased with repetitions was not followed by a consistent aftereffect when the conflicting visual feedback was absent (catch and washout trials). In a control experiment we demonstrated that an intrinsic representation of the temporal structure of perceived vertical motions could provide the error signal allowing for this progressive adaptation of motion timing. These findings suggest that gravity strongly constrains motor learning and the reweighting process between visual and proprioceptive sensory inputs, leading to the selection of a motor plan that is suboptimal in terms of energy expenditure.

Generalization of motor resonance during the observation of hand, mouth, and eye movements.

Transcranial magnetic stimulation (TMS) of the motor cortex shows that hand action observation (AO) modulates corticospinal excitability (CSE). CSE modulation alternatively maps low-level kinematic characteristics or higher-level features, like object-directed action goals. However, action execution is achieved through the control of muscle synergies, consisting of coordinated patterns of muscular activity during natural movements, rather than single muscles or object-directed goals. This synergistic organization of action execution also underlies the ability to produce the same functional output (i.e., grasping an object) using different effectors. We hypothesize that motor system activation during AO may rely on similar principles. To investigate this issue, we recorded both hand CSE and TMS-evoked finger movements which provide a much more complete description of coordinated patterns of muscular activity. Subjects passively watched hand, mouth and eyelid opening or closing, which are performing non-object-directed (intransitive) actions. Hand and mouth share the same potential to grasp objects, whereas eyelid does not allow object-directed (transitive) actions. Hand CSE modulation generalized to all effectors, while TMS evoked finger movements only to mouth AO. Such dissociation suggests that the two techniques may have different sensitivities to fine motor modulations induced by AO. Differently from evoked movements, which are sensitive to the possibility to achieve object-directed action, CSE is generically modulated by "opening" vs. "closing" movements, independently of which effector was observed. We propose that motor activities during AO might exploit the same synergistic mechanisms shown for the neural control of movement and organized around a limited set of motor primitives.

Activating the motor system through action observation: is this an efficient approach in adults and children?

Observing an action performed by another person to learn a new movement is a frequent experience in adult daily life, such as in sports. However, it is an especially common circumstance during the development of motor skills in childhood. Studies on healthy humans indicate that action observation induces a facilitation in the observer's motor system. This effect is supported by an action-perception matching mechanism available both in adults and in children. Because of the simplicity of action observation, it has been proposed to apply this method in clinical contexts. After a brief, non-exhaustive introduction of the essential features underlying action observation in healthy people, we review recent studies reporting beneficial effects of rehabilitative training based on a combination of action perception and execution. We focus on therapeutic interventions for patients with upper-limb motor disabilities such as adults after stroke or children with hemiplegia due to cerebral palsy. Further, we consider data from basic science demonstrating that the facilitation induced by visual perception of the action can be modulated by the combination of multimodal stimuli related to the movement (e.g. visual and acoustic action-related inputs). In line with this, we discuss possible new directions to improve basic knowledge and therapeutic applications of action observation.

Training the motor cortex by observing the actions of others during immobilization.

Limb immobilization and nonuse are well-known causes of corticomotor depression. While physical training can drive the recovery from nonuse-dependent corticomotor effects, it remains unclear if it is possible to gain access to motor cortex in alternative ways, such as through motor imagery (MI) or action observation (AO). Transcranial magnetic stimulation was used to study the excitability of the hand left motor cortex in normal subjects immediately before and after 10 h of right arm immobilization. During immobilization, subjects were requested either to imagine to act with their constrained limb or to observe hand actions performed by other individuals. A third group of control subjects watched a nature documentary presented on a computer screen. Hand corticomotor maps and recruitment curves reliably showed that AO, but not MI, prevented the corticomotor depression induced by immobilization. Our results demonstrate the existence of a visuomotor mechanism in humans that links AO and execution which is able to effect cortical plasticity in a beneficial way. This facilitation was not related to the action simulation, because it was not induced by explicit MI.

Shaping motor cortex plasticity through proprioception.

Short-term upper limb disuse induces a hemispheric unbalance between the primary motor cortices (M1s). However, it is still unclear whether these changes are mainly attributable to the absence of voluntary movements or to the reduction of proprioceptive information. The goal of this work was to investigate the role of proprioception in modulating hemispheric balance during a short-term right arm immobilization. We evaluated the 2 M1s excitability and the interhemispheric inhibition (IHI) between M1s in 3 groups of healthy subjects. Two groups received during the immobilization a proprioceptive (P-VIB, 80 Hz) and tactile (T-VIB, 30 Hz) vibration to the right hand, respectively. Another group did not receive any conditioning sensory inputs (No-VIB). We found that in the No-VIB and in the T-VIB groups immobilization induced a decrease of left M1 excitability and IHI from left to right hemisphere and an increase of right M1 excitability and IHI from right to left hemisphere. Differently, only a partial decrease in left M1 excitability, no change in right M1 excitability and in IHI was observed in the P-VIB group. Our findings demonstrate that the maintenance of dynamic proprioceptive inputs in an immobilized arm through muscle vibration can prevent the hemispheric unbalance induced by short-term limb disuse.

A unifying model of concurrent spatial and temporal modularity in muscle activity.

Modularity in the central nervous system (CNS), i.e., the brain capability to generate a wide repertoire of movements by combining a small number of building blocks ("modules"), is thought to underlie the control of movement. Numerous studies reported evidence for such a modular organization by identifying invariant muscle activation patterns across various tasks. However, previous studies relied on decompositions differing in both the nature and dimensionality of the identified modules. Here, we derive a single framework that encompasses all influential models of muscle activation modularity. We introduce a new model (named space-by-time decomposition) that factorizes muscle activations into concurrent spatial and temporal modules. To infer these modules, we develop an algorithm, referred to as sample-based nonnegative matrix trifactorization (sNM3F). We test the space-by-time decomposition on a comprehensive electromyographic dataset recorded during execution of arm pointing movements and show that it provides a low-dimensional yet accurate, highly flexible and task-relevant representation of muscle patterns. The extracted modules have a well characterized functional meaning and implement an efficient trade-off between replication of the original muscle patterns and task discriminability. Furthermore, they are compatible with the modules extracted from existing models, such as synchronous synergies and temporal primitives, and generalize time-varying synergies. Our results indicate the effectiveness of a simultaneous but separate condensation of spatial and temporal dimensions of muscle patterns. The space-by-time decomposition accommodates a unified view of the hierarchical mapping from task parameters to coordinated muscle activations, which could be employed as a reference framework for studying compositional motor control.

Energy-related optimal control accounts for gravitational load: comparing shoulder, elbow, and wrist rotations.

We permanently deal with gravity force. Experimental evidences revealed that moving against gravity strongly differs from moving along the gravity vector. This directional asymmetry has been attributed to an optimal planning process that optimizes gravity force effects to minimize energy. Yet, only few studies have considered the case of vertical movements in the context of optimal control. What kind of cost is better suited to explain kinematic patterns in the vertical plane? Here, we aimed to understand further how the central nervous system (CNS) plans and controls vertical arm movements. Our reasoning was the following: if the CNS optimizes gravity mechanical effects on the moving limbs, kinematic patterns should change according to the direction and the magnitude of the gravity torque being encountered in the motion. Ten subjects carried out single-joint movements, i.e., rotation around the shoulder (whole arm), elbow (forearm), and wrist (hand) joints, in the vertical plane. Joint kinematics were analyzed and compared with various theoretical optimal model predictions (minimum absolute work-jerk, jerk, torque change, and variance). We found both direction-dependent and joint-dependent variations in several kinematic parameters. Notably, directional asymmetries decreased according to a proximodistal gradient. Numerical simulations revealed that our experimental findings could be attributed to an optimal motor planning (minimum absolute work-jerk) that integrates the direction and the magnitude of gravity torque and minimizes the absolute work of forces (energy-related cost) around each joint. Present results support the general idea that the CNS implements optimal solutions according to the dynamic context of the action.

Reach endpoint formation during the visuomotor planning of free arm pointing.

Volitional motor control generally involves deciding 'where to go' and 'how to go there'. Understanding how these two constituent pieces of motor decision coordinate is an important issue in neuroscience. Although the two processes could be intertwined, they are generally thought to occur in series, whereby visuomotor planning begins with the knowledge of a final hand position to attain. However, daily activities are often compatible with an infinity of final hand positions. The purpose of the present study was to test whether the reach endpoint ('where') is an input of arm motor planning ('how') in such ecological settings. To this end, we considered a free pointing task, namely arm pointing to a long horizontal line, and investigated the formation of the reach endpoint through eye-hand coordination. Although eye movement always preceded hand movement, our results showed that the saccade initiation was delayed by ~ 120 ms on average when the line was being pointed to as compared with a single target dot; the hand reaction time was identical in the two conditions. When the latency of saccade initiation was relatively brief, subjects often performed double, or even triple, saccades before hand movement onset. The number of saccades triggered was found to significantly increase as a function of the primary saccade latency and accuracy. These results suggest that knowledge about the reach endpoint built up gradually along with the arm motor planning process, and that the oculomotor system delayed the primary reach-related saccade in order to gain more information about the final hand position.

The effect of the preferred hand on drawing movement.

The observation that different effectors can execute the same movement suggests functional equivalences driven by limb independent representation of action in the central nervous system. A common invariant motor behavior is the speed and curvature coupling (the 1/3 power law), a low dimensional (abstract) descriptor of movement which is resilient to different sensorimotor contexts. Our purpose is to verify the consistency of such motor equivalence during a drawing task, by testing the effect of manual dominance and movement speed on motor performance. We hypothesize that abstract kinematic variables are not the most resistant to speed or limb effector changes. The results show specific effects of speed and hand side on the drawing task. Movement duration, speed-curvature covariation, and maximum velocity were not significantly affected by hand side, while geometrical features were strongly speed and limb dependent. However, intra-trial analysis performed over the successive drawing movements reveals a significant hand side effect on the variability of movement vigor and velocity-curvature relationship (the 1/3 PL). The identified effects of speed and hand dominance on the kinematic parameters suggest different neural strategies, in a pattern that does not go from the most abstract to the least abstract component, as proposed by the traditional hierarchical organization of the motor plan.

Motor invariants in action execution and perception.

The nervous system is sensitive to statistical regularities of the external world and forms internal models of these regularities to predict environmental dynamics. Given the inherently social nature of human behavior, being capable of building reliable predictive models of others' actions may be essential for successful interaction. While social prediction might seem to be a daunting task, the study of human motor control has accumulated ample evidence that our movements follow a series of kinematic invariants, which can be used by observers to reduce their uncertainty during social exchanges. Here, we provide an overview of the most salient regularities that shape biological motion, examine the role of these invariants in recognizing others' actions, and speculate that anchoring socially-relevant perceptual decisions to such kinematic invariants provides a key computational advantage for inferring conspecifics' goals and intentions.

Action Observation Therapy for Arm Recovery after Stroke: A Preliminary Investigation on a Novel Protocol with EEG Monitoring.

This preliminary study introduces a novel action observation therapy (AOT) protocol associated with electroencephalographic (EEG) monitoring to be used in the future as a rehabilitation strategy for the upper limb in patients with subacute stroke. To provide initial evidence on the usefulness of this method, we compared the outcome of 11 patients who received daily AOT for three weeks with that of patients who undertook two other approaches recently investigated by our group, namely intensive conventional therapy (ICT), and robot-assisted therapy combined with functional electrical stimulation (RAT-FES). The three rehabilitative interventions showed similar arm motor recovery as indexed by Fugl-Meyer's assessment of the upper extremity (FMA_UE) and box and block test (BBT). The improvement in the FMA_UE was yet more favourable in patients with mild/moderate motor impairments who received AOT, in contrast with patients carrying similar disabilities who received the other two treatments. This suggests that AOT might be more effective in this subgroup of patients, perhaps because the integrity of their mirror neurons system (MNS) was more preserved, as indexed by EEG recording from central electrodes during action observation. In conclusion, AOT may reveal an effective rehabilitative tool in patients with subacute stroke; the EEG evaluation of MNS integrity may help to select patients who could maximally benefit from this intervention.