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.

Near optimal combination of sensory and motor uncertainty in time during a naturalistic perception-action task.

Most behavioral tasks have time constraints for successful completion, such as catching a ball in flight. Many of these tasks require trading off the time allocated to perception and action, especially when only one of the two is possible at any time. In general, the longer we perceive, the smaller the uncertainty in perceptual estimates. However, a longer perception phase leaves less time for action, which results in less precise movements. Here we examine subjects catching a virtual ball. Critically, as soon as subjects began to move, the ball became invisible. We study how subjects trade-off sensory and movement uncertainty by deciding when to initiate their actions. We formulate this task in a probabilistic framework and show that subjects' decisions when to start moving are statistically near optimal given their individual sensory and motor uncertainties. Moreover, we accurately predict individual subject's task performance. Thus we show that subjects in a natural task are quantitatively aware of how sensory and motor variability depend on time and act so as to minimize overall task variability.

Separate representations of dynamics in rhythmic and discrete movements: evidence from motor learning.

Rhythmic and discrete arm movements occur ubiquitously in everyday life, and there is a debate as to whether these two classes of movements arise from the same or different underlying neural mechanisms. Here we examine interference in a motor-learning paradigm to test whether rhythmic and discrete movements employ at least partially separate neural representations. Subjects were required to make circular movements of their right hand while they were exposed to a velocity-dependent force field that perturbed the circularity of the movement path. The direction of the force-field perturbation reversed at the end of each block of 20 revolutions. When subjects made only rhythmic or only discrete circular movements, interference was observed when switching between the two opposing force fields. However, when subjects alternated between blocks of rhythmic and discrete movements, such that each was uniquely associated with one of the perturbation directions, interference was significantly reduced. Only in this case did subjects learn to corepresent the two opposing perturbations, suggesting that different neural resources were employed for the two movement types. Our results provide further evidence that rhythmic and discrete movements employ at least partially separate control mechanisms in the motor system.

Nash equilibria in multi-agent motor interactions.

Social interactions in classic cognitive games like the ultimatum game or the prisoner's dilemma typically lead to Nash equilibria when multiple competitive decision makers with perfect knowledge select optimal strategies. However, in evolutionary game theory it has been shown that Nash equilibria can also arise as attractors in dynamical systems that can describe, for example, the population dynamics of microorganisms. Similar to such evolutionary dynamics, we find that Nash equilibria arise naturally in motor interactions in which players vie for control and try to minimize effort. When confronted with sensorimotor interaction tasks that correspond to the classical prisoner's dilemma and the rope-pulling game, two-player motor interactions led predominantly to Nash solutions. In contrast, when a single player took both roles, playing the sensorimotor game bimanually, cooperative solutions were found. Our methodology opens up a new avenue for the study of human motor interactions within a game theoretic framework, suggesting that the coupling of motor systems can lead to game theoretic solutions.

Motor learning.

Although learning a motor skill, such as a tennis stroke, feels like a unitary experience, researchers who study motor control and learning break the processes involved into a number of interacting components. These components can be organized into four main groups. First, skilled performance requires the effective and efficient gathering of sensory information, such as deciding where and when to direct one's gaze around the court, and thus an important component of skill acquisition involves learning how best to extract task-relevant information. Second, the performer must learn key features of the task such as the geometry and mechanics of the tennis racket and ball, the properties of the court surface, and how the wind affects the ball's flight. Third, the player needs to set up different classes of control that include predictive and reactive control mechanisms that generate appropriate motor commands to achieve the task goals, as well as compliance control that specifies, for example, the stiffness with which the arm holds the racket. Finally, the successful performer can learn higher-level skills such as anticipating and countering the opponent's strategy and making effective decisions about shot selection. In this Primer we shall consider these components of motor learning using as an example how we learn to play tennis.

Context-dependent partitioning of motor learning in bimanual movements.

Human subjects easily adapt to single dynamic or visuomotor perturbations. In contrast, when two opposing dynamic or visuomotor perturbations are presented sequentially, interference is often observed. We examined the effect of bimanual movement context on interference between opposing perturbations using pairs of contexts, in which the relative direction of movement between the two arms was different across the pair. When each perturbation direction was associated with a different bimanual context, such as movement of the arms in the same direction versus movement in the opposite direction, interference was dramatically reduced. This occurred over a short period of training and was seen for both dynamic and visuomotor perturbations, suggesting a partitioning of motor learning for the different bimanual contexts. Further support for this was found in a series of transfer experiments. Having learned a single dynamic or visuomotor perturbation in one bimanual context, subjects showed incomplete transfer of this learning when the context changed, even though the perturbation remained the same. In addition, we examined a bimanual context in which one arm was moved passively and show that the reduction in interference requires active movement. The sensory consequences of movement are thus insufficient to allow opposing perturbations to be co-represented. Our results suggest different bimanual movement contexts engage at least partially separate representations of dynamics and kinematics in the motor system.

Statistics of natural movements are reflected in motor errors.

Humans use their arms to engage in a wide variety of motor tasks during everyday life. However, little is known about the statistics of these natural arm movements. Studies of the sensory system have shown that the statistics of sensory inputs are key to determining sensory processing. We hypothesized that the statistics of natural everyday movements may, in a similar way, influence motor performance as measured in laboratory-based tasks. We developed a portable motion-tracking system that could be worn by subjects as they went about their daily routine outside of a laboratory setting. We found that the well-documented symmetry bias is reflected in the relative incidence of movements made during everyday tasks. Specifically, symmetric and antisymmetric movements are predominant at low frequencies, whereas only symmetric movements are predominant at high frequencies. Moreover, the statistics of natural movements, that is, their relative incidence, correlated with subjects' performance on a laboratory-based phase-tracking task. These results provide a link between natural movement statistics and motor performance and confirm that the symmetry bias documented in laboratory studies is a natural feature of human movement.

Motor coordination: when two have to act as one.

Trying to pass someone walking toward you in a narrow corridor is a familiar example of a two-person motor game that requires coordination. In this study, we investigate coordination in sensorimotor tasks that correspond to classic coordination games with multiple Nash equilibria, such as "choosing sides," "stag hunt," "chicken," and "battle of sexes". In these tasks, subjects made reaching movements reflecting their continuously evolving "decisions" while they received a continuous payoff in the form of a resistive force counteracting their movements. Successful coordination required two subjects to "choose" the same Nash equilibrium in this force-payoff landscape within a single reach. We found that on the majority of trials coordination was achieved. Compared to the proportion of trials in which miscoordination occurred, successful coordination was characterized by several distinct features: an increased mutual information between the players' movement endpoints, an increased joint entropy during the movements, and by differences in the timing of the players' responses. Moreover, we found that the probability of successful coordination depends on the players' initial distance from the Nash equilibria. Our results suggest that two-person coordination arises naturally in motor interactions and is facilitated by favorable initial positions, stereotypical motor pattern, and differences in response times.

Computational approaches to motor control.

This review will focus on four areas of motor control which have recently been enriched both by neural network and control system models: motor planning, motor prediction, state estimation and motor learning. We will review the computational foundations of each of these concepts and present specific models which have been tested by psychophysical experiments. We will cover the topics of optimal control for motor planning, forward models for motor prediction, observer models of state estimation arid modular decomposition in motor learning. The aim of this review is to demonstrate how computational approaches, as well as proposing specific models, provide a theoretical framework to formalize the issues in motor control.

Risk sensitivity in a motor task with speed-accuracy trade-off.

When a racing driver steers a car around a sharp bend, there is a trade-off between speed and accuracy, in that high speed can lead to a skid whereas a low speed increases lap time, both of which can adversely affect the driver's payoff function. While speed-accuracy trade-offs have been studied extensively, their susceptibility to risk sensitivity is much less understood, since most theories of motor control are risk neutral with respect to payoff, i.e., they only consider mean payoffs and ignore payoff variability. Here we investigate how individual risk attitudes impact a motor task that involves such a speed-accuracy trade-off. We designed an experiment where a target had to be hit and the reward (given in points) increased as a function of both subjects' endpoint accuracy and endpoint velocity. As faster movements lead to poorer endpoint accuracy, the variance of the reward increased for higher velocities. We tested subjects on two reward conditions that had the same mean reward but differed in the variance of the reward. A risk-neutral account predicts that subjects should only maximize the mean reward and hence perform identically in the two conditions. In contrast, we found that some (risk-averse) subjects chose to move with lower velocities and other (risk-seeking) subjects with higher velocities in the condition with higher reward variance (risk). This behavior is suboptimal with regard to maximizing the mean number of points but is in accordance with a risk-sensitive account of movement selection. Our study suggests that individual risk sensitivity is an important factor in motor tasks with speed-accuracy trade-offs.

Learning optimal adaptation strategies in unpredictable motor tasks.

Picking up an empty milk carton that we believe to be full is a familiar example of adaptive control, because the adaptation process of estimating the carton's weight must proceed simultaneously with the control process of moving the carton to a desired location. Here we show that the motor system initially generates highly variable behavior in such unpredictable tasks but eventually converges to stereotyped patterns of adaptive responses predicted by a simple optimality principle. These results suggest that adaptation can become specifically tuned to identify task-specific parameters in an optimal manner.