DISABILITY AND REHABILITATION,

1996; VOL. 18, NO. 6, 293-299

Motor control research in rehabilitation medicine

MARK L. LATASH and JOHN J. NICHOLAS
general discussion. The primary speakers covered a wide range of topics relevant to both basic motor control research and its possible application to the problems of physical medicine and rehabilitation. Dr Tamar Flash (Israel) presented a state-of-the-art review of the current knowledge and hypotheses in the area of control of human multi-joint limb movements. She illustrated some of the basic concepts with abnormal movement patterns in patients with Parkinsons disease. Dr John Kalaska (Canada) enchanted the audience with beautiful original data on the activity of neuronal populations in the cortex of monkeys, and showed how an index of the activity of a large group of the neurons (a population vector) may be related to external kinematic characteristics of a targeted hand movement. These studies may provide an important link between the activity in a neural substrate and external movement characteristics. Such a link may eventually allow drawing a causal relation between local neurological damage (e.g. in stroke) and a motor impairment. The topic of the talk by Dr Volker Dietz (Switzerland) was postural mechanisms and their role in voluntary movements, in particular during locomotion. This topic is of a great importance for clinicians because many disabling symptoms are related to poor postural control which may prevent, in particular, ambulation, as well as execution of fast and accurate limb movements. Dr Mark Latash (USA) addressed a very basic question: What is a normal movement? His view is that without a clear answer to this question, any discussions of abnormal movements are likely to be less productive. Moreover, an understanding of what is a normal movement is crucial for the development of therapeutic strategies whose goal is to correct an abnormal movement.
What is a normal movement?

Keywords motor control, amputation, Parkinsons disease, Down syndrome. Summary Progress in rehabilitation medicine requires an understanding of the basic rules of motor coordination, as well as of the contribution of adaptive processes within the central nervous system to the patterns of impaired movements. We assume that patterns of voluntary movements reflect rules of coordination that are used by the intact central nervous system of healthy persons. In pathological conditions that may include cognitive, central neurological, and peripheral disorders, the central nervous system may reconsider these rules leading to different peripheral patterns of voluntary movements. In such conditions, changed motor patterns may be considered adaptive to a primary disorder. They may even be viewed as optimal for a given state of the system of movement production. We suggest that the emphasis of therapeutic approaches must be placed not on restoring the motor patterns to as close to normal as possible, but on assisting the central nervous system to develop optimal adaptive reactions to the original underlying pro blern.

Introduction

To improve motor function of patients with motor impairments is one of the major therapeutic goals of rehabilitation medicine. Development and optimization of therapeutic approaches, however, implies a deep understanding of the motor control mechanisms in healthy persons, as well as of the pathological changes underlying abnormal motor patterns seen in patients. Thus, basic and applied motor control research is a major requisite for progress in physical medicine and rehabilitation. This feeling was the major driving force that led to the organization of a symposium Motor Control Research in Rehabilitation Medicine that was sponsored by the National Center for Medical Rehabilitation Research (NIH) and took place on 12 April 1994 within the programme of the VII Congress of the International Rehabilitation Medicine Association (IRMA-VII) in Washington, DC. The Symposium included four talks followed by a
Correspondence 1 0 : Dr Mark Latash, Biomechanics Lab., Penn State University, University Park, PA 16802, USA.
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As already mentioned, a major goal of rehabilitation is improvement of motor function. Frequently, this is equated with bringing the movement patterns of a patient as close as possible to the movement patterns observed in healthy persons. This view is questionable. It is based on two unsubstantiated assumptions :
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patterns of voluntary movements seen in the general population are the only ones which can achieve satisfactory function; and deviations from the normal patterns reflect failure of the central nervous system (CNS) to behave correctly. These assumptions can be traced back to the deep misconception that we know more about motor control than the CNS of a patient does. Let us explain this position. We consider normal movement patterns to represent a spectrum that merges at one end with clumsiness and impaired movements or paralysis and, at the other end, with dexterous and uniquely specified movements. Clumsy children and Michael Jordan are at the opposite ends of the spectrum and provide the limits of natural motor variability. The entire spectrum is associated with basically the same rules that are used by the CNS to solve the problems of motor coordination. Let us address these rules as CNS priorities. Note that motor patterns within a segment of this spectrum may be quite different, e.g. if we compare walking of a heavyweight weightlifter and of a ballet dancer. When we move beyond these limits into an area that may be considered pathological or otherwise special, the CNS priorities may change and lead to apparently atypical motor patterns. This may happen in the absence of any apparent neurological or motor pathology, e.g. due to changes in cognition and/or decision-making (examples being movements of persons with Down syndrome or with schizophrenia). In other pathologies we may encounter morphological, biochemical, or structural CNS changes that may induce differences in motor patterns by themselves, and also by changing the CNS priorities as, for example, in Parkinsons disease and spinal cord injury. There may also be peripheral changes, as in cases of a limb amputation, which certainly limit motor patterns by themselves, but may also lead to reorganization within the CNS (taking advantage of its plasticity), and to resultant changes in CNS priorities. We think that changed CNS priorities may play an important role in defining movement patterns that look abnormal. Note that these patterns reflect control signals that have been elaborated by the CNS based on the current state of its priorities and on the state of the neural and motor structures. In this sense these movement patterns ma)! be considered optimal. The question is: Should a therapist try to change (improve) them? Motor redundancy as a source of adaptive changes First, let us emphasize the well-known redundancy of the human motor system. Typically, any motor task allows a variety of solutions. One of the most universal features of human movements is variability. Attempts at performing the same movement several times always lead to different trajectories in individual joints. This is true even for highly automated movements like hammering by a blacksmith. This variability is a reflection of the fact that the number of control variables accessible for the CNS is higher than the number of parameters that define the task. So, the CNS is always confronted with a problem of choice : Which combinations of control parameters should be chosen in order to fit the task requirements? This problem was originally formulated by Nicholai Bernstein.. In order to solve it, the CNS needs to impose additional constraints upon the neuromotor system. Apparently, it is able to make such a choice based on criteria and considerations that are unknown to us at this time. A few attempts at deciphering these CNS priorities have been made. Most frequently, researchers have tried to guess at the CNSs internal solutions by investigating the consequences of optimizing certain functions of performance related to movement kinematics, dynamics, energy expenditure, and a number of psychophysiological functions (for reviews see refs 3-5). The existence of choice (theoretically, at least) suggests that the CNS may wish to reconsider its priorities in certain situations wherein the components of the system for movement production are grossly changed. A change in the priorities may lead to a corresponding change in the externally observed patterns of voluntary movements. For example, pole-vaulting is apparently not a coordinative pattern the CNS prefers to use for jumping on an everyday basis. But, in the artificial conditions of track-and-field competition, when there are no unexpected changes in the external force field, no hidden obstacles, and there is just one priority (to clear the bar at the greatest height possible), the CNS may be persuaded to use a new, quite unusual pattern of coordination. Consider now the system of motor control of a chronically impaired or otherwise atypical person. His/her lifetime experience is filled with everyday voluntary movements in conditions of frequently changing goals and external forces. If the differences between this person and an average control subject are large enough, there is a fair chance that his/her CNS will reconsider its priorities and elaborate atypical movement patterns for solving everyday motor tasks. This does not

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necessarily mean that the system cannot perform within the normally observed variability of motor patterns. It may be able to demonstrate 'normal' patterns, but prefers to behave differently. We certainly do not wish to claim that changed coordinative rules are the only important factor defining abnormal motor patterns. An impaired system may well be genuinely unable to generate movements seen in the general population ; amputation and complete spinal cord injury being probably the most obvious examples. However, we would like to draw attention to changes in movement patterns that are not forced upon the system by a major chronic impairment but instead result from a person's reaction to a primary disorder. We postulate that, for any apparently abnormal motor pattern, the first question to be asked is: What does the CNS perceive to be its primary goals during the execution o aparticular motor task? A straightforward answer, e.g. f to follow the exact instruction within a given task setting, may be true for motivated, unimpaired subjects, although, even in such subjects, considerations such as minimizing discomfort, or making sure that the experimental set-up does not break, may be as important as optimizing the performance. Other, frequently ignored components of a motor task that may be considered important by the CNS are, for example, those related to maintaining gaze fixation, equilibrium of the head and body, and posture of the limbs with respect to the trunk during the required movements. Voluntary limb movements are nearly always associated with changes in activity of postural (for a review see ref. 9). Some of these changes occur prior to the movement and can be described as anticipatory. Their assumed role is to minimize perturbation of the limb or body posture that would otherwise be induced by the movement. The inability of some of the impaired persons to properly modulate these anticipatory postural corrections may force them to alter the primary movement patterns as well, e.g. to slow down. Such slowing-down could be regarded as a deliberate (although not necessarily consciously perceived) strategy of the CNS, and should be considered adaptive to a primary deficit in anticipatory pre-programming.

and neurophysiological relations developed during lifetime. There is evidence, however, that the consequences of leg amputation may involve a major reorganization of both afferent and efferent projections that by themselves may contribute to the difference of the motor patterns from those seen in unimpaired persons. In particular, somatosensory cortical representations (area 3b) in monkeys have been shown to change after a specific training of one hand,'O." and after digit amputation or fusion.1o, 2 Neurological reorganization of descending l control signals after a below-knee amputation in humans was studied with transcranial magnetic ~timu1ation.l~ In this study, stimuli at optimal positions of the coil recruited a larger percentage of a-motoneurons controlling the muscles in the residual leg. These muscles could also be activated from larger areas of the scalp than the muscles at the intact side. Similar results, also in human subjects, have been reported after upper limb amp~tation.'~ We have recently performed a pilot study of the anticipatory reactions in patients with a unilateral belowknee amputation who were able to stand unassisted with the prosthesis. Healthy persons use anticipatory changes in the activity of virtually all the major leg muscles in preparation to a fast arm movement, e.g. a fast bilateral shoulder flexion. Obviously, our patients could not use their ankle flexors and extensors in the missing part of a leg. We observed in these patients different anticipatory changes in proximal postural muscles of the two legs that were apparently adaptive to the primary cause, the amputation. Should a therapist try to train these patients to demonstrate the 'normal ', symmetrical patterns of anticipatory postural adjustments? In this, most obvious, case everybody will probably agree that the answer is 'No!'
PARKINSON'S DISEASE

Examples of motor pathologies

AMPUTATION

Let us start with the most straightforward example of amputation of a part of a leg. Here, the primary cause of the motor disorders is unambiguously clear. Leg amputation leads to a major disruption of the biomechanical

There are four basic clinical features of Parkinson's disease : tremor, bradykinesia, rigidity, and deficits in postural reflexes.ls Postural disorders in Parkinson's disease involve two components, a poorly controlled increase in the feedback-triggered corrective postural reactions" and a deficit in the anticipatory changes in the activity of postural muscles." Both components are assumed to be based on a mechanism of pre-programming which is involved in the preparation of quick, albeit suboptimally efficient corrections in anticipation of a perturbation. Let us assume, for the sake of discussion, that the primary dysfunction in Parkinson's disease includes problems in triggering pre-programmed reactions. If the
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ability to trigger motor corrections is impaired and there is no compensation, the most commonly used motor programmes may become useless, since any external perturbation would lead to their disruption (e.g. falling down). Let us suppose that the CNS still wants to use some of the programmes that require corrections on the basis of pre-programming like walking and maintenance of vertical posture. The necessary pre-programmed reactions are stored in the memory but the mechanism of their triggering is defective. What kind of adaptive behaviour may be expected from such a system? First, the CNS is likely to prefer to move at slower speeds (bradykinesia) in order to minimize reactive postural perturbations and to have more time for the generation of motor corrections. Second, it may try to compensate for the impaired ability to adequately preprogramme by decreasing the triggering threshold for the pre-programmed corrections and/or increasing their gain, thus leading to a likely overcompensation. An excessively strong corrective movement will give rise to a new perturbation leading to a pre-programmed reaction in the opposite direction. Such a compensatory mechanism may lead to the following changes in the peripheral motor patterns: resistance of the system to externally imposed movements will increase (cf. rigidity), and oscillations can occur with a period corresponding to slightly more than double the latency of the preprogrammed reactions due to the time necessary for the peripheral receptors to react to a perturbation induced by a preceding pre-programmed reaction. This assessment leads to a value of about 5-6 Hz (cf. Parkinsonian tremor). Note, however, that there is a strong evidence for the central nature of the parkinsonian resting tremor.20.21 Also, walking and standing will be possible, although they are likely to look awkwardly rigid. Thus, only the loss of postural reflexes remains a reflection of the hypothetical, primary dysfunction in pre-programming. Should a therapist encourage a patient with Parkinsons disease to walk normally and to make faster movements? This is a non-trivial question. If the primary dysfunction persists, an attempt to generate normal movement patterns may, in the best case, be unsuccessful, and in the worst case, lead to a trauma.
DOWN SYNDROME

Motor disorders in Down syndrome are commonly addressed as clumsiness. The word clumsiness is used to indicate movements that look different from, and less efficient than, those observed in the general population. Two major components of clumsiness in Down syndrome
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include slowness of the movements and the inability to rapidly respond to the changing environment.22 25 The latter factor is seen in the laboratory studies as a deficit in pre-programming and longer reaction time^.":'^'^^" Commonly, clumsiness has been assumed to originate from a malfunction of a subsystem within the general system of movement production that is responsible for information processing, including decision-making. Our basic assumption implies that the CNS of a person whose decision-making component of the system for movement production is in some way impaired, may prefer to facilitate clumsy movements rather than risk total failure during motor task performance. During a lifetime the CNS accumulates experiences that would allow it to predict that unexpected changes in external conditions can include changes in the movement goal, in the external forces, in the inertial loading, etc. Therefore, if the CNS is aware of its impaired ability to make quick, adequate decisions, it may be reluctant to produce motor commands leading to very fast movements in order to have more time for evasive actions or corrections in response to a change in the environment (perturbation) and/or to attenuate potentially damaging effects of the perturbation. Pre-programming during unidirectional single-joint movements in unimpaired control subjects usually involves a reciprocal pattern of muscle activation, i.e. an unexpected loading leads to an increase in the agonist muscle activity, while an unexpected unloading leads to a decrease in the agonist activity with a possible increase in the activity of the antagonist muscle 31 (a reciprocal strategy). Subjects with Down syndrome have frequently demonstrated a coactivation pattern of pre-programming that involves an increase in activity of both agonist and antagonist muscles, irrespective of the direction of a perturbation333 (a coactivation strategy). Should this difference be considered a sign of an inability of the system of pre-programming to behave correctly, or is this a sign of the preferred strategy for a changed CNS? Coactivation could represent the consequence of an altered (impaired) mechanism of pre-programming or it could represent a safety-catch imposed by the CNS to allow movement to be controlled within the constraints of its impaired operating capacity. Novices in the early stages of acquiring a new motor skill frequently demonstrate greater than optimal levels of cocontraction which appear to increase stability and reduce the likelihood of error.34 This cocontraction commonly disappears after the skill is well learned. Thus, we think that muscle coactivation is likely to reflect active intervention by the CNS rather than its inability to use more normal patterns of muscle activation.

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If the reciprocal strategy is used for corrections of unexpected perturbations of a voluntary movement, preprogramming an increase in activity of a wrong muscle group can lead to exacerbation of the effects of the perturbation. The coactivation strategy is more universal in the sense that it leads to an attenuation of the effects of perturbations independently of the perturbation direction. On the other hand, it is always suboptimal since it cannot, in principle, lead to total compensation of the effects of perturbation. This may be the reason why this strategy has not been seen in highly practised control subjects who prefer to use the more effective, although more challenging, reciprocal strategy. Apparently, this strategy is within a safety zone established by their unimpaired CNS. If the individuals ability to make quick decisions is impaired, it may become preferable to adjust the control mechanisms suppressing potentially harmful ones that are likely to include very fast movements and certain patterns of modulation of pre-programmed reactions. In the reproducible and friendly conditions of the laboratory these internal restrictions may be lifted, leading to virtually normal performance in motor tests. In particular, in our experiments,33 subjects with Down syndrome who were well practised frequently demonstrated a mixture of reciprocal and coactivation patterns of pre-programming in different trials within the same series or block of trials. In another prolonged practice of single-joint elbow flexion movements as fast as possible led to a striking improvement in the performance transferable to different distances, and different initial and final positions. The question of whether an improvement acquired in a standardized laboratory environment may benefit everyday movements performed in much less reproducible conditions remains open. We are cautiously pessimistic. When the CNS for the first time encounters unpredictable perturbations, it may quickly return to the old, reliable, safe patterns. It is possible that practice with an element of uncertainty may be successful in persuading the CNS that it is able to reconsider its priorities and shift to more effective albeit more challenging modes of control.
Future directions in motor control research

physicists who built their elegant science on the experience of many generations. The human body and its subsystems, particularly the system for production of voluntary movements, are examples of so-called complex systems whose behaviour cannot be reduced to the behaviour of their elements (e.g. individual neurons, muscles, etc.). We are presently at the very early stages of the development of the physics of complex systems, and there is no general theory of functioning of such systems. The situation gets only worse when one deals with an abnormally functioning complex system. In an ideal world we should have started from square one and moved consistently thrmgh all the intermediate stages towards a general theory that would account for normal and abnormal motor control as particular cases. However, the patients cannot wait for a global theory to emerge, so purely empirical studies are of a great practical importance, particularly those assessing the effectiveness of therapies based on clinical measures and personal subjective feelings of the patient. Let us point out the following major directions of research that we consider crucial for progress in motor control research in rehabilitation medicine :
(1) Understanding the mechanisms of motor control in unimpaired persons. (2) Identifying the basic differences between the motor patterns of abnormal movements and movements of healthy persons. (3) Identifying primary and adaptive components of abnormal motor patterns. (4) Creating hypotheses of the underlying causes of motor abnormalities. (5) Assessing the efficacy of the existing therapeutic approaches in correcting the apparently abnormal patterns. (6) Contributing to the development of new therapeutic strategies.

Progress in any area of science goes through a number of stages whose sequence is usually additive. For example, contemporary physics would not have been developed without an appropriate foundation which consisted, in particular, of a sophisticated mathematical apparatus and Newtonian physics. We can only envy the

There has been considerable progress in understanding normal mechanisms of motor control along several lines. This progress has been most apparent in the studies of relatively simple objects (a single muscle or a single joint) during relatively simple motor tasks (e.g. a unidirectional flexion or extension). At the level of simple single-joint movements there are a few competing theories that specify hypothetical control variables that are used by the CNS to control voluntary movements (for reviews see refs 5, 36 and 37). More natural, multi-joint movements are much harder to analyse because of an increase in the number of components within multi-joint systems, and also because of a number of new factors that have been largely ignored in the studies of single297

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joint movements. These factors involve, in particular, biarticular muscles, reactive forces emerging due to mechanical joint interaction, Coriolis forces, and others. As a result the basic principles of control of multi-joint movements are much less clearly understood, and there is no general theory that would specify control variables used by the CNS to control such movements. Note also that any movement of a multi-segment system is a postural perturbation for virtually every joint within this system. The recent progress in the studies of postural reactions associated with voluntary movements has been recently reviewed by Massion. There has also been considerable progress in understanding an aspect of motor coordination that governs the interaction among many components of a complex system. This promising direction of studies is frequently referred to as dynamic pattern generation (for review see refs 3840). One would certainly like clinical studies of disordered movements to be based on a general theory of motor control, and to address such questions as: Is the CNS of a patient using the same control variables? What are the changes in the patterns of control variables associated with everyday voluntary movements? Have there been changes in the CNS priorities (laws of coordination)? What would be the optimal movement pattern for a given state of the neuromotor system? Is the CNS failing to achieve the optimal pattern because of such factors as pain, the lack of assisting devices, or some others? Can a therapist help the CNS to reach the optimal movement strategy? However, the lack of a universally accepted general theory of motor control forces the researchers in the area of clinical movement studies to turn to more narrow and empirical questions. Most of these studies describe the differences between motor patterns in a patient population and in a control group during standardized motor tasks, and formulate hypotheses on possible links between the apparent neurological (or other) abnormality and impaired movements. Such studies are more likely to have an immediate practical effect. However, they create an impression of the pieces of a jigsaw puzzle that are impossible to put together without a general idea of the whole picture, i.e. a general theory. We have mostly emphasized in this brief review the frequently overlooked important factor of distinguishing between primary and adaptive components in abnormal movements. This factor seems particularly important for the area of motor rehabilitation, in which an understanding of the importance of adaptive processes within the central nervous system is a prerequisite for developing rehabilitation strategies directed towards optimization of the natural process of adaptation to a motor impairment.

It seems obvious to us, however, that considerable progress in the area of motor rehabilitation requires studies along all the aforementioned major directions. We hope that a carefully balanced blend of basic and clinical motor research will succeed in creating a general theory of abnormal movements and providing practical recommendations to physicians.
Acknowledgements We are grateful to Dr Greg Anson for many helpful and inspiring discussions. The study has been supported by a grant HD30128 from the National Center for Medical Rehabilitation Research. NIH. References
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