Interhemispheric Inhibition during Mental Actions of Different Complexity

Several investigations suggest that actual and mental actions trigger similar neural substrates. Yet, neurophysiological evidences on the nature of interhemispheric interactions during mental movements are still meagre. Here, we asked whether the content of mental images, investigated by task complexity, is finely represented in the inhibitory interactions between the two primary motor cortices (M1s). Subjects’ left M1 was stimulated by means of transcranial magnetic stimulation (TMS) while they were performing actual or mental movements of increasing complexity with their right hand and exerting a maximum isometric force with their left thumb and index. Thus, we simultaneously assessed the corticospinal excitability in the right opponent pollicis muscle (OP) and the ipsilateral silent period (iSP) in the left OP during actual and mental movements. Corticospinal excitability in right OP increased during actual and mental movements, but task complexity-dependent changes were only observed during actual movements. Interhemispheric motor inhibition in the left OP was similarly modulated by task complexity in both mental and actual movements. Precisely, the duration and the area of the iSP increased with task complexity in both movement conditions. Our findings suggest that mental and actual movements share similar inhibitory neural circuits between the two homologous primary motor cortex areas.     

Mental Representation of Arm Motion Dynamics in Children and Adolescents

Motor imagery, i.e., a mental state during which an individual internally represents an action without any overt motor output, is a potential tool to investigate action representation during development. Here, we took advantage of the inertial anisotropy phenomenon to investigate whether children can generate accurate motor predictions for movements with varying dynamics. Children (9 and 11 years), adolescents (14 years) and young adults (21 years) carried-out actual and mental arm movements in two different directions in the horizontal plane: rightwards (low inertia) and leftwards (high inertia). We recorded and compared actual and mental movement times. We found that actual movement times were greater for leftward than rightward arm movements in all groups. For mental movements, differences between leftward versus rightward movements were observed in the adults and adolescents, but not among the children. Furthermore, significant differences between actual and mental times were found at 9 and 11 years of age in the leftward direction. The ratio R/L (rightward direction/leftward direction), which indicates temporal differences between low inertia and high inertia movements, was inferior to 1 at all ages, except for the mental movements at 9 years of age, indicating than actual and mental movements were shorter for the rightward than leftward direction. Interestingly, while the ratio R/L of actual movements was constant across ages, it gradually decreased with age for mental movements. The ratio A/M (actual movement/mental movement), which indicates temporal differences between actual and mental movements, was near to 1 in the adults'' groups, denoting accurate mental timing. In children and adolescents, an underestimation of mental movement times appeared for the leftward movements only. However, this overestimation gradually decreased with age. Our results showed a refinement in the motor imagery ability during development. Action representation reached maturation at adolescence, during which mental actions were tightly related to their actual production.     

Abnormalities in the awareness and control of action

Much of the functioning of the motor system occurs without awareness. Nevertheless, we are aware of some aspects of the current state of the system and we can prepare and make movements in the imagination. These mental representations of the actual and possible states of the system are based on two sources: sensory signals from skin and muscles, and the stream of motor commands that have been issued to the system. Damage to the neural substrates of the motor system can lead to abnormalities in the awareness of action as well as defects in the control of action. We provide a framework for understanding how these various abnormalities of awareness can arise. Patients with phantom limbs or with anosognosia experience the illusion that they can move their limbs. We suggest that these representations of movement are based on streams of motor commands rather than sensory signals. Patients with utilization behaviour or with delusions of control can no longer properly link their intentions to their actions. In these cases the impairment lies in the representation of intended movements. The location of the neural damage associated with these disorders suggests that representations of the current and predicted state of the motor system are in parietal cortex, while representations of intended actions are found in prefrontal and premotor cortex.     

The Relation between Geometry and Time in Mental Actions

Mental imagery is a cognitive tool that helps humans take decisions by simulating past and future events. The hypothesis has been advanced that there is a functional equivalence between actual and mental movements. Yet, we do not know whether there are any limitations to its validity even in terms of some fundamental features of actual movements, such as the relationship between space and time. Although it is impossible to directly measure the spatiotemporal features of mental actions, an indirect investigation can be conducted by taking advantage of the constraints existing in planar drawing movements and described by the two-thirds power law (2/3PL). This kinematic law describes one of the most impressive regularities observed in biological movements: movement speed decreases when curvature increases. Here, we compared the duration of identical actual and mental arm movements by changing the constraints imposed by the 2/3PL. In the first two experiments, the length of the trajectory remained constant, while its curvature (Experiment 1) or its number of inflexions (Experiment 2) was manipulated. The results showed that curvature, but not the number of inflexions, proportionally and similarly affected actual and mental movement duration, as expected from the 2/3PL. Two other control experiments confirmed that the results of Experiment 1 were not attributable to eye movements (Experiment 3) or to the perceived length of the displayed trajectory (Experiment 4). Altogether, our findings suggest that mental movement simulation is tuned to the kinematic laws characterizing actions and that kinematics of actual and mental movements is completely specified by the representation of their geometry.     

The knowledge base of the oculomotor system.

In everyday life, eye movements enable the eyes to gather the information required for motor actions. They are thus proactive, anticipating actions rather than just responding to stimuli. This means that the oculomotor system needs to know where to look and what to look for. Using examples from table tennis, driving and music reading we show that the information the eye movement system requires is very varied in origin and highly task specific, and it is suggested that the control program or schema for a particular action must include directions for the oculomotor and visual processing systems. In many activities (reading text and music, typing, steering) processed information is held in a memory buffer for a period of about a second. This permits a match between the discontinuous input from the eyes and continuous motor output, and in particular allows the eyes to be involved in more than one task.     

Task Complexity Differentially Affects Executed and Imagined Movement Preparation: Evidence from Movement-Related Potentials

Background

The neural simulation theory predicts similarity for the neural mechanisms subserving overt (motor execution) and covert (movement imagination) actions. Here we tested this prediction for movement preparation, a key characteristic of motor cognition.

Methodology/Principal Findings

High-density electroencephalogram (EEG) was recorded during covert and overt actions. Movement preparation was studied with a motor priming paradigm, which varied task complexity and amount of advance information. Participants performed simple or complex sequential finger movements either overtly or covertly. Advance information was either fully predictive or partially predictive. Stimulus-locked event-related potential (ERP) data showed the typical pattern of foreperiod activation for overt and covert movements. The foreperiod contingent negative variation (CNV) differed between simple and complex movements only in the execution task. ERP topographies differed between execution and imagination only when advance information was fully predictive.

Conclusions/Significance

Results suggest a differential contribution of the movement preparation network to action imagination and execution. Overt and covert actions seem to involve similar though not identical mechanisms, where overt actions engage a more fine-grained modulation of covert preparatory states.     

Motor representation of actions in children with autism

Background

Children with Autistic Spectrum Disorders (ASD) are frequently hampered by motor impairment, with difficulties ranging from imitation of actions to recognition of motor intentions. Such a widespread inefficiency of the motor system is likely to interfere on the ontogeny of both motor planning and understanding of the goals of actions, thus delivering its ultimate effects on the emergence of social cognition.

Methodology/Principal Findings

We investigate the organization of action representation in 15 high functioning ASD (mean age: 8.11) and in two control samples of typically developing (TD) children: the first one, from a primary school, was matched for chronological age (CA), the second one, from a kindergarten, comprised children of much younger age (CY). We used nine newly designed behavioural motor tasks, aiming at exploring three domains of motor cognition: 1) imitation of actions, 2) production of pantomimes, and 3) comprehension of pantomimes. The findings reveal that ASD children fare significantly worse than the two control samples in each of the inspected components of the motor representation of actions, be it the imitation of gestures, the self-planning of pantomimes, or the (verbal) comprehension of observed pantomimes. In the latter task, owing to its cognitive complexity, ASD children come close to the younger TD children’s level of performance; yet they fare significantly worse with respect to their age-mate controls. Overall, ASD children reveal a profound damage to the mechanisms that control both production and pre-cognitive “comprehension” of the motor representation of actions.

Conclusions/Significance

Our findings suggest that many of the social cognitive impairments manifested by ASD individuals are likely rooted in their incapacity to assemble and directly grasp the intrinsic goal-related organization of motor behaviour. Such impairment of motor cognition might be partly due to an early damage of the Mirror Neuron Mechanism (MNM).     

A word in the hand: action, gesture and mental representation in humans and non-human primates

The movements we make with our hands both reflect our mental processes and help to shape them. Our actions and gestures can affect our mental representations of actions and objects. In this paper, we explore the relationship between action, gesture and thought in both humans and non-human primates and discuss its role in the evolution of language. Human gesture (specifically representational gesture) may provide a unique link between action and mental representation. It is kinaesthetically close to action and is, at the same time, symbolic. Non-human primates use gesture frequently to communicate, and do so flexibly. However, their gestures mainly resemble incomplete actions and lack the representational elements that characterize much of human gesture. Differences in the mirror neuron system provide a potential explanation for non-human primates' lack of representational gestures; the monkey mirror system does not respond to representational gestures, while the human system does. In humans, gesture grounds mental representation in action, but there is no evidence for this link in other primates. We argue that gesture played an important role in the transition to symbolic thought and language in human evolution, following a cognitive leap that allowed gesture to incorporate representational elements.     

Action Possibility Judgments of People with Varying Motor Abilities Due to Spinal Cord Injury

Predictions about one''s own action capabilities as well as the action capabilities of others are thought to be based on a simulation process involving linked perceptual and motor networks. Given the central role of motor experience in the formation of these networks, one''s present motor capabilities are thought to be the basis of their perceptual judgments about actions. However, it remains unknown whether the ability to form these action possibility judgments is affected by performance related changes in the motor system. To determine if judgments of action capabilities are affected by long-term changes in one''s own motor capabilities, participants with different degrees of upper-limb function due to their level (cervical vs. below cervical) of spinal cord injury (SCI) were tested on a perceptual-motor judgment task. Participants observed apparent motion videos of reciprocal aiming movements with varying levels of difficulty. For each movement, participants determined the shortest movement time (MT) at which they themselves and a young adult could perform the task while maintaining accuracy. Participants also performed the task. Analyses of MTs revealed that perceptual judgments for participant''s own movement capabilities were consistent with their actual performance- people with cervical SCI had longer judged and actual MTs than people with below cervical SCI. However, there were no between-group differences in judged MTs for the young adult. Although it is unclear how the judgments were adjusted (altered simulation vs. threshold modification), the data reveal that people with different motor capabilities due to SCI are not completely biased by their present capabilities and can effectively adjust their judgments to estimate the actions of others.     

Mental Representation and Mental Practice: Experimental Investigation on the Functional Links between Motor Memory and Motor Imagery

Recent research on mental representation of complex action has revealed distinct differences in the structure of representational frameworks between experts and novices. More recently, research on the development of mental representation structure has elicited functional changes in novices'' representations as a result of practice. However, research investigating if and how mental practice adds to this adaptation process is lacking. In the present study, we examined the influence of mental practice (i.e., motor imagery rehearsal) on both putting performance and the development of one''s representation of the golf putt during early skill acquisition. Novice golfers (N = 52) practiced the task of golf putting under one of four different practice conditions: mental, physical, mental-physical combined, and no practice. Participants were tested prior to and after a practice phase, as well as after a three day retention interval. Mental representation structures of the putt were measured, using the structural dimensional analysis of mental representation. This method provides psychometric data on the distances and groupings of basic action concepts in long-term memory. Additionally, putting accuracy and putting consistency were measured using two-dimensional error scores of each putt. Findings revealed significant performance improvements over the course of practice together with functional adaptations in mental representation structure. Interestingly, after three days of practice, the mental representations of participants who incorporated mental practice into their practice regime displayed representation structures that were more similar to a functional structure than did participants who did not incorporate mental practice. The findings of the present study suggest that mental practice promotes the cognitive adaptation process during motor learning, leading to more elaborate representations than physical practice only.     

Interaction between descending input and thoracic reflexes for joint coordination in cockroach. II Comparative studies on tethered turning and searching

Tethered cockroaches turn from unilateral antennal contact using asymmetrical movements of mesothoracic (T2) legs (Mu and Ritzmannin J Comp Physiol A 191:1037–1054, 2005). During the turn, the leg on the inside of the turn (the inside T2 leg) has distinctly different motor patterns from those in straight walking. The transformation from walking to inside leg turning could be triggered by descending commands that alter a few critical reflexes that start a cascade of physical changes in leg movement or posture, leading to further alterations. This hypothesis has two implications: First, the descending activities must be able to influence thoracic reflexes. Second, one should be able to initiate the turning motor pattern in the absence of descending signals by mimicking a point farther down in the reflex cascade. We addressed the first implication in the companion paper. To examine the second implication, we compared kinematics and motor activities of the T2 leg during searching with that of inside leg turning. The reaching movements made during searching were found to be similar to the movements made by the inside leg during turning. Moreover, even after disconnecting the brain from the thoracic ganglia the reaching movements were similar. This observation is consistent with the second implication from the hypothesis.     

The Cerebellum Predicts the Temporal Consequences of Observed Motor Acts

It is increasingly clear that we extract patterns of temporal regularity between events to optimize information processing. The ability to extract temporal patterns and regularity of events is referred as temporal expectation. Temporal expectation activates the same cerebral network usually engaged in action selection, comprising cerebellum. However, it is unclear whether the cerebellum is directly involved in temporal expectation, when timing information is processed to make predictions on the outcome of a motor act. Healthy volunteers received one session of either active (inhibitory, 1Hz) or sham repetitive transcranial magnetic stimulation covering the right lateral cerebellum prior the execution of a temporal expectation task. Subjects were asked to predict the end of a visually perceived human body motion (right hand handwriting) and of an inanimate object motion (a moving circle reaching a target). Videos representing movements were shown in full; the actual tasks consisted of watching the same videos, but interrupted after a variable interval from its onset by a dark interval of variable duration. During the ‘dark’ interval, subjects were asked to indicate when the movement represented in the video reached its end by clicking on the spacebar of the keyboard. Performance on the timing task was analyzed measuring the absolute value of timing error, the coefficient of variability and the percentage of anticipation responses. The active group exhibited greater absolute timing error compared with the sham group only in the human body motion task. Our findings suggest that the cerebellum is engaged in cognitive and perceptual domains that are strictly connected to motor control.     

Influence of Action-Effect Associations Acquired by Ideomotor Learning on Imitation

According to the ideomotor theory, actions are represented in terms of their perceptual effects, offering a solution for the correspondence problem of imitation (how to translate the observed action into a corresponding motor output). This effect-based coding of action is assumed to be acquired through action-effect learning. Accordingly, performing an action leads to the integration of the perceptual codes of the action effects with the motor commands that brought them about. While ideomotor theory is invoked to account for imitation, the influence of action-effect learning on imitative behavior remains unexplored. In two experiments, imitative performance was measured in a reaction time task following a phase of action-effect acquisition. During action-effect acquisition, participants freely executed a finger movement (index or little finger lifting), and then observed a similar (compatible learning) or a different (incompatible learning) movement. In Experiment 1, finger movements of left and right hands were presented as action-effects during acquisition. In Experiment 2, only right-hand finger movements were presented during action-effect acquisition and in the imitation task the observed hands were oriented orthogonally to participants’ hands in order to avoid spatial congruency effects. Experiments 1 and 2 showed that imitative performance was improved after compatible learning, compared to incompatible learning. In Experiment 2, although action-effect learning involved perception of finger movements of right hand only, imitative capabilities of right- and left-hand finger movements were equally affected. These results indicate that an observed movement stimulus processed as the effect of an action can later prime execution of that action, confirming the ideomotor approach to imitation. We further discuss these findings in relation to previous studies of action-effect learning and in the framework of current ideomotor approaches to imitation.     

Parietal and hippocampal contribution to topokinetic and topographic memory.

This paper reviews the involvement of the parietal cortex and the hippocampus in three kinds of spatial memory tasks which all require a memory of a previously experienced movement in space. The first task compared, by means of positron emission tomography (PET) scan techniques, the production, in darkness, of self-paced saccades (SAC) with the reproduction, in darkness, of a previously learned sequence of saccades to visual targets (SEQ). The results show that a bilateral increase of activity was seen in the depth of the intraparietal sulcus and the medial superior parietal cortex (superior parietal gyrus and precuneus) together with the frontal sulcus but only in the SEQ task, which involved memory of the previously seen targets and possibly also motor memory. The second task is the vestibular memory contingent task, which requires that the subject makes, in darkness, a saccade to the remembered position of a visual target after a passively imposed whole-body rotation. Deficits in this task, which involves vestibular memory, were found predominantly in patients with focal vascular lesions in the parieto-insular (vestibular) cortex, the supplementary motor area-supplementary eye field area, and the prefrontal cortex. The third task requires mental navigation from the memory of a previously learned route in a real environment (the city of Orsay in France). A PET scan study has revealed that when subjects were asked to remember visual landmarks there was a bilateral activation of the middle hippocampal regions, left inferior temporal gyrus, left hippocampal regions, precentral gyrus and posterior cingulate gyrus. If the subjects were asked to remember the route, and their movements along this route, bilateral activation of the dorsolateral cortex, posterior hippocampal areas, posterior cingulate gyrus, supplementary motor areas, right middle hippocampal areas, left precuneus, middle occipital gyrus, fusiform gyrus and lateral premotor area was found. Subtraction between the two conditions reduced the activated areas to the left hippocampus, precuneus and insula. These data suggest that the hippocampus and parietal cortex are both involved in the dynamic aspects of spatial memory, for which the name ''topokinetic memory'' is proposed. These dynamic aspects could both overlap and be different from those involved in the cartographic and static aspects of ''topographic'' memory.     

Simulating My Own or Others Action Plans? – Motor Representations,Not Visual Representations Are Recalled in Motor Memory

Action plans are not generated from scratch for each movement, but features of recently generated plans are recalled for subsequent movements. This study investigated whether the observation of an action is sufficient to trigger plan recall processes. Participant dyads performed an object manipulation task in which one participant transported a plunger from an outer platform to a center platform of different heights (first move). Subsequently, either the same (intra-individual task condition) or the other participant (inter-individual task condition) returned the plunger to the outer platform (return moves). Grasp heights were inversely related to center target height and similar irrespective of direction (first vs. return move) and task condition (intra- vs. inter-individual). Moreover, participants'' return move grasp heights were highly correlated with their own, but not with their partners'' first move grasp heights. Our findings provide evidence that a simulated action plan resembles a plan of how the observer would execute that action (based on a motor representation) rather than a plan of the actually observed action (based on a visual representation).     

Beyond Motor Scheme: A Supramodal Distributed Representation in the Action-Observation Network

The representation of actions within the action-observation network is thought to rely on a distributed functional organization. Furthermore, recent findings indicate that the action-observation network encodes not merely the observed motor act, but rather a representation that is independent from a specific sensory modality or sensory experience. In the present study, we wished to determine to what extent this distributed and ‘more abstract’ representation of action is truly supramodal, i.e. shares a common coding across sensory modalities. To this aim, a pattern recognition approach was employed to analyze neural responses in sighted and congenitally blind subjects during visual and/or auditory presentation of hand-made actions. Multivoxel pattern analyses-based classifiers discriminated action from non-action stimuli across sensory conditions (visual and auditory) and experimental groups (blind and sighted). Moreover, these classifiers labeled as ‘action’ the pattern of neural responses evoked during actual motor execution. Interestingly, discriminative information for the action/non action classification was located in a bilateral, but left-prevalent, network that strongly overlaps with brain regions known to form the action-observation network and the human mirror system. The ability to identify action features with a multivoxel pattern analyses-based classifier in both sighted and blind individuals and independently from the sensory modality conveying the stimuli clearly supports the hypothesis of a supramodal, distributed functional representation of actions, mainly within the action-observation network.     

Control over conflict during movement preparation: role of posterior parietal cortex

Flexible behavior in humans often requires that rapid choices be made between conflicting action plans. Although much attention has focused on prefrontal regions, little is understood about the contribution of parietal cortex under situations of response conflict. Here we show that right parietal damage associated with spatial neglect leads to paradoxical facilitation (speeding) of rightward movements in the presence of conflicting leftward response plans. These findings indicate a critical role for parietal regions in action planning when there is response competition. In contrast, patients with prefrontal damage have an augmented cost of conflict for both leftward and rightward movements. The results suggest involvement of two independent systems in situations of response conflict, with right parietal cortex being a crucial site for automatic activation of competing motor plans and prefrontal regions acting independently to inhibit action plans irrelevant to current task goals.     

From thought to action: the parietal cortex as a bridge between perception, action, and cognition

The lateral intraparietal area (LIP) is a subdivision of the inferior parietal lobe that has been implicated in the guidance of spatial attention. In a variety of tasks, LIP provides a "salience representation" of the external world-a topographic visual representation that encodes the locations of salient or behaviorally relevant objects. Recent neurophysiological experiments show that this salience representation incorporates information about multiple behavioral variables-such as a specific motor response, reward, or category membership-associated with the task-relevant object. This integration occurs in a wide variety of tasks, including those requiring eye or limb movements or goal-directed or nontargeting operant responses. Thus, LIP acts as a multifaceted behavioral integrator that binds visuospatial, motor, and cognitive information into a topographically organized signal of behavioral salience. By specifying attentional priority as a synthesis of multiple task demands, LIP operates at the interface of perception, action, and cognition.     

Updating visual space during motion in depth

Whether we are riding in a car or walking, our internal map of the environment must be continuously updated to maintain spatial constancy. Using a memory eye movement task, we examined whether nonhuman primates can keep track of changes in the distance of nearby objects when moved toward or away from them. We report that memory-guided eye movements take into account the change in distance traveled, illustrating that monkeys can update retinal disparity information in order to reconstruct three-dimensional visual space during motion in depth. This ability was compromised after destruction of the vestibular labyrinths, suggesting that the extraretinal signals needed for updating can arise from vestibular information signaling self-motion through space.