A process-oriented model of human motor behavior: toward a theory-based rehabilitation approach.

Each year hundreds of thousands of new cases of damage to the nervous system are reported. A large number of people with neurological problems are in urgent need of medical or neuropsychological treatment. A therapeutic approach aimed at rehabilitation of patients with neurological (or orthopedic) problems should be based on a sound theory regarding how the brain regulates human motor behavior. Without such a theory, it is difficult to analyze the observed problems, to select the most adequate treatment procedure, and to predict its outcome. The basic role of a theory is to provide an underlying model that guides the fragmented practical ideas into a coherent treatment philosophy.

Such a theoretical basis, in general, is lacking or, when available, often does not fit with current knowledge on motor control. The regulation of human motor behavior is often seen in obsolete terms, and, in general, treatment regimens are founded primarily on empirical-clinical knowledge. In this article, a model on human motor behavior is presented that may be of importance for rehabilitation and that could play a role in the development of a theory-based rehabilitation approach.

Human Motor Control and

Learning--A Model

If you observe someone drinking coffee while he or she participates in a lively conversation, you might see him or her bending forward while extending an arm to reach for the cup, adapting finger position to the size of the cup. The person then lifts the cup carefully, brings it to the mouth, and sips the hot coffee. The person stops talking, but continues after a few seconds. The cup is held in the hand somewhere between the mouth and the table, and finally the cup is replaced on the table.

On the one hand, you observed a normal daily life scene, but, on the other hand, you observed a wonderful biological machine designed for adaptive and flexible functioning in an ever-changing context. You did not see a movement, but an action with perceptual, cognitive, and motor aspects. Each movement is always the result of such a subtle interplay among cognitive, perceptual, and motor aspects. [1-5]

Because the observable output of the nervous system is always in terms of movements, in most discussions of human motor behavior, the motor aspect is not only highly overestimated but often seen as the only relevant factor. Perception and cognition are seen as independent elements studied and discussed separately from motor aspects. It is remarkable that in most physical therapy procedures, the emphasis is almost totally on the motor system and the perceptual and cognitive aspects are ignored or treated separately. [6-9]

In this article, I argue that such an element-oriented standpoint cannot be justified and that motor behavior should be studied (and treated) as the output of an integrated and adaptive system. A model of human motor behavior is presented in which cognition, perception, and action are not separate but form the components of a flexible, functional system (Figure). The model represents a way of thinking that may be of relevance to physical therapy. This way of thinking is closely related to a cognitive view of human behavior. Nothing is really new in the model; each part of it refers to the work of others. It is based on Schmidt's [10-13] schema theory, but there are also strong influences from the work performed in the Netherlands by Hulstijn and Van Galen [14,15] and Van Galen and colleagues. [16-19] Neurobiological ideas, as discussed by Cools, [20] also play an important role.

Activation

To perform an act, an optimal level of activation is necessary. [21,22] Extreme exhaustion, coma, certain drugs, and so on lower the arousal level to such a degree that the organism is no longer able to react adequately to stimuli.

Intention

Each movement a person makes has intentional aspects; it is almost never an isolated movement or a displacement of body segments in empty space. Movements should be seen in terms of strategies for solving a problem or for reaching a goal in the environment (eg, picking up a cup of coffee). [23] An intention activates a stored repertoire of acquired abstract motor schemata. [24] The relationship between intention and action, however, is far from clear. [25]

Sensory Input Selection

The moving organism is continuously bombarded by a multitude of input (eg, visual, auditory, proprioceptive, vestibular, tactile). Not all of this information is relevant for the act under performance, and the organism has to select the most relevant information; that is, the organism must be able to pick up the essential information from the environment. [26,27] This is a crucial requirement, because when this input-selection (attentional) mechanism is damaged, th environment loses its logical structure. Indeed, when each bit of information has the same value and the same potential to trigger a reaction, the organism would quickly become overwhelmed by the input. [28] These selection processes serve to facilitate future behavioral responses and to access memory.

Stimulus Recognition and

Memory Mechanisms

The determination of the relevance of stimuli is directly related to the identification of these stimuli. It is impossible, therefore, to separate the recognition "stage" from the input-selection phase. In the example about drinking coffee, the cup has to be recognized as a graspable object and its functional significance has to be known. Its significance can only be known when there is contact with memory. Memory contact, however, is not a discrete phase; at each moment of the unfolding motor act, contact with a knowledge base is necessary.

The interplay between knowledge and motor processes is a crucial characteristic of motor behavior. The information picked up from an object has an important anticipatory function. For example, the stretch and shape of the fingers at the start of a reaching movement are determined by the functional characteristics of the object (eg, different for a telephone and a cup). [29,30] Rosenbaum et al [31] showed that, in reaching, people occasionally adopt awkward starting postures to end up in comfortable ones. He gives the following example: A waiter is reaching for a glass that has been placed upside down on a table. The waiter reached for the glass with an underhand posture, that is, with his thumb pointing down. After picking up the glass, he turned it over to fill it with water. In principle, the waiter could have reached for the glass with an overhand grip, but this would have put him in the awkward position of having to hold the glass with his thumb pointing down during the pouring operation. To avoid ending in this awkward position, the waiter initially grabbed the glass in a manner that was relatively uncomfortable. [31](pp322-323)

This example clearly indicates the subtle interaction between knowledge and movement. Its importance is true not only for complex acts, such as dancing or musical performances, but also for very simple acts, such as pushing a button or moving a lever. [32] These movements must be based on basic computations concerning the length of the arm, the place where the arm actually is, the distance to the goal, and so on. As Granit [33] argued, without such intrinsic knowledge, the movement can be performed, but is delayed and has lost its accuracy. Much of this knowledge, however, is tacit knowledge.

Response Selection

Response selection refers to one of the most fascinating aspects of human motor behavior, its flexibility. In the coffee-drinking example, there are thousands of ways to pick up the cup. The possibilities depend on the context and the momentary position of the body relative to the cup. [31] The question is, How we are able to select the most adequate movement? The classical explanation was the use of a motor program, stored in memory and containing detailed muscle-specific information for each movement. [11,34-36] The logical consequence of such an explanation, however, would be that there are as many motor programs as there are possibilities to move. Each movement would require its own motor program. The performance of novel movements is difficult to explain by means of such a motor program. Therefore, the concept of a rigid motor program has been rejected in favor of a much more abstract concept, which I will term a "programming rule," that to a large degree is similar to a schema rule as described by Schmidt [10-13] and others for motor control [37-39] as well as for cognitive skill acquisition. [2,40]

I argue that, at the level of response selection, a detailed response is not selected from the "central nervous warehouse." Instead, a programming rule, which should be seen as a very abstract and prototypical representation of the task, is selected. The programming rule contains an amodal representation of the task that is not specifically visual, acoustic, or haptic. [41] Consider, for example, a character such as the letter B. At the highest level of control, this character is represented as an amodal prototype, containing no information about its size, or about the muscles needed to write it on a sheet of paper or to etch it in the sand with your foot, or about how to copy its form while driving a car or flying an airplane, or about how to pronounce it. It is a purely abstract representation, far away from the physical act of producing it.

The following perceptual example may further clarify this concept. When you see a dog (see article by Schmidt [10]), you immediately know that it is a dog, without the necessity of retrieving from memory the images of all the dogs you ever saw. You know what a dog is because, on the basis of a rich experience with many different exemplars of this specieis, a prototypical representation has been formed. Something very similar is suggested to explain the control of movements: on the basis of numerous repetitions of a certain class of movements, a prototypical representation develops, which was termed a programming rule.

Hence, what formerly was thought to be an almost infinite set of detailed motor programs now becomes a limited set of acquired programming rules. Together, these rules form a "grammar of action," which functions as the interface between cognition and action.

Programming

Programming is the construction of ad hoc motor programs on the basis of acquired rules and the actual information available in the environment. It is argued here that programming consists of at least two processes: planning and parameter specification. Planning is operationally defined as the temporal ordering of the sequence of operations necessary to perform a required act efficiently. [42] Everyone who works with brain-damaged patients is familiar with planning errors, that is, errors against the correct ordering of an act. In functional acts, such as preparing a cup of coffee or spreading butter and marmalade on a piece of bread, it is the sequence in which the individual elements should be performed that is mixed up by the patient, whereas the individual movements themselves are performed satisfactorily. [43-45]

Parametric specification refers to the adding of context- and task-dependent information (eg, force, direction) to the motor program under construction. [16] Patients with Parkinson's disease show, among many other deficits, the inability to specify the correct force parameter. [46]

Postural Control

All movements are normally and most easily made against the background of postural stability. When a person extends an arm to reach for a cup, the arm has to be controlled, but so must other parts of the body (eg, the trunk). Before the arm can move, a large set of muscles involved in postural control must be activated. The work of Asatryan and Fel'dman, [47] Belen'kii et al, [48] and Lee [49] indicated that postural adjustments take place before movement starts. The work of Lee and colleagues [50-52] showed that visual input plays an important role in this anticipatory postural activity. Perceptual input allows postural mechanisms to be tuned to future disturbances. [53-55]

Initiation

The sequence of computational processes ends with the actual initiation of the movement.

Feedback and Feedforward 

A large set of afferent inputs inform the higher levels of the system about the state of the lower levels. Several types of feedback loops can be distinguished (here arbitrarily defined as Fb1-Fb5) that end at several levels. Fb1 informs the lower levels of the system about the selected parameter specifications, whereas Fb2 contains information concerning the sequencing of the act. Note that planning and parametric errors may occur without affecting response selection; that is, a correctly selected programming rule may result in a disordered execution because of a planning and/or parametric error. Hence, errors in response (rule) selection should be distinguished from programming errors. Fb3 informs the system about the selected response (the selected rule). Fb4 informs the system about the quality of the task performance in relation to the determined goal. When the desired goal has been obtained, the information is stored in memory to increase the existing knowledge base. Fb5 plays a role in the regulation of posture. Although the number of feedback loops is strictly arbitrary and although the presented diagram is a simplification, it is clear that in the model the total ensemble of response-produced information plays a crucial role in the regulation of movements. The continuous stream of afferent information is needed for the development and updating of the programming rules.

Regulation entirely by feedback, however, is often unsatisfactory, because the feedback operates only after faulty output has already appeared, so it compensates for disturbances that may no longer be present. [56] Therefore, the motor system also operates with a feedforward control mode. Feedforward can be defined as the sending of some signal ahead of the response in order to prepare the system for input. [13,37,38] This preparation may take the form of the introduction of a specific bias or it may just be a temporary increase in sensitivity. [38] The postural system fully exploits this sort of feedforward control. [13,47-49]

There is a close resemblance between the feedforward principle and older concepts such as corollary discharge or efference copy. [57,58] The basic idea behind these concepts is that efferent information destined for the effector mechanisms is also sent to brain areas that are primarily sensory in nature. This information alerts these areas to anticipate the arrival of the response-produced feedback. A reference of correctness is established against which the feedback of the actual movement will be compared.

Summary

Movements are the visible end result of a complex series of serial and parallel processes in which information is transformed. Motor pathology can be studied as the reflection of a disorder at one or more of the above-described processes. To understand the character of the pathology, however, it is often not sufficient to study the motor apparatus; a neuropsychological analysis of the system as an integrated (cognitive-perceptual-motor) network, uniquely linked to its environment, is required.

Motor acts are not regulated by means of muscle-specific, detailed motor programs, but are constructed on the basis of stored rules. How these rules are reacquired is the topic of the next section.

Rehabilitation Therapy as

the Reacquisition of Rules

A large part of therapy can be seen as a learning process during which patients must master new skills (eg, walking with a prosthesis or ambulating with a wheelchair) or must reacquire old skills (eg, walking or speaking). The therapist is, in essence, a designer of learning situations. Although everyone uses the word "learning," learning is an abstract concept that is difficult to define precisely. Generally, learning is seen as a set of processes associated with practice or experience and leading to a relatively stable change in behavior. [13] Hence, real learning effects should be more or less permanent and must be distinguished from performance effects, which are temporary changes of short duration attributable to increased motivation or arousal. [59,60] I have already argued that motor learning is not the learning of muscle control or movement control, but the acquisitions of programming rules that enable the subject to behave flexibly under different conditions.

The process-oriented model, as presented in this article, implicates three crucial requirements for the acquisition of programming rules: (1) the availability of adequate feedback and knowledge of results (KR), (2) variability, of practice, and (3) adequate design of the learning situation (according to the "law" of identical elements) (see works by Mulder [61] and Mulder and Hulstijn [62]). It is important to note, however, that these requirements are general requirements in that they are not necessarily of equal significance for every patient in all situations.

Feedback and Knowledge

of Results

Feedback can be roughly classified into (1) information available prior to movement (eg, position of the limb, relevant aspects of the environment), (2) information available to guide an ongoing response (knowledge of performance), and (3) information available as a result of movement. The last form of feedback has been termed "response-produced feedback," [13] or "information feedback." [63,64] This form of feedback can be further subdivided into two classes: (1) intrinsic feedback, which refers to the wide variety of information inherent to the production of a movement (ie, muscle spindle information; tendon information; joint-receptor information; auditory, tactile, and visual cues), and (2) extrinsic information, which is information provided about the task in addition to those sources of feedback that are usually perceived when a response is made. Extrinsic information (KR) can be presented verbally, mechanically, or electronically to the performer to indicate the outcome of the performance. This information can be used to represent the error in the performance as compared with some defined goal. Annett and Kay [65] have referred to KR as essential to motor learning (also see Annett's book entitled Feedback and Human Behavior), and Newell [67] viewed KR as the single most important variable governing the acquisition of skills.

Most motor tasks performed in natural settings by healthy subjects provide the performer immediately and automatically with KR. Because the patient with motor dysfunction often also has sensory and perceptual problems, he or she is totally dependent on the therapist for information concerning the outcomes of his or her attempts to perform motor tasks. This dependence is especially true during the first stages of therapy when the task is new to the patient and when the primary concern is to understand what has to be done and how. [68-70] It is during this phase that adequate and consistent feedback and KR, [70] as well as clear instructions [13] and models for observational learning, [71,72] are particularly effective and should be used with great care by therapists.

Many researchers have attempted to separate the motivational aspects of KR from the informational aspects. In general, they have concluded that KR has an informational role, a conclusion based mainly on classical learning studies such as that of Trowbridge and Cason, [73] who showed in line-drawing tasks that KR stated in quantitative terms (eg, + 2, -4) was more effective than KR stated in qualitative terms (eg, right, wrong). I argue, however, that such a dichotomy is false; motivation and information cannot be separated. [68] Indeed, the subject must be motivated to pick up the presented information (which can increase the motivation further). Against this background, the data presented by Locke [74,75] are interesting. Locke showed, in a series of visual reaction-time tasks, that the amount of information or specificity of KR did not govern performance, but rather the goals that the subjects set for themselves in relation to the information they received (see works by Jensen et al, [76] Schendel, [77] Patrick and Mutlusoy, [78] and Newell [79] for a general discussion of KR and motor learning).

There exists ample evidence for the statement that feedback and KR are of crucial importance for the learning or therapy process and that therapists should be well aware of the importance of Kr for learning. [10,13,59-70,80,81] Without adequate information, it is almost impossible to redevelop programming rules. Furthermore, although less supported by data, I argue that the positive effects of feedback and KR may be further increased by performing tasks that are inherently motivating for the patients. In general, tasks performed under everyday environmental conditions will fulfill this requirement better than the routinely used artificial (clinical) task conditions.

Variability of Practice

I have previously argued that a dog you never saw before can be immediately recognized as a dog because a prototypical representation of a dog, termed a rule, has been stored in memory. This rule can be "narrow" or "broad." A narrow rule is not very flexible; thus, only a limited number of dog types can be recognized. The following, rather bizarre, example may clarify this point. Suppose that your exprience with dogs is very limited and that during your entire life you have seen only large dogs of a certain kind (eg, German shepherds). It is plausible that this limited experience would lead to a rather narrow (representation) rule. Something like this can be observed in small children.

Although we do not know whether something similar exists in motor learning, the following analogy is intriguing. Suppose a trainee (or patient) exercises by repeating a correct response in the same context. It is tempting to suggest that the learner will acquire a task representation (rule) that is rather narrow and fully conditioned to the training context. A similar argument was made by Schmidt, [10] who predicted that the rule for a class of actions becomes broader as the motor skills acquisition or practice process becomes more variable. Variability refers to practice in a range of task conditions instead of repeating the same movements under essentially identical learning conditions.

The practical implications for rehabilitation are clear. For example, gait training (after hemiplegia or a serious orthopedic problem) would normally take place in a physical therapy department under very predictable conditions. The progress achieved under these conditions, however, often does not generalize to daily-life situations (see the works of Wilson [82] and Gouvier [83] for similar arguments).

To improve the generalization value of the therapy result, the variability of practice should be increased. The therapy should not take place solely under relatively simple and predictable conditions, but under a range of different conditions (eg, flat floor, sand or gravel walking surfaces, with and without obstacles, with and without noise, combined with secondary tasks). For a real relearning of gait, it is necessary to create a "learning landscape" in which relevant aspects of the environment can be simulated and implemented into the therapy. Furthermore, the development of home training programs should be stimulated.

Design of the Learning Situation

I have argued that separate movements play no role in the learning process and that detailed, muscle-specific combinations are not learned, but rather abstract programming rules are developed. The usefulness of these rules for daily-life activities depends to a high degree on the structure of the therapy approach. A therapy approach focused at the level of muscles and separate movements, that is, at the "repair" of distorted elements, will inevitably result in the production of narrow rules of limited value, often only applicable in a specific therapy situation. In the previous section, I have argued that the generalization value of the therapy can be improved by increasing the variability of practice. I believe variability, alone, however, is not enough. The patient should be exercised in a setting resembling real-life conditions, or even in the real would itself. In classical psychology (see article by Thorndike [84}), it was proposed that transfer of task A to task B depends on the number of identifical elements these tasks have in common. If the gap between the two tasks (situations) is too large, no transfer could be expected. After "translating" this to rehabilition, one could argue that if the gap between the clinical environment and the real world is too large, no transfer from the therapy situation to the daily-life situation can be expected. If the two situations are too different, it is plausible to suggest that what is learned in these two situations also will be different. If a therapy situation is characterized by a rather artificial and predictable learning environment in which the patient has to repeat the same movement patterns, I contend that the patient will learn these patterns, but often not more than that. The therapist is doomed to fail. Even though motor behaviors learned in the clinical setting can last even over relatively long periods, there is no guarantee that the learned motor patterns can or will be applied in other situations.

The home situationm on the other hand, is characterized by the continuous availability of KR and by a large degree of variability. It obeys the "law" of identical elements and therefore provides better conditions for learning. Indeed, the cooperation and motivation of the brain-injured person will be maximal if the tasks are inherently interesting and ecologically relevant.

Conclusions

Movement should not be seen solely in terms of motor systems but as the output of a complex integrated functional system closely linked to the environment of the organism. Clearly, no absolute separation can be made between cognitive, perceptual, and motor mechanisms. Sperry, [85] in 1952, criticized that arbitrary separation between mental and motor functions, and Trevarthen [86] wrote that visual perception and the plans for voluntary action are so intimately bound together that they may be considered products of one cerebral functions. More recently, Turvey was even more clear when he stated,

it must necessarily be the case that, like warp and woof, perception and action are interwonen and we are likely to lose perspective if we attend to one and neglect the other; for it is in the manner of their union that the properties of each are rationalized. [54](p211)

Motor control cannot be understood in terms of muscle-specific motor programs. In my view, motor learning therefore cannot be seen as the acquisition of muscle control or movement control, but as the acquisition of programming rules. The present model is of particular importance for understanding how these rules are acquired. It presents a view of motor learning and a new look at the understanding of motor disorders, namely, as the reflection of a disordered network instead of a disordered motor apparatus. The model is of less importance for the explanation of preprogrammed or "hard-wired" motor patterns (eg, walking) in healthy subjects. These motor patterns, to a large degree, are regulated by fast "hardware" mechanisms that function in direct interaction with the environmental input and do not need the slow computational "software" as described here.

Final Remarks

In this article, a model has been described that may be of value for the development of a theory-based physical therapy approach. Because cognition, perception, and action cannot be separated, physical therapy cannot be seen as a learning process directed only at the reacquisition and reorganization of movements. There is currently an urgent need for integrated theory-based therapeutical procedures aimed at the restoration of motor behabior. Only a few attempts have been made to develop such procedures (see the work of Carr et al [87] for one of the exceptions.) The present article should be seen as a modest contribution toward the development of such a theory-based treatment procedure.

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T Mulder, PdD, is Department Head, Department of Research and Development, St Maartenskliniek, PO Box 9011, 6500 GM Nijmegen the Netherlands.