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Biomedical subjects

Daniel M Wolpert

Publications and source records attributed to Daniel M Wolpert.

At least 19 recordsLinked to original sources

Computational principles of sensorimotor control that minimize uncertainty and variability.

Sensory and motor noise limits the precision with which we can sense the world and act upon it. Recent research has begun to reveal computational principles by which the central nervous system reduces the sensory uncertainty and movement variability arising from this internal noise. Here we review the role of optimal estimation and sensory filtering in extracting the sensory information required for motor planning, and the role of optimal control, motor adaptation and impedance control in the specification of the motor output signal.

Algorithms↗

Actions and consequences in bimanual interaction are represented in different coordinate systems.

Moving one part of the body can generate interaction forces that tend to destabilize other parts of the body. However, stability is maintained by mechanisms that predict and actively oppose these interaction forces. When our body or environment changes, these anticipatory mechanisms adapt so as to continue to produce accurate predictions. In this study, we examine the acquisition of a novel predictive coordination between the arms, in a situation in which a force is produced on one hand as a consequence of the action of the other hand. Specifically, a force was applied to the left hand that depended on the velocity of the right hand. With practice, subjects learned to stabilize the perturbed left arm during right-arm movements by predicting and actively opposing the externally applied forces. After adaptation, we examined how learning generalized to a new joint configuration of the right or left arm to investigate the coordinate systems in which the internal transformation from movement to force is represented. This revealed a dissociation between the representation of the action of the right arm and the representation of its consequence, that is the force on the left arm. The movement is represented in extrinsic coordinates related to the velocity of the hand, whereas the force resulting from the movement is represented in a joint-based intrinsic coordinate system.

Adaptation, Physiological↗

Bayesian decision theory in sensorimotor control.

Action selection is a fundamental decision process for us, and depends on the state of both our body and the environment. Because signals in our sensory and motor systems are corrupted by variability or noise, the nervous system needs to estimate these states. To select an optimal action these state estimates need to be combined with knowledge of the potential costs or rewards of different action outcomes. We review recent studies that have investigated the mechanisms used by the nervous system to solve such estimation and decision problems, which show that human behaviour is close to that predicted by Bayesian Decision Theory. This theory defines optimal behaviour in a world characterized by uncertainty, and provides a coherent way of describing sensorimotor processes.

Brain↗

The main sequence of saccades optimizes speed-accuracy trade-off.

In primates, it is well known that there is a consistent relationship between the duration, peak velocity and amplitude of saccadic eye movements, known as the 'main sequence'. The reason why such a stereotyped relationship evolved is unknown. We propose that a fundamental constraint on the deployment of foveal vision lies in the motor system that is perturbed by signal-dependent noise (proportional noise) on the motor command. This noise imposes a compromise between the speed and accuracy of an eye movement. We propose that saccade trajectories have evolved to optimize a trade-off between the accuracy and duration of the movement. Taking a semi-analytical approach we use Pontryagin's minimum principle to show that there is an optimal trajectory for a given amplitude and duration; and that there is an optimal duration for a given amplitude. It follows that the peak velocity is also fixed for a given amplitude. These predictions are in good agreement with observed saccade trajectories and the main sequence. Moreover, this model predicts a small saccadic dead-zone in which it is better to stay eccentric of target than make a saccade onto target. We conclude that the main sequence has evolved as a strategy to optimize the trade-off between accuracy and speed.

Animals↗

Attenuation of self-generated tactile sensations is predictive, not postdictive.

When one finger touches the other, the resulting tactile sensation is perceived as weaker than the same stimulus externally imposed. This attenuation of sensation could result from a predictive process that subtracts the expected sensory consequences of the action, or from a postdictive process that alters the perception of sensations that are judged after the event to be self-generated. In this study we observe attenuation even when the fingers unexpectedly fail to make contact, supporting a predictive process. This predictive attenuation of self-generated sensation may have evolved to enhance the perception of sensations with an external cause.

Adolescent↗

Probabilistic mechanisms in sensorimotor control.

Uncertainty constitutes a fundamental constraint on human sensorimotor control. Our sensors are noisy and do not provide perfect information about all the properties of the world. Moreover, our muscles generate noisy outputs and many tasks we perform vary in an unpredictable way. Here we review the computations that the CNS uses in the face of such sensory, motor and task uncertainty. We show that the CNS reduces the uncertainty in estimates about the state of the world by using a Bayesian combination of prior knowledge and sensory feedback. It is shown that these mechanisms generalize to state estimation of ones own body during movement. We review how the CNS optimizes decisions based on these estimates, examining the error criterion that people optimize when performing targeted movements. Finally, we describe how signal-dependent noise on the motor output places constraints on performance. Goal-directed movement arises from a model in which the statistics of our actions are optimized. Together these studies provide a probabilistic framework for sensorimotor control.

Animals↗

Sensorimotor attenuation by central motor command signals in the absence of movement.

Voluntary actions typically produce suppression of afferent sensation from the moving body part. We used transcranial magnetic stimulation to delay the output of motor commands from the motor cortex during voluntary movement. We show attenuation of sensation during this delay, in the absence of movement. We conclude that sensory suppression mainly relies on central signals related to the preparation for movement and that these signals are upstream of primary motor cortex.

Electric Stimulation↗

Motor systems.

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Animals↗

Rhythmicity, randomness and synchrony in climbing fiber signals.

The role of the climbing fiber input to the cerebellum has been enigmatic, with recent studies focusing on its temporal and spatial firing patterns. Debate remains as to whether climbing fibers provide a periodic clock for coordinating movements or lead to long-term modification of Purkinje cell activity as the basis of motor learning. Rhythmic and synchronous activity of climbing fibers can cause movements at the same frequency in some preparations, suggesting a role in motor timing. However, in awake monkeys climbing fiber signals have been reported to occur at random, presenting a problem for clock theories. Yet synchronous patterns of discharge are consistently observed among several Purkinje cells within a narrow parasagittal longitudinal band. Here, we review recent experimental and theoretical studies and attempt to provide a coherent account of the interplay between rhythmicity, randomness and synchrony in climbing fiber activity, with a particular reference to studies in chaos.

Animals↗

Widespread access to predictive models in the motor system: a short review.

Recent behavioural and computational studies suggest that access to internal predictive models of arm and object dynamics is widespread in the sensorimotor system. Several systems, including those responsible for oculomotor and skeletomotor control, perceptual processing, postural control and mental imagery, are able to access predictions of the motion of the arm. A capacity to make and use predictions of object dynamics is similarly widespread. Here, we review recent studies looking at the predictive capacity of the central nervous system which reveal pervasive access to forward models of the environment.

Brain↗

Where does your own action influence your perception of another person's action in the brain?

Activation of premotor cortex during the observation and imitation of human actions is now increasingly accepted, but it remains unclear how the CNS is able to resolve potential conflicts between the observation of another person's action and the ongoing control of one's own action. Recent data suggest that this overlap leads to a systematic bias, where lifting a box influences participant's perceptual judgments of the weight of a box lifted by another person. We now investigate the neural basis of this bias effect using fMRI. Seventeen participants performed a perceptual weight judgment task or two control conditions while lifting a light box, a heavy box or no box during scanning. Brain regions related to perceptual bias were localized by correlating individual differences in bias with BOLD signal. Five regions were found to show correlations with psychophysical bias: left inferior frontal gyrus, left central sulcus, left extrastriate body area, left lingual gyrus and right intraparietal sulcus. The cluster in primary motor cortex was also activated by box lifting, and the cluster in extrastriate body area by the observation of hand actions and the weight judgment task. We suggest that these brain areas are part of a network where motor processing modulates perceptual judgment of observed human actions, and thus visual and motor processes cannot be thought of as two distinct systems, but instead interact at many levels.

Adolescent↗

Optimal control of redundant muscles in step-tracking wrist movements.

An important question in motor neuroscience is how the nervous system controls the spatiotemporal activation patterns of redundant muscles in generating accurate movements. The redundant muscles may not only underlie the flexibility of our movements but also pose the challenging problem of how to select a specific sequence of muscle activation from the huge number of possible activations. Here, we propose that noise in the motor command that has an influence on task achievement should be considered in determining the optimal motor commands over redundant muscles. We propose an optimal control model for step-tracking wrist movements with redundant muscles that minimizes the end-point variance under signal-dependent noise. Step-tracking wrist movements of human and nonhuman primates provide a detailed data set to investigate the control mechanisms in movements with redundant muscles. The experimental EMG data can be summarized by two eminent features: 1) amplitude-graded EMG pattern, where the timing of the activity of the agonist and antagonist bursts show slight variations with changes in movement directions, and only the amplitude of activity is modulated; and 2) cosine tuning for movement directions exhibited by the agonist and antagonist bursts, and the discrepancy found between a muscle's agonist preferred direction and its pulling direction. In addition, it is also an important observation that subjects often overshoot the target. We demonstrate that the proposed model captures not only the spatiotemporal activation patterns of wrist muscles but also trajectory overshooting. This suggests that when recruiting redundant muscles, the nervous system may optimize the motor commands across the muscles to reduce the negative effects of motor noise.

Biomechanical Phenomena↗

Perception of the consequences of self-action is temporally tuned and event driven.

It has been proposed that in order to increase the salience of sensations with an external cause, sensations that are predictable based on one's own actions are attenuated [1 and 2]. This may explain why self-imposed tickle [3 and 4] or constant forces [5] are perceived as less intense than the same stimuli externally imposed. Here, subjects used their right index finger to tap a force sensor mounted above their left index finger. When a motor generated a tap on the left finger synchronously with the right tap, simulating contact between the fingers, the perception of force in the left finger was attenuated compared to the same tap experienced during rest. Attenuation gradually reduced as the left tap was either delayed or advanced relative to the active right tap. However, no attenuation was seen to left taps triggered by right-finger movements that stopped above or passed wide of the sensor. We conclude that there is a window of sensory attenuation that is broadly temporally tuned and centered on the time at which the fingers would normally make contact. That is, predictive tactile sensory attenuation is linked to specific external events arising from movement rather than to the movement per se.

Adolescent↗

Common encoding of novel dynamic loads applied to the hand and arm.

In manual action, the relationship between a given motor command and the ensuing movement depends on the dynamics of both the arm and hand-held objects. Skilled performance relies on the brain learning both these dynamics, and previous studies have examined how people adapt to novel loads applied to either the hand or the arm. In this study, we ask whether these different kinds of load are represented independently as a result of changes in cutaneous feedback and hand-arm coordination. We used a robotic apparatus that could either apply forces to an object held in the subject's hand or directly to the segments of the arm. We tested whether subjects could retain learning of a force field applied to the hand after subsequently experiencing the opposing field applied to the arm (or vice versa), or whether retrograde interference would be observed. In separate experiments, we used force fields and torque fields that were linearly related to either hand or joint velocities, respectively. Our finding of complete interference between opposing fields suggests that loads applied to the arm and hand are not represented independently by the sensorimotor system. This interference occurred despite markedly different cutaneous inputs that were directly related to the movement task. This result suggests that the brain represents dynamics independently of these sensory inputs. In addition, we found that the rate at which subjects adapted to a given force field, specified either in hand or joint coordinates, was independent of whether the forces were applied to the hand or arm segments.

Adult↗

Interference between velocity-dependent and position-dependent force-fields indicates that tasks depending on different kinematic parameters compete for motor working memory.

Humans demonstrate motor learning when exposed to changes in the dynamics of movement or changes in the visuomotor map. However, when two opposing dynamic transformations are learned in succession, the memory of the first is overwritten by learning of the second; the same is true for two opposing visuomotor rotations. This retrograde interference is not seen for all combinations of transformations, however. When a dynamic transformation is learned subsequent to a visuomotor rotation, the presence or absence of interference appears to depend crucially on the structure of the dynamic task: a force-field dependent on the position of the hand produces interference, whereas an inertial load applied lateral to the hand does not. To explain these results, it has been hypothesized that two transformations can be learned without interference if they depend on two different kinematic parameters of movement (such as position and velocity of the hand). Here we demonstrate, contrary to this hypothesis, interference between a dynamic transformation that depends on the position of the hand and one that depends on its velocity. However, the interference was found to be incomplete, supporting the view that the ability to retain motor memories for different tasks depends on the degree to which their representations conflict in working memory.

Adaptation, Physiological↗

Activation in posterior superior temporal sulcus parallels parameter inducing the percept of animacy.

An essential, evolutionarily stable feature of brain function is the detection of animate entities, and one of the main cues to identify them is their movement. We developed a model of a simple interaction between two objects, in which an increase of the correlation between their movements varied the amount of interactivity and animacy observers attributed to them. Functional magnetic resonance imaging revealed that activation in the posterior superior temporal sulcus and gyrus (pSTS/pSTG) increased in relation to the degree of correlated motion between the two objects. This activation increase was not different when subjects performed an explicit or implicit task while observing these interacting objects. These data suggest that the pSTS and pSTG play a role in the automatic identification of animate entities, by responding directly to an objective movement characteristic inducing the percept of animacy, such as the amount of interactivity between two moving objects.

Adult↗

High-frequency repetitive transcranial magnetic stimulation over the hand area of the primary motor cortex disturbs predictive grip force scaling.

When we repetitively lift an object, our grip force is influenced by the mechanical object properties of the preceding lift, irrespective of whether the subsequent lift is performed with the same hand or the hand opposite to the preceding lift. This study investigates if repetitive high-frequency transcranial magnetic stimulation (rTMS) over the dominant primary motor cortex affects this relationship. After completion of 10 lifts of an object using the dominant hand, rTMS was applied over the dominant primary motor cortex for 20 s. On the first lift following rTMS, the peak grip force was significantly higher than on the lift preceding rTMS. Moreover, this measure remained elevated throughout the following set of lifts after rTMS. rTMS did not change the peak lift force generated by more proximal arm muscles. The same effect was observed when the lifts following rTMS over the dominant motor cortex were performed with the ipsilateral hand. These effects were not observed when subjects rested both hands on their lap or when a sham stimulation was applied for the same period of time. These preliminary data suggest that rTMS over the sensorimotor cortex disturbs predictive grip force planning.

Adult↗

Evidence for sensory prediction deficits in schizophrenia.

OBJECTIVE: Patients with schizophrenia experiencing delusions and hallucinations can misattribute their own actions to an external source. The authors test the hypothesis that patients with schizophrenia have defects in their ability to predict the sensory consequences of their actions. METHOD: The authors measured sensory attenuation of self-produced stimuli by patients with schizophrenia and by healthy subjects. RESULTS: Patients with schizophrenia demonstrated significantly less sensory attenuation than healthy subjects. CONCLUSIONS: Patients with a diagnosis of schizophrenia have a dysfunction in their predictive mechanisms.

Adult↗