Accurate reaching after active but not passive movements of the hand: evidence for forward modeling

Converging behavioral findings support recent models of motor control suggesting that estimates of the future positions of a limb as well as the expected sensory consequences of a planned movement may be derived, in part, from efference copies of motor commands. These estimates are referred to as forward models. However, relatively little behavioral evidence has been obtained for proposed forward models that provide on-line estimates of current position. We report data from a patient (JD) who reached accurately to visualized targets with and without vision of her hand despite substantial proprioceptive loss. Additionally, we administered a double-start reaching test to examine the possibility that efference copy information could be used to estimate current limb position. JD reached accurately, without vision, to a final target after actively reaching to a landmark, but exhibited severely impaired reaching after passive movements to the landmark. This finding suggests that forward modeling of efference copy signals may provide relatively accurate estimates of current limb position for the purpose of motor planning. The possibility that such estimates may also contribute to the awareness of body position and to self-recognition is discussed.     

Differential reliance of chimpanzees and humans on automatic and deliberate control of motor actions

Humans are often unaware of how they control their limb motor movements. People pay attention to their own motor movements only when their usual motor routines encounter errors. Yet little is known about the extent to which voluntary actions rely on automatic control and when automatic control shifts to deliberate control in nonhuman primates. In this study, we demonstrate that chimpanzees and humans showed similar limb motor adjustment in response to feedback error during reaching actions, whereas attentional allocation inferred from gaze behavior differed. We found that humans shifted attention to their own motor kinematics as errors were induced in motor trajectory feedback regardless of whether the errors actually disrupted their reaching their action goals. In contrast, chimpanzees shifted attention to motor execution only when errors actually interfered with their achieving a planned action goal. These results indicate that the species differed in their criteria for shifting from automatic to deliberate control of motor actions. It is widely accepted that sophisticated motor repertoires have evolved in humans. Our results suggest that the deliberate monitoring of one’s own motor kinematics may have evolved in the human lineage.     

Effects of motor intention on the perception of somatosensory events: A behavioural and functional magnetic resonance imaging study

The intention to execute a movement can modulate our perception of sensory events, and this modulation is observed ahead of both ocular and upper limb movements. However, theoretical accounts of these effects, and also the empirical data, are often contradictory. Accounts of “active touch”, and the premotor theory of attention, have emphasized how movement intention leads to enhanced perceptual processing at the target of a movement, or on the to-be-moved effector. By contrast, recent theories of motor control emphasize how internal “forward” model (FM) estimates may be used to cancel or attenuate sensory signals that arise as a result of self-generated movements. We used behavioural and functional brain imaging (functional magnetic resonance imaging, fMRI) to investigate how perception of a somatosensory stimulus differed according to whether it was delivered to a hand that was about to execute a reaching movement or the alternative, nonmoving, hand. The results of our study demonstrate that a somatosensory stimulus delivered to a hand that is being prepared for movement is perceived to have occurred later than when that same stimulus is delivered to a nonmoving hand. This result indicates that it takes longer for a tactile stimulus to be detected when it is delivered to a moving limb and may correspond to a change in perceptual threshold. Our behavioural results are paralleled by the results of our fMRI study that demonstrated that there were significantly reduced blood-oxygen-level-dependent (BOLD) responses within the parietal operculum and insula following somatosensory stimulation of the hand being prepared for movement, compared to when an identical stimulus was delivered to a nonmoving hand. These findings are consistent with the prediction of FM accounts of motor control that postulate that central sensory suppression of somatosensation accompanies self-generated limb movements, and with previous reports indicating that effects of sensory suppression are observed in higher order somatosensory regions.     

Effects of motor intention on the perception of somatosensory events: a behavioural and functional magnetic resonance imaging study

The intention to execute a movement can modulate our perception of sensory events, and this modulation is observed ahead of both ocular and upper limb movements. However, theoretical accounts of these effects, and also the empirical data, are often contradictory. Accounts of "active touch", and the premotor theory of attention, have emphasized how movement intention leads to enhanced perceptual processing at the target of a movement, or on the to-be-moved effector. By contrast, recent theories of motor control emphasize how internal "forward" model (FM) estimates may be used to cancel or attenuate sensory signals that arise as a result of self-generated movements. We used behavioural and functional brain imaging (functional magnetic resonance imaging, fMRI) to investigate how perception of a somatosensory stimulus differed according to whether it was delivered to a hand that was about to execute a reaching movement or the alternative, nonmoving, hand. The results of our study demonstrate that a somatosensory stimulus delivered to a hand that is being prepared for movement is perceived to have occurred later than when that same stimulus is delivered to a nonmoving hand. This result indicates that it takes longer for a tactile stimulus to be detected when it is delivered to a moving limb and may correspond to a change in perceptual threshold. Our behavioural results are paralleled by the results of our fMRI study that demonstrated that there were significantly reduced blood-oxygen-level-dependent (BOLD) responses within the parietal operculum and insula following somatosensory stimulation of the hand being prepared for movement, compared to when an identical stimulus was delivered to a nonmoving hand. These findings are consistent with the prediction of FM accounts of motor control that postulate that central sensory suppression of somatosensation accompanies self-generated limb movements, and with previous reports indicating that effects of sensory suppression are observed in higher order somatosensory regions.     

Motor IOR revealed for reaching

Inhibition of return (IOR) is a spatial phenomenon that is thought to promote visual search functions by biasing attention and eye movements toward novel locations. Considerable research suggests distinct sensory and motor flavors of IOR, but it is not clear whether the motor type can affect responses other than eye movements. Most studies claiming to reveal motor IOR in the reaching control system have been confounded by their use of peripheral signals, which can invoke sensory rather than motor-based inhibitory effects. Other studies have used central signals to focus on motor, rather than sensory, effects in arm movements but have failed to observe IOR and have concluded that the motor form of IOR is restricted to the oculomotor system. Here, we show the first clear evidence that motor IOR can be observed for reaching movements when participants respond to consecutive central stimuli. This observation suggests that motor IOR serves a more general function than the facilitation of visual search, perhaps reducing the likelihood of engaging in repetitive behavior.     

The man who executed "imagined" movements: evidence for dissociable components of the body schema

We examined the nature of representations underlying motor imagery and execution in a patient (CW) with bilateral parietal lesions. When imagining hand movements, CW executed the imagined motor act but was unaware of the movements. These movements were significantly more accurate than volitional movements for the left but not right hand. CW also exhibited preserved motor imagery for the left but not right hand. Consistent with previous accounts, these findings suggest that motor imagery may normally involve the inhibition of movements. CW's unawareness of movements during motor imagery may reflect inattention or misattribution of the unexpected sensory feedback. Furthermore, in line with current models of motor control, motor imagery may depend on the integrity of a "forward model" derived from motor outflow information to generate a prediction of the consequences of a motor command. Such predictions appear to be preserved for imagery of left but not right hand movements in CW. Action may additionally depend on precise updating of effector position derived from the comparison of predicted and actual sensory information. We propose that CW's impaired volitional movements may be attributable to the degradation of such an updating mechanism.     

Aspects of body self-calibration

The representation of body orientation and configuration is dependent on multiple sources of afferent and efferent information about ongoing and intended patterns of movement and posture. Under normal terrestrial conditions, we feel virtually weightless and we do not perceive the actual forces associated with movement and support of our body. It is during exposure to unusual forces and patterns of sensory feedback during locomotion that computations and mechanisms underlying the ongoing calibration of our body dimensions and movements are revealed. This review discusses the normal mechanisms of our position sense and calibration of our kinaesthetic, visual and auditory sensory systems, and then explores the adaptations that take place to transient Coriolis forces generated during passive body rotation. The latter are very rapid adaptations that allow body movements to become accurate again, even in the absence of visual feedback. Muscle spindle activity interpreted in relation to motor commands and internally modeled reafference is an important component in permitting this adaptation. During voluntary rotary movements of the body, the central nervous system automatically compensates for the Coriolis forces generated by limb movements. This allows accurate control to be maintained without our perceiving the forces generated.     

Functional roles of the proprioceptive system in the control of goal-directed movement.

This article explored functional roles of the proprioceptive system during the control of goal-directed movements. Proprioceptive information contributes to the control of movement through both reflex and central connections. Spinal and transcortical reflex loops establish a servomechanism which provides automatic corrections of unexpected changes in muscle length and allows compensation for undesirable irregularities in the mechanical properties of muscles by modulating limb stiffness at the subconscious level. Central connections provide the control system with information about peripheral states which is used in voluntary components of movement control. Before the initiation of movement, proprioceptive information about initial limb orientation becomes a basis for the programming of motor commands. During a movement, proprioceptive input about velocities and angular displacements of a limb is used to regulate movement by triggering planned sequences of muscle activation and modulating motor commands. After movement, feedback produced by responses is compared with previously stored information, verifying the quality of the movement. Considering potential roles of the reflex and central connections, the proprioceptive system seems to constitute an important aspect of motor control mechanisms, providing the control system with efficiency and flexibility in the regulation of goal-directed movements.     

Sensory feedback in the learning of a novel motor task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement an provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than "natural" (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Is the cerebellum a smith predictor?

The motor system may use internal predictive models of the motor apparatus to achieve better control than would be possible by negative feedback. Several theories have proposed that the cerebellum may form these predictive representations. In this article, we review these theories and try to unify them by reference to an engineering control model known as a Smith Predictor. We suggest that the cerebellum forms two types of internal model. One model is a forward predictive model of the motor apparatus (e.g., limb and muscle), providing a rapid prediction of the sensory consequences of each movement. The second model is of the time delays in the control loop (due to receptor and effector delays, axonal conductances, and cognitive processing delays). This model delays a copy of the rapid prediction so that it can be compared in temporal register with actual sensory feedback from the movement. The result of this comparison is used both to correct for errors in performance and as a training signal to learn the first model. We discuss evidence that the cerebellum could form both of these models and suggest that the cerebellum may hold at least two separate Smith Predictors. One, in the lateral cerebellum, would predict the movement outcome in visual, egocentric, or peripersonal coordinates. Another, in the intermediate cerebellum, would predict the consequences in motor coordinates. Generalization of the Smith Predictor theory is discussed in light of cerebellar involvement in nonmotor control systems, including autonomic functions and cognition.     

Sensory Feedback in the Learning of a Novel Motor Task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement can provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than “natural” (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.     

Terminal accuracy of unexpectedly loaded rapid movements: evidence for a mass-spring mechanism in programming

Experiments using rapid-positioning movements in humans, where the subject is suddenly and unexpectedly provided with a change in the load characteristics of the limb, are described. Taken together, the pattern of results supports a mass-spring model of unidirectional limb action, where the limb moves to a position defined by the relative tensions in the agonist and antagonist. As well, various results provide evidence contrary to predictions from an impulse-timing viewpoint, where the motor program times the onset of impulses to the musculature, and against a feedback-processing viewpoint, where limb position is defined by minimizing positioning error indicated by feedback. The evidence suggests that the role of phasing in motor programs may be different for unidirectional actions on the one band and multi-directional and/or multi-component actions on the other.     

Effect of distorted visual feedback on the sense of agency

It has been hypothesized that an internal model is involved in controlling and recognizing one's own actions (action attribution). This results from a comparison process between the predicted sensory feedback of the action and its real sensory consequences. The aim of the present study is to distinguish the respective importance of two action parameters (time and direction) on such an attribution judgment. We used a device that allows introduction of discordance between the movements actually performed and the sensory feedback displayed on a computer screen. Participants were asked to judge whether they were viewing 1) their own movements, 2) their own movements modified (spatially or temporally displaced), or 3) those of another agent (i.e, the experimenter). In fact, in all conditions they were only shown their own movements either unaltered or modified by varying amounts in space or time. Movements were only attributed to another agent when there was a high spatial discordance between participants' hand movements and sensory feedback. This study is the first to show that the direction of movements is a cardinal feature in action attribution, whereas temporal properties of movements play a less important role.     

Thresholds of Illumination for the Visual Discrimination of Direction of Movement and for the Discrimination of Discreteness

Currently, relatively little is known about what drives the choice of limb for goal-oriented reaching. Traditionally, the explanation has been tied predominately to motor dominance as manifested in handedness. This article offers data and an argument suggesting that handedness can be modified by attentional (spatial) information. Although motor dominance may be the controlling factor in the programming and execution of reaching movements at the midline and hemispace ipsilateral (same side) to the dominant limb, attentional information alters the programming of movements in what would be contralateral space. The general trend of behavior is characterized by reaching on the same side as the stimulus, in ipsilateral fashion, a phenomenon explained by kinesthetic efficiency and hemispheric bias.     

Comparison of grasping movements made by healthy subjects in a 3-dimensional immersive virtual versus physical environment

Virtual reality (VR) technology is being used with increasing frequency as a training medium for motor rehabilitation. However, before addressing training effectiveness in virtual environments (VEs), it is necessary to identify if movements made in such environments are kinematically similar to those made in physical environments (PEs) and the effect of provision of haptic feedback on these movement patterns. These questions are important since reach-to-grasp movements may be inaccurate when visual or haptic feedback is altered or absent. Our goal was to compare kinematics of reaching and grasping movements to three objects performed in an immersive three-dimensional (3D) VE with haptic feedback (cyberglove/grasp system) viewed through a head-mounted display to those made in an equivalent physical environment (PE). We also compared movements in PE made with and without wearing the cyberglove/grasp haptic feedback system. Ten healthy subjects (8 women, 62.1 ± 8.8 years) reached and grasped objects requiring 3 different grasp types (can, diameter 65.6 mm, cylindrical grasp; screwdriver, diameter 31.6 mm, power grasp; pen, diameter 7.5 mm, precision grasp) in PE and visually similar virtual objects in VE. Temporal and spatial arm and trunk kinematics were analyzed. Movements were slower and grip apertures were wider when wearing the glove in both the PE and the VE compared to movements made in the PE without the glove. When wearing the glove, subjects used similar reaching trajectories in both environments, preserved the coordination between reaching and grasping and scaled grip aperture to object size for the larger object (cylindrical grasp). However, in VE compared to PE, movements were slower and had longer deceleration times, elbow extension was greater when reaching to the smallest object and apertures were wider for the power and precision grip tasks. Overall, the differences in spatial and temporal kinematics of movements between environments were greater than those due only to wearing the cyberglove/grasp system. Differences in movement kinematics due to the viewing environment were likely due to a lack of prior experience with the virtual environment, an uncertainty of object location and the restricted field-of-view when wearing the head-mounted display. The results can be used to inform the design and disposition of objects within 3D VEs for the study of the control of prehension and for upper limb rehabilitation.     

What determines choice of limb for unimanual reaching movements?

Currently, relatively little is known about what drives the choice of limb for goal-oriented reaching. Traditionally, the explanation has been tied predominately to motor dominance as manifested in handedness. This article offers data and an argument suggesting that handedness can be modified by attentional (spatial) information. Although motor dominance may be the controlling factor in the programming and execution of reaching movements at the midline and hemispace ipsilateral (same side) to the dominant limb, attentional information alters the programming of movements in what would be contralateral space. The general trend of behavior is characterized by reaching on the same side as the stimulus, in ipsilateral fashion, a phenomenon explained by kinesthetic efficiency and hemispheric bias.     

Generalization as a behavioral window to the neural mechanisms of learning internal models

In generating motor commands, the brain seems to rely on internal models that predict physical dynamics of the limb and the external world. How does the brain compute an internal model? Which neural structures are involved? We consider a task where a force field is applied to the hand, altering the physical dynamics of reaching. Behavioral measures suggest that as the brain adapts to the field, it maps desired sensory states of the arm into estimates of force. If this neural computation is performed via a population code, i.e., via a set of bases, then activity fields of the bases dictate a generalization function that uses errors experienced in a given state to influence performance in any other state. The patterns of generalization suggest that the bases have activity fields that are directionally tuned, but directional tuning may be bimodal. Limb positions as well as contextual cues multiplicatively modulate the gain of tuning. These properties are consistent with the activity fields of cells in the motor cortex and the cerebellum. We suggest that activity fields of cells in these motor regions dictate the way we represent internal models of limb dynamics.     

Are there age-related differences in learning to optimize speed, accuracy, and energy expenditure?

Studies of age-related differences in manual aiming have indicated that older adults take longer to complete their movements than their younger counterparts because they tend to rely on time-consuming feedback-based control processes. Many authors have suggested that the reliance on feedback is the result of a "play-it-safe" strategy that has been adopted to compensate for a deterioration in accurate and consistent force generation. That is, perhaps because older adults know that their motor systems are not as reliable as the systems were at a younger age, they plan shorter movements that conserve time and space for feedback control to correct their programmed actions. The vast majority of the previous studies that have revealed these age-related differences in aiming, however, have used computer-based tasks that involve the transformation of perceptual into motor space. In the present experiment, older and younger adults completed real aiming movements over three sessions. The results suggest that, when acting in a real environment, the main difference between older and younger adults in movement execution lies in the efficient use of response-related feedback, not in the programming of movement.     

Feedback and intention during motor-skill learning: a connection with prospective memory

The intention to complete an action in the future can improve the learning of this action, but it is unknown whether this effect persists when feedback is manipulated during encoding. In Experiment 1, participants were instructed to learn a motor skill with or without intending to reproduce this learning in the future, and feedback on their movements was administrated by self-decision, that is, participants asked for feedback whenever they wanted it. The results showed that intention increased the frequency with which feedback was requested, but did not improve motor performance. In Experiment 2, participants had to learn the task with high or few feedbacks, which they could not control. In these conditions, intention was beneficial in promoting motor learning only for a low feedback schedule. We suggest that the beneficial effect of intention on learning can be overshadowed or emphasised by the feedback processing during encoding. These findings are discussed in light of theories surrounding prospective memory.     

Human supplementary motor area contribution to predictive motor planning

The supplementary motor area (SMA) is involved in planning limb movements. An important component of such planning is the prediction of the sensory consequences of action. The authors used transcranial magnetic stimulation (TMS) to probe the contribution of SMA to motor planning during a predictive load-bearing task. Single TMS pulses were delivered over the SMA after a cue instructing the participant to release a platform supporting his or her right hand, which in turn held a 2 kg mass. Participants were less able to bear the load successfully when TMS was delivered 400-500 ms prior to the response. This result suggests that the SMA contributes to the prediction of the sensory consequences of movement well before movement onset.