Once more on the equilibrium-point hypothesis (lambda model) for motor control

The equilibrium control hypothesis (lambda model) is considered with special reference to the following concepts: (a) the length-force invariant characteristic (IC) of the muscle together with central and reflex systems subserving its activity; (b) the tonic stretch reflex threshold (lambda) as an independent measure of central commands descending to alpha and gamma motoneurons; (c) the equilibrium point, defined in terms of lambda, IC and static load characteristics, which is associated with the notion that posture and movement are controlled by a single mechanism; and (d) the muscle activation area (a reformulation of the "size principle")--the area of kinematic and command variables in which a rank-ordered recruitment of motor units takes place. The model is used for the interpretation of various motor phenomena, particularly electromyographic patterns. The stretch reflex in the lambda model has no mechanism to follow-up a certain muscle length prescribed by central commands. Rather, its task is to bring the system to an equilibrium, load-dependent position. Another currently popular version defines the equilibrium point concept in terms of alpha motoneuron activity alone (the alpha model). Although the model imitates (as does the lambda model) spring-like properties of motor performance, it nevertheless is inconsistent with a substantial data base on intact motor control. An analysis of alpha models, including their treatment of motor performance in deafferented animals, reveals that they suffer from grave shortcomings. It is concluded that parameterization of the stretch reflex is a basis for intact motor control. Muscle deafferentation impairs this graceful mechanism though it does not remove the possibility of movement.     

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.     

Proprioceptive control of goal-directed movements in man, studied by means of vibratory muscle tendon stimulation

The purpose of this study was to investigate the role of propriomuscular feedback in the control of pluriarticular pointing movements, performed without visual feedback toward visual targets. The proprioceptive inputs were distorted during movements by applying vibration to the distal tendon of the biceps muscle. Various movement and vibration durations were imposed. The results show that vibration affects the spatial outcome of the movements. The effects of vibration were movement time-independent when the durations were shorter than 450 ms and became movement time-dependent with longer durations. Moreover, the effects of vibration became more marked when a short vibration was applied at the end rather than at the beginning of a slow movement. These studies suggest that at least two types of proprioceptive control loops may be involved in correcting this kind of movement, depending on the execution time. In slow movements, the final phase might be a privileged period for on-line, propriomuscular-based corrections. Lastly, it emerged that the regulation of a goal-directed movement on the basis of proprioceptive feedback processing can take place within at most 200 ms.     

Rapid Error Correction During Human Arm Movements

Studies were made of rapid error correction movements in eight subjects performing a visually guided tracking task involving flexion-extension movements about the elbow. Subjects were required to minimize reaction times in this two-choice task. Errors in initial movement direction occurred in about 3% of the trials. Error correction times (time from initiation to reversal of movement in incorrect direction) ranged from 30-150 ms. The first sign of correction of the error movement was a suppression of the electromyographic (EMG) activity in the muscle producing the error movement. This suppression started as early as 20-40 ms after the initiation of the error-related EMG activity and as much as 50 ms before any overt sign of limb movement. The correction of the error movement was also accompanied by an increase in the drive to the muscle which moved the arm in the correct direction. This increased activity always occurred after the initiation of the error movement. It is concluded that the first step in the error correction, suppression of drive to the muscle producing the error movement, cannot be based on information from the moving limb. It is thus suggested that this earliest response to the error movement is based on central monitoring of the commands for movement.     

Rapid error correction during human arm movements: evidence for central monitoring

Studies were made of rapid error correction movements in eight subjects performing a visually guided tracking task involving flexion-extension movements about the elbow. Subjects were required to minimize reaction times in this two-choice task. Errors in initial movement direction occurred in about 3% of the trials. Error correction times (time from initiation to reversal of movement in incorrect direction) ranged from 30-150 ms. The first sing of correction of the error movement was a suppression of the electromyographic (EMG) activity in the muscle producing the error movement. This suppression started as early as 20-40 ms after the initiation of the error-related EMG activity and as much as 50 ms before any overt sign of limb movement. The correction of the error movement was also accompanied by an increase in the drive to the muscle which moved the arm in the correct direction. This increased activity always occurred after the initiation of the error movement. it is concluded that the first step in the error correction, suppression of drive to the muscle producing the error movement, cannot be based on information from the moving limb. It is thus suggested that this earliest response to the error movement is based on central monitoring of the commands for movement.     

Aspects of body self-calibration

The representation of body orientation and configuration is dependent on multiple sources of afferent and efferent information about ongoing and intended patterns of movement and posture. Under normal terrestrial conditions, we feel virtually weightless and we do not perceive the actual forces associated with movement and support of our body. It is during exposure to unusual forces and patterns of sensory feedback during locomotion that computations and mechanisms underlying the ongoing calibration of our body dimensions and movements are revealed. This review discusses the normal mechanisms of our position sense and calibration of our kinaesthetic, visual and auditory sensory systems, and then explores the adaptations that take place to transient Coriolis forces generated during passive body rotation. The latter are very rapid adaptations that allow body movements to become accurate again, even in the absence of visual feedback. Muscle spindle activity interpreted in relation to motor commands and internally modeled reafference is an important component in permitting this adaptation. During voluntary rotary movements of the body, the central nervous system automatically compensates for the Coriolis forces generated by limb movements. This allows accurate control to be maintained without our perceiving the forces generated.     

Adaptation to visual rearrangement: Role of sensory discordance

The relative contributions of proprioceptive and efferent information in eliciting adaptation to visual rearrangement were studied under two conditions of visual stimulation. Subjects permitted sight of their forearm under normal room illumination showed significant adaptation when the forearm was (a) moved up and down under the action of tonic vibration reflexes, (b) voluntarily moved through the same trajectory at the same pace, (c) viewed while still, and (d) viewed while the margins of the elbow were vibrated. The reflex movement condition elicited significantly greater adaptation than the other conditions. Subjects allowed only sight of a point source of light attached to their hand showed significant adaptation when the forearm was (a) reflexly moved, (b) voluntarily moved through the same trajectory at the same rate, (c) passively moved, (d) still, and (e) vibrated while still. Less adaptation occurred as the amount of proprioceptive information about limb position was decreased. The adaptation elicited by voluntary movements of the forearm and by reflex movements did not differ significantly. It is concluded that corollary-discharge signals may not be crucial in adaptation to visual rearrangement; a more important factor appears to be discordance between proprioceptive and visual information.     

Orienting to targets by looking and pointing: Parallels and interactions in ocular and manual performance

Orienting to a target by looking and pointing is examined for parallels between the control of the two systems and interactions due to movement of the eyes and limb to the same target. Parallels appear early in orienting and may be due to common processing of spatial information for the ocular and manual systems. The eyes and limb both have shorter response latency to central visual and peripheral auditory targets. Each movement also has shorter latency and duration when the target presentation is short enough (200 msec) that no analysis of feedback of the target position is possible during the movement. Interactions appear at many stages of information processing for movement. Latency of ocular movement is much longer when the subject also points, and the eye and limb movement latencies are highly correlated for orienting to auditory targets. Final position of eyes and limb are significantly correlated only when target duration is short (200 msec). This illustrates that sensory information obtained before the movement begins is an important, but not the only, source of input about target position. Additional information that assists orienting may be passed from one system to another, since visual information gained by looking aided pointing to lights and proprioceptive information from the pointing hand seemed to assist the eyes in looking to sounds. Thus the production of this simple set of movements may be partly described by a cascade-type process of parallel analysis of spatial information for eye and hand control, but is also, later in the movement, assisted by cross-system interaction.     

Interaction of Afferent and Efferent Signals Underlying Joint Position Sense

A model of joint position sense is considered based on the concept that central motor commands are adequately expressed in terms of shifts of the so-called invariant length-tension characteristics for agonist and antagonist muscles. The main points of this concept are discussed to clarify them and to prevent misunderstanding. The basic idea of the model is that the efferent copy of the central motor commands plays the role of a reference frame for evaluation of afferent proprioceptive discharges. An experiment with reproduction of constrained movements was performed in order to investigate the influence of voluntary flexor or extensor muscle tension on position sense in the elbow joint. The results demonstrate adequate perception of joint position on the background of voluntary muscle tension and thus are quite consistent with the model. The role of afferent and efferent signals in position sense is discussed with special reference to views expressed recently by different authors. The interrelation between position sense and sense of effort is considered, based on a concept of senso-motor space.     

Interaction of afferent and efferent signals underlying joint position sense: empirical and theoretical approaches

A model of joint position sense is considered based on the concept that central motor commands are adequately expressed in terms of shifts of the so-called invariant length-tension characteristics for agonist and antagonist muscles. The main points of this concept are discussed to clarify them and to prevent misunderstanding. The basic idea of the model is that the efferent copy of the central motor commands plays the role of a reference frame for evaluation of afferent proprioceptive discharges. An experiment with reproduction of constrained movements was performed in order to investigate the influence of voluntary flexor or extensor muscle tension on position sense in the elbow joint. The results demonstrate adequate perception of joint position on the background of voluntary muscle tension and thus are quite consistent with the model. The role of afferent and efferent signals in position sense is discussed with special reference to views expressed recently by different authors. The interrelation between position sense and sense of effort is considered, based on a concept of senso-motor space.     

Simulation Studies of Descending and Reflex Control of Fast Movements

Several neurological control strategies for fast head movements are considered using computer simulations of a stretch reflex model. Each control strategy incorporates a different amount of proprioceptive feedback contributing to braking and/or clamping the movement. The model behavior for each control strategy is qualitatively compared to experimental data that includes the agonist and antagonist EMGs, and the head position, velocity, and acceleration. Significance of the study is discussed with respect to the characteristic tri-phasic EMG pattern for fast voluntary movements and the possible roles that the stretch reflex may have in contributing to this pattern of activation.     

Role of proprioceptive information in movement programming and control in 5 to 11-year old children

The role of proprioceptive inputs in the control of goal-directed movements was examined, by means of the tendon vibration technique, in 5 to 11-year old children performing a serial pointing task. Children pointed, with movements of various amplitudes and at various positions, by alternating wrist flexions and extensions. Tendon vibration was applied to both agonist and antagonist muscles to perturb relevant muscular proprioceptive inputs during the static or dynamic phase of the task, i.e., during stops on targets or during movement execution. Constant and variable amplitude errors as well as constant position error were evaluated. Vibratory perturbation applied during movement execution resulted in a similar reduction in movement amplitude, yielding an increased constant error in all age groups and a systematic position error in the direction of the movement starting point. Perturbing proprioception during static phases preceding movement resulted in an age-related increase in the variable amplitude error, which was maximal in 5-year old children performing extension movements. The results were interpreted in terms of the use of proprioceptive information in the feedforward and feedback based components of movement control in children. In particular, the results indicated (1) developmental changes in the relative weighting of each component, (2) an increased capacity to move from one strategy to the other, depending on the availability of information, and (3) developmental changes from an alternated to an integrated control of amplitude and position in serial pointing.     

Kinematic analysis of goal-directed aims made against early and late perturbations: an investigation of the relative influence of two online control processes

Examination of goal-directed movements has evidenced two processes of visually regulated online control: early trajectory control that operates to make movement adjustments on the basis of limb velocity comparisons to internally generated models of the expected limb velocity, and late trajectory control that uses allocentric information about the limb and target positions. The results of experiments using illusory perturbations suggest that the two systems have an additive influence on movement outcome, and are relatively independent. In this theoretical context, three experiments were conducted in which actual perturbations to the aiming limb dynamics and the tasks demands were introduced. Compressed air expulsed through a stylus, in the direction of, or opposite to, that of the movement was used to impact limb velocity and the target location was moved at movement initiation to impact late evaluation of target and limb position. The results of the compressed air-only and moving target-only conditions replicated the previous evidence of early and late control, respectively. Interestingly, movement accuracy measures yielded an interactive effect of the two perturbations when presented in tandem. It appears that the perturbations prompted parallel operation of the two control processes.     

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.     

Control of goal-directed movements: the contribution of orienting of visual attention and motor preparation.

Three experiments investigated the role of attention and motor preparation for the control of goal-directed movements. In Experiment 1 (double step paradigm), a movement correction was required on 25% of the trials towards the left or right of the initial target. Within these 25% of trials, the probability of location of the second target was manipulated. The efficiency of movement control increased when increasing the probability of correcting the movement in a given direction. In Experiment 2, attentional processes were isolated by asking the subjects to verbally detect the more or less probable target displacement, without correcting their movement. Subjects were able to orient visual attention during movement execution, thus improving the processing of visual feedbacks from target displacement. In Experiment 3, motor preparation processes were isolated by asking the subjects to correct their movement towards a fixed target in response to a more or less probable mechanical perturbation. It was shown that motor preparation not only specifies the initial movement parameters but may also include some parameters of the most probable movement modulations. Overall, these results highlight the role of both attentional and motor preparation processes in the control of goal-directed movements and suggest that the feedback-based corrections of the movement are modulated by a feedforward control.     

Central fatigue mechanisms are responsible for decreases in hand proprioceptive acuity following shoulder muscle fatigue

Muscle fatigue is a complex phenomenon, consisting of central and peripheral mechanisms which contribute to local and systemic changes in motor performance. In particular, it has been demonstrated that afferent processing in the fatigued muscle (e.g., shoulder), as well as in surrounding or distal muscles (e.g., hand) can be altered by fatigue. Currently, it is unclear how proximal muscle fatigue affects proprioceptive acuity of the distal limb. The purpose of the present study was to assess the effects of shoulder muscle fatigue on participants’ ability to judge the location of their hand using only proprioceptive cues. Participants’ (N = 16) limbs were moved outwards by a robot manipulandum and they were instructed to estimate the position of their hand relative to one of four visual reference targets (two near, two far). This estimation task was completed before and after a repetitive pointing task was performed to fatigue the shoulder muscles. To assess central versus peripheral effects of fatigue on the distal limb, the right shoulder was fatigued and proprioceptive acuity of the left and right hands were tested. Results showed that there was a significant decrease in the accuracy of proprioceptive estimates for both hands after the right shoulder was fatigued, with no change in the precision of proprioceptive estimates. A control experiment (N = 8), in which participants completed the proprioceptive estimation task before and after a period of quiet sitting, ruled out the possibility that the bilateral changes in proprioceptive accuracy were due to a practice effect. Together, these results indicate that shoulder muscle fatigue decreases proprioceptive acuity in both hands, suggesting that central fatigue mechanisms are primarily responsible for changes in afferent feedback processing of the distal upper limb.     

A Computational Model of the Simplest Motor Program

A computational procedure (program) is defined to generate control signals for the motoneuron pools of agonist and antagonist muscles that will move a limb segment from one stationary position to another. The program accounts for the ability to move different distances with different inertial loads and for the influence of instructions concerning movement speed and accuracy. These motor commands allow the program to produce EMG patterns as well as force and kinematic trajectories that are consistent with much of the data found in the literature of these movements. The program is premised on the notion that kinematically defined tasks are accomplished by programming commands to the motoneuron pools, based on only a few cognitively recognized kinematic and dynamic features of the task. Most of the features found in EMG and kinematic patterns can be considered consequences of the program's algorithmic procedures rather than specifically planned features of those movements.     

Descending control to the nonparetic limb degrades the cyclic activity of paretic leg muscles

During anti-phased locomotor tasks such as cycling or walking, hemiparetic phasing of muscle activity is characterized by inappropriate early onset of activity for some paretic muscles and prolonged activity in others. Pedaling with the paretic limb alone reduces inappropriate prolonged activity, suggesting a combined influence of contralesional voluntary commands and movement-related sensory feedback. Five different non-target leg movement state conditions were performed by 15 subjects post-stroke and 15 nonimpaired controls while they pedaled with the target leg and EMG was recorded bilaterally. Voluntary engagement of the non-lesioned motor system increased prolonged paretic vastus medialis (VM) activity and increased phase-advanced rectus femoris (RF) activity. We suggest bilateral descending commands are primarily responsible for the inappropriate activity in the paretic VM during anti-phase pedaling, and contribute to the dysfunctional motor output in the paretic RF. Findings from controls suggest that even an undamaged motor system can contribute to this phenomenon.     

Adaptation to visual and proprioceptive rearrangement: Origin of the differential effectiveness of active and passive movements

In Experiment 1, subjects exposed to a discordance between the visual and ”proprioceptive” locations of external targets were found to exhibit aftereffects when later pointing without sight of their hands at visual targets. Aftereffects occur both when the discordance is introduced in the traditional fashion by displacing the visual locations of targets and when the proprioceptive locations of targets are displaced. These observations indicate that there is nothing unique about the visual rearrangement paradigm—the crucial factor determining whether adaptation will be elicited is the presence of a discordance in the positional information being conveyed over two different sensory modalities. In a second experiment, the effectiveness of active and passive movements in eliciting adaptation was studied using an experimental paradigm in which subjects were exposed to a systematic discordance between the visual and proprioceptive locations of external targets without ever being permitted sight of their hands; a superiority of active movements was observed, just as is usually found in visual rearrangement experiments in which sight of the hand is permitted. Evidence is presented that the failure of passive movements to elicit adaptation is related to a deterioration in accuracy of position sense information during passive limb movement.     

Sensory feedback in the learning of a novel motor task

The role of different forms of feedback is examined in learning a novel motor task. Five groups of ten subjects had to learn the voluntary control of the abduction of the big toe, each under a different feedback condition (proprioceptive feedback, visual feedback, EMG feedback, tactile feedback, force feedback). The task was selected for two reasons. First, in most motor learning studies subjects have to perform simple movements which present hardly any learning problem. Second, studying the learning of a new movement an provide useful information for neuromuscular reeducation, where patients often also have to learn movements for which no control strategy exists. The results show that artificial sensory feedback (EMG feedback, force feedback) is more powerful than "natural" (proprioceptive, visual, and tactile) feedback. The implications of these results for neuromuscular reeducation are discussed.