Functional roles of the proprioceptive system in the control of goal-directed movement.

This article explored functional roles of the proprioceptive system during the control of goal-directed movements. Proprioceptive information contributes to the control of movement through both reflex and central connections. Spinal and transcortical reflex loops establish a servomechanism which provides automatic corrections of unexpected changes in muscle length and allows compensation for undesirable irregularities in the mechanical properties of muscles by modulating limb stiffness at the subconscious level. Central connections provide the control system with information about peripheral states which is used in voluntary components of movement control. Before the initiation of movement, proprioceptive information about initial limb orientation becomes a basis for the programming of motor commands. During a movement, proprioceptive input about velocities and angular displacements of a limb is used to regulate movement by triggering planned sequences of muscle activation and modulating motor commands. After movement, feedback produced by responses is compared with previously stored information, verifying the quality of the movement. Considering potential roles of the reflex and central connections, the proprioceptive system seems to constitute an important aspect of motor control mechanisms, providing the control system with efficiency and flexibility in the regulation of goal-directed movements.     

Time and direction preparation of the long latency stretch reflex

This study investigated time and direction preparation of motor response to force load while intending to maintain the finger at the initial neutral position. Force load extending or flexing the index finger was given while healthy humans intended to maintain the index finger at the initial neutral position. Electromyographic activity was recorded from the first dorsal interosseous muscle. A precue with or without advanced information regarding the direction of the forthcoming force load was given 1000 ms before force load. Trials without the precue were inserted between the precued trials. A long latency stretch reflex was elicited by force load regardless of its direction, indicating that the long latency stretch reflex is elicited not only by muscle stretch afferents, but also by direction-insensitive sensations. Time preparation of motor response to either direction of force load enhanced the long latency stretch reflex, indicating that time preparation is not mediated by afferent discharge of muscle stretch. Direction preparation enhanced the long latency stretch reflex and increased corticospinal excitability 0–20 ms after force load when force load was given in the direction stretching the muscle. These enhancements must be induced by preset of the afferent pathway mediating segmental stretch reflex.     

The problem of redundancy in movement control: The adaptive model theory approach

Summary The problem of redundancy in movement control is encountered when one attempts to answer the question: How does the central nervous system (CNS) determine the pattern of neural activity required in some 5,000,000 descending motor fibres to control only 100–150 biomechanical degrees of freedom of movement? Mathematically this is equivalent to solving a set of simultaneous equations with many more unknowns than equations. This system of equations is redundant because it has an infinite number of possible solutions. The problem is solved by the neuronal circuitry hypothesized in Adaptive Model Theory (AMT). According to AMT, the CNS includes neuronal circuitry able to compute and maintain adaptively the accuracy of internal models of the reciprocal multivariable relationships between outgoing motor commands and their resulting sensory consequences. To identify these input-output relationships by means of regression analysis, correlations between the input signals have to be taken into account. For example, if the inputs are perfectly correlated, the model reduces to a virtual one-input system. In general, the number of inputs modelled equals the number of degrees of freedom encoded by the signals; that is, the number of independently varying (orthogonal) signals. The adaptive modelling circuitry proposed in AMT automatically tunes itself to extract independently varying sensory and motor signals before computing the dynamic relationships between them. Inverse models are employed during response execution to translate movements preplanned as desired trajectories of these high-level sensory-feature signals into appropriately co-ordinated motor commands to send to the muscles. Since movement is preplanned in terms of a number of orthogonalized sensory-feature signals equal to the number of degrees of freedom in the desired response, the problem of redundancy is solved and the correlation or co-ordination between motor-command signals is automatically introduced by the adaptive models.     

The Effect of Motor Preparation on Changes in H Reflex Amplitude During the Response Latency of a Warned Reaction Time Task

Monosynaptic Hoffman reflexes (H reflexes) were recorded from the soleus muscle during the response latency of a warned reaction time (RT) task that required plantarflexion of the foot. The task was done under four conditions of predictability of the response signal (RS), created by the factorial combination of foreperiod duration (1 and 4 s) and variability (fixed and variable). RT varied systematically with RS predictability and was facilitated in conditions that favored prediction of the RS. The response latency was divided into two successive phases by the onset of reflex augmentation: a premotor phase of constant reflex amplitude and a succeeding motor phase marked by progressively increasing reflex amplitude. Reflex augmentation during the motor phase was coupled more closely to the imminent movement than to the preceding signal to respond. The duration of the premotor phase was unaffected by RS predictability, but the duration of the motor phase (like RT) was shorter when the RS was more predictable. The maximum H reflex amplitude reached during the motor phase was greater when the RS was more predictable. The tonic level of H reflex amplitude during the premotor phase was greater in conditions that made prediction of the RS difficult. A second experiment showed that this difference was present throughout the foreperiod.

These results suggest that conditions that favor prediction of the RS enhance motor preparation. Changes in motor preparation (which affect RT) affect the processes underlying reflex augmentation in the motor phase. Enhanced preparation may allow more efficient organization of the descending commands to move, causing higher levels of spinal excitability to be reached in a briefer time. The higher tonic reflex amplitudes in the premotor phase and throughout the preceding foreperiod, in conditions that make prediction of the RS difficult, appear to reflect heightened general arousal.     

Control of Trajectory Modifications in Target-Directed Reaching

Human reaching movements to fixed and displaced visual targets were recorded and compared with simulated movements generated by using a two-joint arm model based on the equilibrium-point (EP) hypothesis (lambda model) of motor control (Feldman, 1986). The aim was to investigate the form of central control signals underlying these movements. According to this hypothesis, movements result from changes in control variables that shift the equilibrium position (EP) of the arm. At any time, muscle activations and forces will depend on the difference between the arm's EP and its actual position and on the limb's velocity. In this article, we suggest that the direction of EP shift in reaching is specified at the hand level, whereas the rate of EP shift may be specified at the hand or joint level. A common mechanism underlying reaching to fixed and displaced targets is proposed whereby the EP of the hand shifts in a straight line toward the present target. After the target is displaced, the direction of the hand EP shift is modified toward the second target. The results suggest that the rate of shift of the hand EP may be modified for movements in different parts of the work space. The model, with control signals that vary in a simple fashion over time, is able to generate the kinematic patterns observed empirically.     

Evidence for adaptive shoulder-elbow control in cyclical movements with different amplitudes, frequencies, and orientations

The evolution of joint dynamics and muscle patterning in the shoulder and elbow was studied for cyclical line drawing tasks at different frequencies, amplitudes, and orientations in the horizontal plane. Three main modes of control were identified: elbow-centered, shoulder-centered, and elbow-shoulder, each referring to the principal joints or joint combinations that were used to achieve the behavioral goals. The contribution of the shoulder joint was most prominent across the majority of movement orientations and largely paralleled changes in the dynamic (inertial) forces in the end effector (shoulder-centered control). The two joints either exchanged roles during the performance of the right diagonal movement (elbow-centered control) or shifted from a single-joint strategy to a dual-joint strategy during the performance of large amplitudes with low or medium cycling frequencies (shoulder-elbow control). These behavioral results support the existence of a modular control mode that allows the central nervous system to effectively tune motor commands to meet a broad variety of orientations, amplitudes, and frequencies. This refers to the emergence of a context-dependent control mode for the shoulder and elbow that optimizes the implementation of the underlying motor goals under a rich combination of spatial and temporal manipulations.     

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.     

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.     

Reflex responses of human lip muscles to mechanical stimulation during speech

The role played by reflex pathways in the production of movement has been a significant issue for motor control theorists interested in a wide variety of motor behaviors. From studies of locomotion and chewing, it appears that gains in reflex pathways can be altered so that activity in these pathways does not produce destabilizing responses during movement. In speech production, recent experimental evidence has been interpreted to suggest that autogenetic lip reflexes (perioral reflexes) are suppressed during sustained phonation or speech production. The present study was conducted to assess the effects of phonation, direction of movement, and ongoing speech production on reflex responses of lip muscles. The present results suggest, in contrast to earlier work, that this reflex pathway is not suppressed or absent because the amplitude of the observed response depends upon the activation levels of the various muscles of the lower lip and, therefore, indirectly on the nature of the gesture the subject is instructed to produce.     

Reflex Responses of Human Lip Muscles to Mechanical Stimulation During Speech

The role played by reflex pathways in the production of movement has been a significant issue for motor control theorists interested in a wide variety of motor behaviors. From studies of locomotion and chewing, it appears that gains in reflex pathways can be altered so that activity in these pathways does not produce destabilizing responses during movement. In speech production, recent experimental evidence has been interpreted to suggest that autogenetic lip reflexes (perioral reflexes) are suppressed during sustained phonation or speech production. The present study was conducted to assess the effects of phonation, direction of movement, and ongoing speech production on reflex responses of lip muscles. The present results suggest, in contrast to earlier work, that this reflex pathway is not suppressed during phonation or speech. However, the response may appear to be suppressed or absent because the amplitude of the observed response depends upon the activation levels of the various muscles of the lower lip and, therefore, indirectly on the nature of the gesture the subject is instructed to produce.     

Training-specific adaptations of H- and stretch reflexes in human soleus muscle

The authors investigated the effect of physical exercise on reflex excitability in a controlled intervention study. Healthy participants (N = 21) performed 4 weeks of either power training (ballistic strength training) or balance training (sensorimotor training [SMT]). Both training regimens enhanced balance control and rate of force development, whereas reductions in peak-to-peak amplitudes of stretch reflexes and in the ratio of the maximum Hoffman reflex to the maximum efferent motor response (Hmax:Mmax) measured at rest were limited to SMT. The differences in reflex excitability between the training regimens indicated different underlying neural mechanisms of adaptation. The reduced reflex excitability following SMT was most likely induced by supraspinal influence. The authors discuss an overall increase in presynaptic inhibition of Ia afferent fibers as a possible mechanism.     

Visual prediction: psychophysics and neurophysiology of compensation for time delays

A necessary consequence of the nature of neural transmission systems is that as change in the physical state of a time-varying event takes place, delays produce error between the instantaneous registered state and the external state. Another source of delay is the transmission of internal motor commands to muscles and the inertia of the musculoskeletal system. How does the central nervous system compensate for these pervasive delays? Although it has been argued that delay compensation occurs late in the motor planning stages, even the earliest visual processes, such as phototransduction, contribute significantly to delays. I argue that compensation is not an exclusive property of the motor system, but rather, is a pervasive feature of the central nervous system (CNS) organization. Although the motor planning system may contain a highly flexible compensation mechanism, accounting not just for delays but also variability in delays (e.g., those resulting from variations in luminance contrast, internal body temperature, muscle fatigue, etc.), visual mechanisms also contribute to compensation. Previous suggestions of this notion of "visual prediction" led to a lively debate producing re-examination of previous arguments, new analyses, and review of the experiments presented here. Understanding visual prediction will inform our theories of sensory processes and visual perception, and will impact our notion of visual awareness.     

Motor maps and synergies

Consider the process of raising and lowering the arm in the sagittal plane. Different parts of different muscles operate over different sectors of the angular range. How and why does the nervous system implement this differential muscle activation according to joint angle? We contend that such control depends on the adaptive formation of motor maps. These solve the problem of redundancy in the musculoskeletal system by connecting a relatively small number of cortical columns in the motor cortex to a large number of alpha motor neuron pools. We argue that motor maps are formed such that each functional muscle is activated in proportion to its moment arm about the movement. Because of this the required agonist and antagonist turning forces are generated with a minimum demand for metabolic energy. We know from biomechanical principles that, at any given posture, those muscle fibres that change length most in response to a small joint-angle change are those with the greatest moment arm. Likewise those that change least have the smallest. By establishing a model of the polynomial relationships between the lengths of functional muscles l and the corresponding changes in joint angles theta, the nervous system can generate signals partial differentiallj/ partial differentialthetai (where lj is the length of the jth functional muscle and thetai is the magnitude of the ith elemental movement). These signals create motor maps by modulating the gains of descending motor pathways. As a result, functional muscles are activated in proportion to their moment arms. This reduces the demand for metabolic energy to a minimum. Since moment arms change with joint angle, it also accounts for the experimental observations above. Such motor mapping effectively provides a minimum energy "wired-in" synergy. Established in utero, motor maps are the first stage of synergy formation and provide the basis for the development of subsequent task-dependent synergies.     

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.     

The role of the perioral reflex in lip motor control for speech.

The analysis of spinal and brainstem reflexes has been shown to be a useful method of quantifying the various inputs to motoneuron pools involved in voluntary motor control. This work is selectively reviewed as a background to a discussion of the role of the perioral reflex in lip motor control for speech. Data on the sensorimotor innervation of the lips and the static and dynamic properties of the perioral reflex are presented in support of the notions that (1) perioral reflex analysis provides a viable technique for analyzing brainstem excitability changes underlying lip muscle contraction for speech, and (2) the perioral reflex loop is an important functional element in lip motor control for speech.     

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.     

Common pathways in mental imagery and pain perception: an fMRI study of a subject with an amputated arm

The present paper reviews data from two previous studies in our laboratory, as well as some additional new data, on the neuronal representation of movement and pain imagery in a subject with an amputated right arm. The subject imagined painful and non-painful finger movements in the amputated stump while being in a MRI scanner, acquiring EPI-images for fMRI analysis. In Study I (Ersland et al., 1996) the Subject alternated tapping with his intact left hand fingers and imagining "tapping" with the fingers of his amputated right arm. The results showed increased neuronal activation in the right motor cortex (precentral gyrus) when tapping with the fingers of the left hand, and a corresponding activation in the left motor cortex when imagining tapping with the fingers of the amputated right arm. Finger tappings of the intact left hand fingers also resulted in a larger activated precentral area than imagery "finger tapping" of the amputated right arm fingers. In Study II (Rosen et al., 2001 in press) the same subject imagining painful and pleasurable finger movements, and still positions of the fingers of the amputated arm. The results showed larger activations over the motor cortex for movement imagining versus imagining the hand being in a still position, and larger activations over the sensory cortex when imagining painful experiences. It can therefore be concluded that not only does imagery activate the same motor areas as real finger movements, but also that adding instructions of pain together with imaging moving the fingers intensified the activation compared with adding instructions about non-painful experiences. From these studies, it is clear that areas activated during actual motor execution to a large extent also are activated during mental imagery of the same motor commands. In this respect the present studies add to studies of visual imagery that have shown a similar correspondence in activation between actual object perception and imagery of the same object.     

What do fully paralyzed awake humans feel when they attempt to move?

Subjects are able to judge the strength of muscle contraction. In theory, the force of muscular exertion could be perceived either from mechanoreceptor afferents or from knowledge of central motor command (corollary discharge). Sensations of great effort or exerted force have been described by subjects when their limbs were weakened by fatigue or partial paralysis. This has been taken as evidence that effort sensations arise from central motor commands rather than from mechanoreceptor afferent signals produced by muscle contraction. To differentiate between these possibilities, we used neuromuscular block to completely paralyze four waking subjects and required them to attempt maximal contraction of inspiratory muscles and of hand muscles. They were questioned after recovery about what their sensations were when attempting these contractions. None described the sensations of exerted force, great effort, or heaviness, which would have been expected if motor commands alone were the source of these sensations. The contradiction between our findings and those previously reported suggests that the specific neural mechanisms for effort sensations must be reexamined.     

Toward a theory of apractic syndromes

Theoretical development on human motor behavior has occurred largely independently of data on pathological movement disorders. This paper represents an initial attempt to interface findings from studies of apraxia and those of normal motor behavior with a view to formulating a common theoretical framework. Such an integration may ultimately aid in understanding the nature of skill acquisition and provide insights into the organization of motor systems. Three putative theoretical models of movement control are discussed with reference to apractic syndromes. The most commonly accepted view—the hierarchy—possesses properties such as linear transitivity and unidirectionality of information flow that render it inadequate in explaining functional plasticity in the central nervous system. The heterarchy, which incorporates reciprocity of function and circular transitivity, is a more likely candidate but suffers from an inability to regulate the degrees of freedom of the system. Our favored candidate is the coalition model which embodies heterarchical principles, but in addition, offers a solution to the problems of degrees of freedom and context for motor systems. Evidence is reviewed from apraxia of speech and limbs in terms of a coalitional style of control and an experimental approach, consonant with coalitional organization, is developed. We promote the claim that an understanding of apractic behavior—and perhaps motor systems in general—will benefit when clinicians and experimenters embrace a theory of context and constraints rather than a theory of commands as is currently in vogue.