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.     

The representation of predictive force control and internal forward models: evidence from lesion studies and brain imaging

Force control on the basis of prediction avoids time delays from sensory feedback during motor performance. Thus, self-produced loads arising from gravitational and inertial forces during object manipulation can be compensated for by simultaneous anticipatory changes in grip force. It has been suggested that internal forward models predict the consequences of our movements, so that grip force can be programmed in anticipation of movement-induced loads. The cerebellum has been proposed as the anatomical correlate of such internal models. Here, we present behavioural data from patients with cerebellar damage and data from brain imaging in healthy subjects further elucidating the role of the cerebellum in predictive force control. Patients with cerebellar damage exhibited clear deficits in the coupling between grip force and load. A positron-emission-tomography (PET) paradigm that separated the process of the grip force/load coupling from the isolated production of similar grip forces and loads was developed. Interaction and conjunction analyses revealed a strong activation peak in the ipsilateral posterior cerebellum particularly devoted to the predictive coupling between grip force and load. Both approaches clearly demonstrate that the cerebellum plays a major role in force prediction that cannot be compensated for by other sensorimotor structures in case of cerebellar disease. However, evidence suggests that also extra-cerebellar structures may significantly contribute to predictive force control: (1) grip force/load coupling may also be impaired after cerebral and peripheral sensorimotor lesions, (2) a coupling-related activation outside the cerebellum was observed in our PET study, and (3) the scaling of the grip force level and the dynamic grip force coupling are dissociable aspects of grip force control.     

The cerebellum and the timing of coordinated eye and hand tracking.

The cerebellum is known to have important functions in motor control, coordination, motor learning, and timing. It may have other "higher" functions as well, up to and including cognitive processing independent of motor behavior. In this article, we will review some of the evidence from functional imaging, lesion studies, electrophysiological recordings, and anatomy which support the theory that the cerebellum provides a "forward model" of the motor system. This forward model would be used for control of movement; it could also underlie a cerebellar role in coordination. In this role, the forward model would generate time-specific signals predicting the motion of each motor effector, essential for predictive control of, for example, eye and hand movements. Data are presented from human eye and hand tracking that support this. Tracking performance is better if eye and hand follow the same spatial trajectory, but better still if the eye leads the hand by about 75 to 100 ms. This suggests that information from the ocular control system feeds into the manual control system to assist its tracking.     

Cerebellar Contributions to Proactive and Reactive Control in the Stop Signal Task: A Systematic Review and Meta-Analysis of Functional Magnetic Resonance Imaging Studies

Neuropsychology Review - The cerebellum facilitates and modulates cognitive functions using forward and inverse internal models to predict and control behavior, respectively. Despite neuroimaging...     

Forward modeling allows feedback control for fast reaching movements

Delays in sensorimotor loops have led to the proposal that reaching movements are primarily under pre-programmed control and that sensory feedback loops exert an influence only at the very end of a trajectory. The present review challenges this view. Although behavioral data suggest that a motor plan is assembled prior to the onset of movement, more recent studies have indicated that this initial plan does not unfold unaltered, but is updated continuously by internal feedback loops. These loops rely on a forward model that integrates the sensory inflow and motor outflow to evaluate the consequence of the motor commands sent to a limb, such as the arm. In such a model, the probable position and velocity of an effector can be estimated with negligible delays and even predicted in advance, thus making feedback strategies possible for fast reaching movements. The parietal lobe and cerebellum appear to play a crucial role in this process. The ability of the motor system to estimate the future state of the limb might be an evolutionary substrate for mental operations that require an estimate of sequelae in the immediate future.     

Cerebellum and conditioned reflexes

The central assumption of existing models of motor learning in the cerebellum is that cerebellar mossy fibres signal information about the context in which a movement is to be performed and climbing fibres signal in relation to a movement error. This leads to changes in the responsiveness of Purkinje cells, which on the next occasion will generate a corrected output in a given context. Support for this view has come mainly from work on adaptation of the vestibulo-ocular reflex. The discovery that classically conditioned eyeblink responses depend critically on the cerebellum offers the possibility to study the learning of a novel behaviour, rather than modification of an existing reflex. After repeated pairing of a neutral stimulus, such as a tone, with a blink-eliciting stimulus, the tone will acquire the ability to elicit a blink on its own. We review evidence from studies employing a wide variety of techniques that the cerebellum is critical in this type of learning as well as evidence that mossy and climbing fibres have roles assigned to them in cerebellar learning models.     

Neural basis of motor control and its cognitive implications

It has recently been demonstrated that human subjects and nonhuman primates adapt their arm movements when subjected to complex patterns of disturbing forces. The presence of aftereffects following the removal of the disturbing forces indicates that adaptation takes place through the development of an internal model of the disturbing force. The experimental evidence described in this paper has identified some important properties of this internal model: (1) it is limited to a region surrounding that part of the space where the disturbances had been experienced; (2) there is an enhancement of the internal model that depends only on the passage of time; and (3) there is a process of consolidation of the internal model, which takes a minimum of four hours. Anatomically, the substrate of the internal model is distributed; the motor cortex, basal ganglia, and cerebellum are interconnected structures that are active to different degrees during the acquisition of motor skills. Recent investigation of the spinal cord has suggested the existence of modules that organize the motor output in a discrete set of synergies. The outputs of these modules combine by addition, and might thus form the building blocks for the internal models represented by supraspinal structures.     

Internal models for bi-manual tasks

Co-ordinated bi-manual actions form the basis for many everyday motor skills. In this review, the internal model approach to the problem of bi-manual co-ordination is presented. Bi-manual coordinative tasks are often regarded as a hallmark of complex action. They are often associated with object manipulation, whether the holding of a single object between the two hands or holding an object in each hand. However, the task of movement and control is deceptively difficult even when we execute an action with a single hand without holding an object. The simplest voluntary action requires the problems of co-ordination, timing and interaction between neural, muscular and skeletal structures to be overcome. When we are making a movement whilst holding an object, a further requirement is that an internal model is able to predict the dynamics of the object that is being held as well as the dynamics of the motor system. There has been extensive work examining the formation of internal models when acting in novel environments. The majority of studies examine uni-lateral learning of a task generally to the participant's dominant hand. However, many everyday motor tasks are bi-manual, and the existing findings regarding the learning of internal models in uni-manual tasks and their subsequent generalization highlights the complexities that must underlie the formation of bi-manual tasks. Our ability to perform bi-manual tasks raises interesting questions about how internal models are specified for co-ordinative actions, and also for how the motor system learns to represent the properties of objects.     

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.     

Updating process of internal model of action as assessed from motor and postural strategies in young adults

Internal models are constantly updated based on the actions and experiences of a person in the world. In the present study, we proposed to assess the updating process of internal models of action by providing new environmental constraints for motor planning, postural control, and execution processes in daily tasks such as STS and BTS. STS and BTS tasks were performed with different inclinations of the support surface on which the participant and the chair were positioned: horizontal support, support tilted 10° to the right, or forward. Twelve healthy adults participated in this experiment. Kinematic characteristics were recorded using an optoelectronic motion analysis system. Movement duration and trunk inclination amplitudes were analyzed for STS and BTS as well as trunk orientation and strategies of head stabilization. Concerning the movement analysis our results showed (1) temporal asymmetry between STS and BTS, attributed mainly to the integration of the mechanical effects of gravity, and (2) a decrease of trunk movements when the support was tilted forward, attesting to an immediate adaptation process. Concerning the postural analysis our study revealed that adults adopted selective head stabilization on space strategy with respect to balance constraints. To conclude, young adults were able to immediately update their internal model of action in order to optimize motor control and vertical body orientation.     

Neuroimaging studies of the cerebellum: language, learning and memory

During the decade following a functional neuroimaging study of language that showed cerebellar involvement in a cognitive task, PET and fMRI studies have continued to provide evidence that the role of the cerebellum extends beyond that of motor control and that this structure contributes in some way to cognitive operations. In this review, we describe neuroimaging evidence for cerebellar involvement in working memory, implicit and explicit learning and memory, and language, and we discuss some of the problems and limitations faced by researchers who use neuroimaging to investigate cerebellar function. We also raise a set of outstanding questions that need to be addressed through further neuroimaging and behavioral experiments before differing functional accounts of cerebellar involvement in cognition can be resolved.     

时间认知神经科学研究进展

当前对时间认知的脑机制探讨有三个模型：特异化计时模型、分布网络模型和定域计时模型。在这些模型的框架下,时间认知的神经心理学研究集中探讨了小脑、基底神经节、前额叶在时间信息加工中的作用和大脑两半球在时间认知中的不对称性。小脑作为内部计时系统对时间控制具有重要作用,在周期性动作任务中,小脑对不连续动作计时具有特异性。基底神经节在时间加工任务中与小脑存在明显的作用分离,其具体机制还有待深入研究。前额叶的计时功能可能与注意和工作记忆对时间信息的获得、维持和组织有关。此外,还发现大脑右半球与时问信息的加工关系密切。     

Muscle fatigue as an investigative tool in motor control: A review with new insights on internal models and posture–movement coordination

Muscle fatigue is a common phenomenon experienced in everyday life which affects both our force capacity and movement production. In this paper, we review works dealing with muscle fatigue and motor control and we attempt to demonstrate how the Central Nervous System deals with this particular state. We especially focus on how internal models – neural substrates which can estimate the current state as well as the future state of the body – face this internal perturbation. Moreover, we show that muscle fatigue is an interesting investigative tool in understanding the mechanisms involved in posture–movement coordination.     

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.     

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.     

The evolution of cognition—a hypothesis

Behavior may be controlled by reactive systems. In a reactive system the motor output is exclusively driven by actual sensory input. An alternative solution to control behavior is given by “cognitive” systems capable of planning ahead. To this end the system has to be equipped with some kind of internal world model. A sensible basis of an internal world model might be a model of the system's own body. I show that a reactive system with the ability to control a body of complex geometry requires only a slight reorganization to form a cognitive system. This implies that the assumption that the evolution of cognitive properties requires the introduction of new, additional modules, namely internal world models, is not justified. Rather, these modules may already have existed before the system obtained cognitive properties. Furthermore, I discuss whether the occurrence of such world models may lead to systems having internal perspective.     

Degrees of freedom and motor planning in purposive movement

This paper presents empirical evidence suggesting that healthy humans can perform a two degree of freedom visuo-motor pursuit tracking task with the same response time delay as a one degree of freedom task. In contrast, the time delay of the response is influenced markedly by the nature of the motor synergy required to produce it. We suggest a conceptual account of this evidence based on adaptive model theory, which combines theories of intermittency from psychology and adaptive optimal control from engineering. The intermittent response planning stage has a fixed period. It possesses multiple optimal trajectory generators such that multiple degrees of freedom can be planned concurrently, without requiring an increase in the planning period. In tasks which require unfamiliar motor synergies, or are deemed to be incompatible, internal adaptive models representing movement dynamics are inaccurate. This means that the actual response which is produced will deviate from the one which is planned. For a given target-response discrepancy, corrective response trajectories of longer duration are planned, consistent with the principle of speed-accuracy trade-off. Compared to familiar or compatible tasks, this results in a longer response time delay and reduced accuracy. From the standpoint of the intermittency approach, the findings of this study help make possible a more integral and predictive account of purposive action.     

A neural network model for development of reaching and pointing based on the interaction of forward and inverse transformations

Pointing is one of the communicative actions that infants acquire during their first year of life. Based on a hypothesis that early pointing is triggered by emergent reaching behavior toward objects placed at out‐of‐reach distances, we proposed a neural network model that acquires reaching without explicit representation of ‘targets’. The proposed model controls a two‐joint arm in a horizontal plane, and it learns a loop of internal forward and inverse transformations; the former predicts the visual feedback of hand position and the latter generates motor commands from the visual input through random generation of the motor commands. In the proposed model, the motor output and visual input were represented by broadly tuned neural units. Even though explicit ‘targets’ were not presented during learning, the simulation successfully generated reaching toward visually presented objects at within‐reach and out‐of‐reach distances.     

Towards a broader scope of biomechanics in developmental studies: a commentary on Jensen (2005)

In this article, we discuss where biomechanical analysis can contribute to our understanding of motor development, and more particularly in what ways biomechanics can contribute to (1) explaining the universal sequence in motor milestones; (2) explaining variations in developmental sequence between individuals; (3) understanding the impact of context on the actions of an individual; and (4) understanding, preventing, and managing chronic disabilities. In our view, biomechanics is concerned with the dynamics of the musculo‐skeletal system (MSS) and thus provides insights in the way motion is affected by the activation of muscles and the mechanical interaction between the MSS and the environment. Biomechanical analysis is important in understanding the development of actions that depend on the perceptual‐motor loop although it cannot provide a full account of the changes in the behaviour. The contributions and limitations of specific biomechanical analyses such as the inverse and forward dynamical models are discussed in the light of the article of Jensen (2005). Copyright © 2005 John Wiley & Sons, Ltd.     

Multiple systems of spatial memory and action

Recent findings from spatial cognition and cognitive neuroscience suggest that different types of mental representations could mediate the off-line retrieval of spatial relations from memory and the on-line guidance of motor actions in space. As a result, a number of models proposing multiple systems of spatial memory have been recently formulated. In the present article we review these models and we evaluate their postulates based on available experimental evidence. Furthermore, we discuss how a multiple-system model can apply to situations in which people reason about their immediate surroundings or non-immediate environments by incorporating a model of sensorimotor facilitation/interference. This model draws heavily on previous accounts of sensorimotor interference and takes into account findings from the stimulus-response compatibility literature.