Motor prediction.
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Central Nervous System↗
Biomedical subjects
D M Wolpert
Publications and source records attributed to D M Wolpert.
The cerebellum is involved in predicting the sensory consequences of action.
We used H2(15)O PET to examine neural responses to parametrically varied degrees of discrepancy between the predicted and actual sensory consequences of movement. Subjects used their right hand to move a robotic arm. The motion of this robotic arm determined the position of a second foam-tipped robotic arm, which made contact with the subject's left palm. Using this robotic interface, computer controlled delays were introduced between the movement of the right hand and the tactile stimulation on the left. Activity in the right lateral cerebellar cortex showed a positive correlation with delay. These results suggest the cerebellum is involved in signalling the sensory discrepancy between the predicted and actual sensory consequences of movements.
Adult↗
The influence of previous experience on predictive motor control.
Anticipating the consequences of our motor commands is a fundamental component of sensorimotor control. For example, when one hand pulls on an object held in the other, the restraining hand generates an anticipatory increase in grip force thereby preventing the object from slipping. To investigate how such anticipation is learned subjects held an object, whose properties were under computer control, between their hands. This allowed instant changes in the behaviour of the manipulated object on a trial by trial basis. The extent of grip force modulation seen in one hand, when the other pulled on the object was found to depend in a systematic way on the object's properties experienced over at least the previous three trials.
Adult↗
Sensorimotor prediction and memory in object manipulation.
When people lift objects of different size but equal weight, they initially employ too much force for the large object and too little force for the small object. However, over repeated lifts of the two objects, they learn to suppress the size-weight association used to estimate force requirements and appropriately scale their lifting forces to the true and equal weights of the objects. Thus, sensorimotor memory from previous lifts comes to dominate visual size information in terms of force prediction. Here we ask whether this sensorimotor memory is transient, preserved only long enough to perform the task, or more stable. After completing an initial lift series in which they lifted equally weighted large and small objects in alternation, participants then repeated the lift series after delays of 15 minutes or 24 hours. In both cases, participants retained information about the weights of the objects and used this information to predict the appropriate fingertip forces. This preserved sensorimotor memory suggests that participants acquired internal models of the size-weight stimuli that could be used for later prediction.
Adolescent↗
Sensorimotor integration compensates for visual localization errors during smooth pursuit eye movements.
To localize a seen object, the CNS has to integrate the object's retinal location with the direction of gaze. Here we investigate this process by examining the localization of static objects during smooth pursuit eye movements. The normally experienced stability of the visual world during smooth pursuit suggests that the CNS essentially compensates for the eye movement when judging target locations. However, certain systematic localization errors are made, and we use these to study the process of sensorimotor integration. During an eye movement, a static object's image moves across the retina. Objects that produce retinal slip are known to be mislocalized: objects moving toward the fovea are seen too far on in their trajectory, whereas errors are much smaller for objects moving away from the fovea. These effects are usually studied by localizing the moving object relative to a briefly flashed one during fixation: moving objects are then mislocalized, but flashes are not. In our first experiment, we found that a similar differential mislocalization occurs for static objects relative to flashes during pursuit. This effect is not specific for horizontal pursuit but was also found in other directions. In a second experiment, we examined how this effect generalizes to positions outside the line of eye movement. We found that large localization errors were found in the entire hemifield ahead of the pursuit target and were predominantly aligned with the direction of eye movement. In a third experiment, we determined whether it is the flash or the static object that is mislocalized ahead of the pursuit target. In contrast to fixation conditions, we found that during pursuit it is the flash, not the static object, which is mislocalized. In a fourth experiment, we used egocentric localization to confirm this result. Our results suggest that the CNS compensates for the retinal localization errors to maintain position constancy for static objects during pursuit. This compensation is achieved in the process of sensorimotor integration of retinal and gaze signals: different retinal areas are integrated with different gaze signals to guarantee the stability of the visual world.
Brain↗
Mosaic model for sensorimotor learning and control.
Humans demonstrate a remarkable ability to generate accurate and appropriate motor behavior under many different and often uncertain environmental conditions. We previously proposed a new modular architecture, the modular selection and identification for control (MOSAIC) model, for motor learning and control based on multiple pairs of forward (predictor) and inverse (controller) models. The architecture simultaneously learns the multiple inverse models necessary for control as well as how to select the set of inverse models appropriate for a given environment. It combines both feedforward and feedback sensorimotor information so that the controllers can be selected both prior to movement and subsequently during movement. This article extends and evaluates the MOSAIC architecture in the following respects. The learning in the architecture was implemented by both the original gradient-descent method and the expectation-maximization (EM) algorithm. Unlike gradient descent, the newly derived EM algorithm is robust to the initial starting conditions and learning parameters. Second, simulations of an object manipulation task prove that the architecture can learn to manipulate multiple objects and switch between them appropriately. Moreover, after learning, the model shows generalization to novel objects whose dynamics lie within the polyhedra of already learned dynamics. Finally, when each of the dynamics is associated with a particular object shape, the model is able to select the appropriate controller before movement execution. When presented with a novel shape-dynamic pairing, inappropriate activation of modules is observed followed by on-line correction.
Brain↗
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.
Agnosia↗
The CNS updates its context estimate in the absence of feedback.
Human motor behaviour is remarkably accurate and appropriate even though our bodies and the objects we interact with change over time. To achieve such performance the motor system has to tailor the motor commands to the current context, that is the properties of objects in the world and the prevailing environmental conditions. The current context can be estimated by integrating two sources of information, sensory feedback and knowledge about how the context is likely to have changed from the previous estimate. Here we show that in the absence of sensory feedback about the context the second process is able to extrapolate the likely evolution of the context without requiring awareness that the context is changing.
Adult↗
Explaining the symptoms of schizophrenia: abnormalities in the awareness of action.
We propose that the primary cognitive deficit associated with delusions of control is a lack of awareness of certain aspects of motor control. This problem arises because of a failure in the mechanism by which the predicted consequences of an action are derived from a forward model based on the intended sequence of motor commands. This problem leads to a number of behavioural consequences, such as a lack of central error correction, many of which have been observed in patients with delusions of control and related symptoms. At the physiological level, delusions of control are associated with over-activity in parietal cortex. We suggest that this over-activity results from a failure to attenuate responses to sensations of limb movements even though these sensations can be anticipated on the basis of the movements intended. The lack of attenuation may arise from long range cortico-cortical disconnections which prevent inhibitory signals arising in the frontal areas which generate motor commands from reaching the appropriate sensory areas.
Awareness↗
Computational principles of movement neuroscience.
Unifying principles of movement have emerged from the computational study of motor control. We review several of these principles and show how they apply to processes such as motor planning, control, estimation, prediction and learning. Our goal is to demonstrate how specific models emerging from the computational approach provide a theoretical framework for movement neuroscience.
Animals↗
Learning and decay of prediction in object manipulation.
Anticipating the consequences of our own actions is a fundamental component of normal sensorimotor control and is seen, for example, during the manipulation of objects. When one hand pulls on an object held in the other hand, there is an anticipatory increase in grip force in the restraining hand that prevents the object from slipping. This anticipation is thought to rely on a forward internal model of the manipulated object and motor system, enabling the prediction of the consequences of our motor commands. Here we investigate the development of such a predictive response. Each hand held an object that was attached to its own torque motor. On each trial the subject was required to pull on the object held in the left hand and to maintain the position of the object held in the right hand. The torque motors were computer controlled so that the objects could be either "linked" so that the forces on the objects were equal and opposite, acting as though they were a single object, or "unlinked," so that they acted as two independent objects. A predictive response in the restraining hand is only necessary when the objects are linked and is unnecessary in the unlinked condition where there is no risk of the object slipping. To examine the learning and decay of predictive responses, we measured the grip force responses during unlinked trials that followed a linked trial. After a single linked trial, anticipatory grip force was quick to develop, but decayed slowly over the following unlinked trials. Varying the time between trials showed that the rate of decay depended on the number of trials since the last linked trial rather than time. Increasing the frequency of linked trials showed an increased level of subsequent grip force modulation, but did not alter the decay rate. When the torque motors simulated a linked object that did not have normal physical properties, prediction was reduced. These results show that the use of predictive responses has a different time course for learning and decay, and the response depends on experience and the physical properties of the objects.
Adult↗
Context estimation for sensorimotor control.
Human motor behavior is remarkably accurate and appropriate even though the properties of our own bodies as well as the objects we interact with vary over time. To adjust appropriately, the motor system has to estimate the context, that is the properties of objects in the world and the prevailing environmental conditions. Here we show that to determine the current context the CNS uses information from both prior knowledge of how the context might evolve over time and from the comparison of predicted and actual sensory feedback. We show that these two sources of information may be modeled within the CNS and combined to derive an accurate estimate of the context which adjusts motor command selection. This provides a novel probabilistic framework for sensorimotor control.
Adaptation, Physiological↗
Multiple single unit recording in the cortex of monkeys using independently moveable microelectrodes.
Simultaneous recording from multiple single neurones presents many technical difficulties. However, obtaining such data has many advantages, which make it highly worthwhile to overcome the technical problems. This report describes methods which we have developed to permit recordings in awake behaving monkeys using the 'Eckhorn' 16 electrode microdrive. Structural magnetic resonance images are collected to guide electrode placement. Head fixation is achieved using a specially designed headpiece, modified for the multiple electrode approach, and access to the cortex is provided via a novel recording chamber. Growth of scar tissue over the exposed dura mater is reduced using an anti-mitotic compound. Control of the microdrive is achieved by a computerised system which permits several experimenters to move different electrodes simultaneously, considerably reducing the load on an individual operator. Neurones are identified as pyramidal tract neurones by antidromic stimulation through chronically implanted electrodes; stimulus control is integrated into the computerised system. Finally, analysis of multiple single unit recordings requires accurate methods to correct for non-stationarity in unit firing. A novel technique for such correction is discussed.
Animals↗
The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation.
We used fMRI to examine neural responses when subjects experienced a tactile stimulus that was either self-produced or externally produced. The somatosensory cortex showed increased levels of activity when the stimulus was externally produced. In the cerebellum there was less activity associated with a movement that generated a tactile stimulus than with a movement that did not. This difference suggests that the cerebellum is involved in predicting the specific sensory consequences of movements and providing the signal that is used to attenuate the sensory response to self-generated stimulation. In this paper, we use regression analyses to test this hypothesis explicitly. Specifically, we predicted that activity in the cerebellum contributes to the decrease in somatosensory cortex activity during self-produced tactile stimulation. Evidence in favor of this hypothesis was obtained by demonstrating that activity in the thalamus and primary and secondary somatosensory cortices significantly regressed on activity in the cerebellum when tactile stimuli were self-produced but not when they were externally produced. This supports the proposal that the cerebellum is involved in predicting the sensory consequences of movements. In the present study, this prediction is accurate when tactile stimuli are self-produced relative to when they are externally produced, and is therefore used to attenuate the somatosensory response to the former type of tactile stimulation but not the latter.
Adult↗
The effect of visuomotor displacements on arm movement paths.
The gently curved paths evident in point-to-point arm movements have been attributed to both an imperfect execution of a planned straight-hand path or as an emergent property of a control strategy in which an intrinsic cost, dependent on arm dynamics, is minimised. We used a virtual visual feedback system to test whether path curvature was mainly determined by the visually perceived or actual location of the moving limb. Hand paths were measured for movements between three pairs of targets under both veridical and uniformly translated visual feedback. This allowed us to decouple the actual and perceived hand location during movement. Under different conditions of visual feedback the curvature of the hand paths did not correlate with either the visually perceived location of the limb or the actual location but rather with the relative displacement between the actual and visually perceived limb locations. The results are consistent with the hypothesis that in planning a movement the internal estimate of intrinsic coordinates, such as joint angles, is at least partially derived from visual information.
Adolescent↗
Evidence for an eye-centered spherical representation of the visuomotor map.
During visually guided movement, visual coordinates of target location must be transformed into coordinates appropriate for movement. To investigate the representation of this visuomotor coordinate transformation, we examined changes in pointing behavior induced by a local visuomotor remapping. The visual feedback of finger position was limited to one location within the workspace, at which a discrepancy was introduced between the actual and visually perceived finger position. This remapping induced a change in pointing that extended over the entire workspace and was best captured by a spherical coordinate system centered near the eyes.
Adult↗
Predictive motor learning of temporal delays.
Anticipatory responses can minimize the disturbances that result from the action of one part of the body on another. Such a predictive response is evident in the anticipatory increase in grip force seen when one hand pulls on an object held in the other hand, thereby preventing the object from slipping. It is postulated that such a response depends on predicting the consequences of the descending motor command, as signaled by efference copy, using an internal model of both one's own body and the object. Here we investigate how the internal model learns the temporal consequences of the motor command. We employed two robots to simulate a virtual object held in one hand and acted on by the other. Delays were introduced between the action of one hand on the object and the effects of this action on the other hand. An initial reactive grip force response to the delayed load decayed with the development of appropriate anticipatory grip force modulation. However, no predictive modulation was seen when the object's movement was not generated by the subject, even when the motion was cued by a tone. These results suggest that, when an internal model learns new temporal relationships between actions and their consequences, this learning involves generating a novel response rather than adapting the original predictive response.
Adult↗
Spatio-temporal prediction modulates the perception of self-produced stimuli.
We investigated why self-produced tactile stimulation is perceived as less intense than the same stimulus produced externally. A tactile stimulus on the palm of the right hand was either externally produced, by a robot or self-produced by the subject. In the conditions in which the tactile stimulus was self-produced, subjects moved the arm of a robot with their left hand to produce the tactile stimulus on their right hand via a second robot. Subjects were asked to rate intensity of the tactile sensation and consistently rated self-produced tactile stimuli as less tickly, intense, and pleasant than externally produced tactile stimuli. Using this robotic setup we were able to manipulate the correspondence between the action of the subjects' left hand and the tactile stimulus on their right hand. First, we parametrically varied the delay between the movement of the left hand and the resultant movement of the tactile stimulus on the right hand. Second, we implemented varying degrees of trajectory perturbation and varied the direction of the tactile stimulus movement as a function of the direction of left-hand movement. The tickliness rating increased significantly with increasing delay and trajectory perturbation. This suggests that self-produced movements attenuate the resultant tactile sensation and that a necessary requirement of this attenuation is that the tactile stimulus and its causal motor command correspond in time and space. We propose that the extent to which self-produced tactile sensation is attenuated (i.e., its tickliness) is proportional to the error between the sensory feedback predicted by an internal forward model of the motor system and the actual sensory feedback produced by the movement.
Adult↗