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.

Retinal adaptation of visual processing time delays.

A significant proportion of the processing delays within the visual system are luminance dependent. Thus placing an attenuating filter over one eye causes a temporal delay between the eyes and thus an illusion of motion in depth for objects moving in the fronto-parallel plane, known as the Pulfrich effect. We have used this effect to study adaptation to such an interocular delay in two normal subjects wearing 75% attenuating neutral density filters over one eye. In two separate experimental periods both subjects showed about 60% adaptation over 9 days. Reciprocal effects were seen on removal of the filters. To isolate the site of adaptation we also measured the subjects' flicker fusion frequencies (FFFs) and contrast sensitivity functions (CSFs). Both subjects showed significant adaptation in their FFFs. An attempt to model the Pulfrich and FFF adaptation curves with a change in a single parameter in Kelly's [(1971) Journal of the Optical Society of America, 71, 537-546] retinal model was only partially successful. Although we have demonstrated adaptation in normal subjects to induced time delays in the visual system we postulate that this may at least partly represent retinal adaptation to the change in mean luminance.

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.

Representations of uncertainty in sensorimotor control.

Uncertainty is ubiquitous in our sensorimotor interactions, arising from factors such as sensory and motor noise and ambiguity about the environment. Setting it apart from previous theories, a quintessential property of the Bayesian framework for making inference about the state of world so as to select actions, is the requirement to represent the uncertainty associated with inferences in the form of probability distributions. In the context of sensorimotor control and learning, the Bayesian framework suggests that to respond optimally to environmental stimuli the central nervous system needs to construct estimates of the sensorimotor transformations, in the form of internal models, as well as represent the structure of the uncertainty in the inputs, outputs and in the transformations themselves. Here we review Bayesian inference and learning models that have been successful in demonstrating the sensitivity of the sensorimotor system to different forms of uncertainty as well as recent studies aimed at characterizing the representation of the uncertainty at different computational levels.

Risk-sensitivity in sensorimotor control.

Recent advances in theoretical neuroscience suggest that motor control can be considered as a continuous decision-making process in which uncertainty plays a key role. Decision-makers can be risk-sensitive with respect to this uncertainty in that they may not only consider the average payoff of an outcome, but also consider the variability of the payoffs. Although such risk-sensitivity is a well-established phenomenon in psychology and economics, it has been much less studied in motor control. In fact, leading theories of motor control, such as optimal feedback control, assume that motor behaviors can be explained as the optimization of a given expected payoff or cost. Here we review evidence that humans exhibit risk-sensitivity in their motor behaviors, thereby demonstrating sensitivity to the variability of "motor costs." Furthermore, we discuss how risk-sensitivity can be incorporated into optimal feedback control models of motor control. We conclude that risk-sensitivity is an important concept in understanding individual motor behavior under uncertainty.

Structure learning in a sensorimotor association task.

Learning is often understood as an organism's gradual acquisition of the association between a given sensory stimulus and the correct motor response. Mathematically, this corresponds to regressing a mapping between the set of observations and the set of actions. Recently, however, it has been shown both in cognitive and motor neuroscience that humans are not only able to learn particular stimulus-response mappings, but are also able to extract abstract structural invariants that facilitate generalization to novel tasks. Here we show how such structure learning can enhance facilitation in a sensorimotor association task performed by human subjects. Using regression and reinforcement learning models we show that the observed facilitation cannot be explained by these basic models of learning stimulus-response associations. We show, however, that the observed data can be explained by a hierarchical Bayesian model that performs structure learning. In line with previous results from cognitive tasks, this suggests that hierarchical Bayesian inference might provide a common framework to explain both the learning of specific stimulus-response associations and the learning of abstract structures that are shared by different task environments.

Changes of mind in decision-making.

A decision is a commitment to a proposition or plan of action based on evidence and the expected costs and benefits associated with the outcome. Progress in a variety of fields has led to a quantitative understanding of the mechanisms that evaluate evidence and reach a decision. Several formalisms propose that a representation of noisy evidence is evaluated against a criterion to produce a decision. Without additional evidence, however, these formalisms fail to explain why a decision-maker would change their mind. Here we extend a model, developed to account for both the timing and the accuracy of the initial decision, to explain subsequent changes of mind. Subjects made decisions about a noisy visual stimulus, which they indicated by moving a handle. Although they received no additional information after initiating their movement, their hand trajectories betrayed a change of mind in some trials. We propose that noisy evidence is accumulated over time until it reaches a criterion level, or bound, which determines the initial decision, and that the brain exploits information that is in the processing pipeline when the initial decision is made to subsequently either reverse or reaffirm the initial decision. The model explains both the frequency of changes of mind as well as their dependence on both task difficulty and whether the initial decision was accurate or erroneous. The theoretical and experimental findings advance the understanding of decision-making to the highly flexible and cognitive acts of vacillation and self-correction.

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.

Risk-sensitivity and the mean-variance trade-off: decision making in sensorimotor control.

Numerous psychophysical studies suggest that the sensorimotor system chooses actions that optimize the average cost associated with a movement. Recently, however, violations of this hypothesis have been reported in line with economic theories of decision-making that not only consider the mean payoff, but are also sensitive to risk, that is the variability of the payoff. Here, we examine the hypothesis that risk-sensitivity in sensorimotor control arises as a mean-variance trade-off in movement costs. We designed a motor task in which participants could choose between a sure motor action that resulted in a fixed amount of effort and a risky motor action that resulted in a variable amount of effort that could be either lower or higher than the fixed effort. By changing the mean effort of the risky action while experimentally fixing its variance, we determined indifference points at which participants chose equiprobably between the sure, fixed amount of effort option and the risky, variable effort option. Depending on whether participants accepted a variable effort with a mean that was higher, lower or equal to the fixed effort, they could be classified as risk-seeking, risk-averse or risk-neutral. Most subjects were risk-sensitive in our task consistent with a mean-variance trade-off in effort, thereby, underlining the importance of risk-sensitivity in computational models of sensorimotor control.

Multiple grasp-specific representations of tool dynamics mediate skillful manipulation.

Skillful tool use requires knowledge of the dynamic properties of tools in order to specify the mapping between applied force and tool motion. Importantly, this mapping depends on the orientation of the tool in the hand. Here we investigate the representation of dynamics during skillful manipulation of a tool that can be grasped at different orientations. We ask whether the motor system uses a single general representation of dynamics for all grasp contexts or whether it uses multiple grasp-specific representations. Using a novel robotic interface, subjects rotated a virtual tool whose orientation relative to the hand could be varied. Subjects could immediately anticipate the force direction for each orientation of the tool based on its visual geometry, and, with experience, they learned to parameterize the force magnitude. Surprisingly, this parameterization of force magnitude showed limited generalization when the orientation of the tool changed. Had subjects parameterized a single general representation, full generalization would be expected. Thus, our results suggest that object dynamics are captured by multiple representations, each of which encodes the mapping associated with a specific grasp context. We suggest that the concept of grasp-specific representations may provide a unifying framework for interpreting previous results related to dynamics learning.

Internal models in the cerebellum.

This review will focus on the possibility that the cerebellum contains an internal model or models of the motor apparatus. Inverse internal models can provide the neural command necessary to achieve some desired trajectory. First, we review the necessity of such a model and the evidence, based on the ocular following response, that inverse models are found within the cerebellar circuitry. Forward internal models predict the consequences of actions and can be used to overcome time delays associated with feedback control. Secondly, we review the evidence that the cerebellum generates predictions using such a forward model. Finally, we review a computational model that includes multiple paired forward and inverse models and show how such an arrangement can be advantageous for motor learning and control.

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.

Earthquakes, influenza and cycles of Indian kala-azar.

It is suggested that previous data indicate 3 major epidemics of kala-azar in Assam between 1875 and 1950, with inter-epidemic periods of 30-45 and 20 years. This deviates from the popular view of regular cycles with a 10-20 year period. A deterministic mathematical model of kala-azar is used to find the simplest explanation for the timing of the 3 epidemics, paying particular attention to the role of extrinsic (drugs, natural disasters, other infectious diseases) versus intrinsic (host and vector dynamics, birth and death rates, immunity) processes in provoking the second. We conclude that, whilst widespread influenza in 1918-1919 may have magnified the second epidemic, intrinsic population processes provide the simplest explanation for its timing and synchrony throughout Assam. The model also shows that the second inter-epidemic period is expected to be shorter than the first, even in the absence of extrinsic agents, and highlights the importance of a small fraction of patients becoming chronically infectious (with post kala-azar dermal leishmaniasis) after treatment during an epidemic.