Proprioceptive feedback during point-to-point arm movements is tuned to the expected dynamics of the task

It has previously been found that in point-to-point movements against inertial loads, proprioceptive feedback is centrally suppressed in the beginning of movement and is facilitated at a time that is correlated with the expected time of peak velocity. This suggests that the modulation of proprioceptive feedback is governed by the desired movement kinematics. Here we show that in movements against inertial and viscous loads, the correlation of the time when the feedback is facilitated is strongest with the time when the joint torque is expected to be maximal. This suggests that the modulation of proprioceptive feedback is governed by the desired movement dynamics. We applied unexpected perturbations in point-to-point elbow flexion movements against known light and heavy inertial and viscous loads and determined the time and magnitude of responses in the electromyogram (EMG) of the biceps and triceps muscles. In movements against the inertial and viscous loads, the time of the EMG responses was better predicted by the time of the peak joint torque in the unperturbed movement than by the time of peak velocity or the time of peak acceleration or by measures related to the agonist EMG. Moreover, the EMG response changed from a reciprocal pattern in the inertial load conditions to a co-contraction pattern in the viscous load conditions. Our results suggest that during movements against known stable dynamic loads, proprioceptive feedback is tuned to the expected task dynamics and is facilitated so as to maintain muscle stiffness at a time when the muscles are expected to generate maximal force.     

Control of fast elbow movement: a study of electromyographic patterns during movements against unexpectedly decreased inertial load

Predictions of three models of single-joint motor control were compared with experimental observations of the changes in electromyographic (EMG) patterns during fast voluntary movements against an unexpectedly reduced inertial load. The subjects performed elbow flexions over 40° as fast as possible in two series. During the first series, an approximately 40% decrease in inertia, simulated by a torque-motor, might occur unpredictably on half of the trials (unloaded trials). During the second series, all the trials were unloaded. The major findings are: (1) no differences in the antagonist burst latency in unexpectedly unloaded and unperturbed trials; (2) a decrease in the antagonist latency during expected unloadings; (3) a small, statistically non significant decrease in the first agonist burst EMG integral; and (4) a larger, statistically significant increase in the antagonist burst EMG integral in unexpectedly unloaded trials as compared to unperturbed trials. The data are in good correspondence with a version of the equilibrium-point hypothesis that assumes central programming of the beginning of the antagonist burst and incorporates the possibility of reflex-induced changes in EMG amplitudes.     

Voluntary rhythmical movement is reset by stimulating the motor cortex

Using six normal subjects, we mapped the best location for magnetic cortical stimulation to reset the phase of a voluntary alternating movement of the right wrist made against three different torques (0.26 N m extension, 0 and 0.09 N m flexion torque) at the subjects' preferred rate. We used nett resetting as a measure of phase resetting, based upon the relative amplitudes of the averages of the stimulated and a phase-locked control position record. Nine sites covering a 5 cm square region of the contralateral cortex were systematically stimulated. All the subjects showed evidence of resetting in response to magnetic stimulation over one or more cortical sites during movements made against the extension torque and all subjects demonstrated higher levels of nett resetting under these conditions than in response to similar cortical stimulation during unloaded movements. The best cortical sites for inducing resetting were the same as those from which the largest short-latency responses were evoked in the contralateral forearm flexor and extensor muscles, i.e. the motor cortex. At the cortical sites where magnetic stimulation did induce resetting, the initial electromyographic (EMG) effects consisted of a short-latency excitation followed by a period of inhibition. This silent period was followed by a short burst of excitation often occurring simultaneously in the wrist flexor and extensor muscles, and only thereafter by the return of rhythmical alternating EMG activity characteristic of the wrist movement. The latency to the first rhythmical EMG peak following the stimulus was closely related to the period of the subject's prestimulus movement.     

Activity of neurons in the lower precentral cortex during voluntary and rhythmical jaw movements in the monkey

Summary The activity of 171 neurons in the lower precentral cortex and superior temporal gyrus were recorded in monkeys making voluntary and semiautomatic rhythmical jaw movements. The discharge pattern of 75% of the precentral neurons was related to the performance of jaw movements and repetitive electrical stimulation of the region containing responsive units evoked coordinated rhythmical masticatory movements. Responsive neurons were divided according to their patterns of discharge.Fifteen neurons discharged preferentially during all types of jaw opening movements. They apparently received a proprioceptive sensory input since they fired when the jaw was opened by the experimenter. Loads which aided jaw opening increased their discharge frequency during opening movements and the maximum discharge frequency was proportional to the maximum displacement of the mandible. It was suggested that these neurons excite jaw opening motoneurons and inhibit jaw closers.Thirty-six neurons fired with a weaker phase relationship to jaw opening, 25 neurons discharged when the jaw was open and 5 neurons discharged during protrusion of the tongue. These neurons may control the many jaw, face and tongue muscles which are not principally responsible for opening or closing the jaw. Sixteen neurons were excited or inhibited throughout a series of movements, but fluctuations in their discharge frequency were not correlated to the phase of movement.Only 4 neurons discharged preferentially during closure under all conditions. Their firing frequency was not affected by loads aiding or opposing closure and did not correlate with the velocity or displacement of the jaw.Thirteen neurons discharged when the teeth were in contact or when apple was crushed between the teeth and probably received a sensory input from the periodontal pressor receptors. It was suggested that this type of neuron could control the tension developed in jaw closing muscles when their contraction is opposed by a resistance between the teeth. However, unopposed closing movements, such as those occurring during rhythmical semiautomatic tasting movements, are probably controlled at the brain stem level.Supported by the Medical Research Council, Canada.Scholar of the Medical Research Council, Canada.Member, Medical Research Council Group in Neurological Sciences.     

Neurophysiological examination of the corticospinal system and voluntary motor control in motor-incomplete human spinal cord injury

This study employed neurophysiological methods to relate the condition of the corticospinal system with the voluntary control of lower-limb muscles in persons with motor-incomplete spinal cord injury. It consisted of two phases. In a group of ten healthy subjects, single and paired transcranial magnetic stimulation (TMS) of the motor cortex was used to study the behavior of the resulting motor evoked potentials (MEP) in lower-limb muscles. Interstimulus intervals (ISIs) of 15–100 ms were examined for augmentation of test MEPs by threshold or subthreshold conditioning stimuli. The second phase of this study examined eight incomplete spinal cord injured (iSCI) subjects, American Spinal Injury Association Impairment Scale C (n =5) and D (n =3) in whom voluntary motor control was quantified using the surface EMG (sEMG) based Voluntary Response Index (VRI). The VRI is calculated to characterize relative output patterns across ten lower-limb muscles recorded during a standard protocol of elementary voluntary motor tasks. VRI components were calculated by comparing the distribution of sEMG in iSCI subjects with prototype patterns collected from 15 healthy subjects using the same rigidly administered protocol, The resulting similarity index (SI) and magnitude values provided the measure of voluntary motor control. Corticospinal system connections were characterized by the thresholds for MEPs in key muscles. Key muscles were those that function as the prime-movers, or agonists for the voluntary movements from which the VRI data were calculated. Results include healthy-subject data that showed significant increases in conditioned MEP responses with paired stimuli of 15–50 ms ISI. Stimulus pairs of 75 and 100 ms showed no increase in MEP peak amplitude over that of the single-pulse conditioning stimulus alone, usually no response. For the iSCI subjects, 42% of the agonists responded to single-pulse TMS and 25% required paired-pulse TMS to produce an MEP. American Spinal Injury Association Impairment Scale component motor scores for agonist muscles, Quadriceps, Tibialis Anterior, and Triceps Surae, were significantly lower where MEPs could not be obtained (p <0.05). VRI values were also significantly lower for motor tasks with agonists that had no resting MEP (p <0.01). Therefore, the presence of a demonstrable connection between the motor cortex and spinal motor neurons in persons with SCI was related to the quality of post-injury voluntary motor control as assessed by the VRI.     

Practice improves even the simplest movements

Summary Three subjects practiced accurate, fast elbow flexions of 54° to a 3° wide target. Movements of 36°, 54° and 72° were then tested. Comparison over the three distances showed that the normally monotonic relationship between movement distance and movement time is alterable by specific training. Subjects learn to go faster over the practiced distance by refining their neural commands to the muscles. The benefits of practice only partially transfer to other distances. We conclude that many of the relationships seen among movement variables in simple tasks are plastic in nature and affected by prior experience.     

Three-dimensional localization of SMA activity preceding voluntary movement

Summary Previous studies by magnetoencephalography (MEG) failed to consistently localize the activity of the supplementary motor area (SMA) prior to voluntary movements in healthy human subjects. Based on the assumption that the SMA of either hemisphere is active prior to volunatry movements, the negative findings of previous studies could be explained by the hypothesis that magnetic fields of current dipole sources in the two SMAs may cancel each other. The present MEG study was performed in a patient with a complete vascular lesion of the right SMA. In this case it was possible to consistently localize a current dipole source in the intact left SMA starting about 1200 msec prior to the initiation of voluntary movements of the right thumb. Starting at about 600 msec prior to movement onset the assumption of a current dipole source in the left primary motor cortex was needed to account for the observed fields. Measurements of brain potentials were consistent with MEG findings of activity of the left SMA starting about 1200 msec prior to movement onset.     

The generation of the efferent command and the importance of joint compliance in fast elbow movements

We describe the effects of changing an elastic or inertial load on the trajectory and EMG patterns during fast, voluntary elbow flexions. These effects depend upon whether the load is known to the subject in advance of the movement or is only determined as the movement is performed. The EMG patterns change in a well-defined manner when the load is known in advance. When the load change is unexpected, the change in the EMG patterns is smaller and later and the effects on the trajectory are greater. In neither case did the loads used here have large effects. We show that joint compliant properties are responsible for minimizing the effects of external load changes on the trajectory. We conclude that there is no evidence for a large contribution by length-sensitive stretch reflexes to this process.     

The effects of practice on movement distance and final position reproduction: implications for the equilibrium-point control of movements

Predictions of two views on single-joint motor control, namely programming of muscle force patterns and equilibrium-point control, were compared with the results of experiments with reproduction of movement distance and final location during fast unidirectional elbow flexions. Two groups of subjects were tested. The first group practiced movements over a fixed distance (36°), starting from seven different initial positions (distance group, DG). The second group practiced movements from the same seven initial positions to a fixed final location (location group, LG). Later, all the subjects were tested at the practiced task with their eyes closed, and then, unexpectedly for the subjects, they were tested at the other, unpracticed task. In both groups, the task to reproduce final position had lower indices of final position variability than the task to reproduce movement distance. Analysis of the linear regression lines between initial position and final position (or movement distance) also demonstrated a better (more accurate) performance during final position reproduction than during distance reproduction. The data are in a good correspondence with the predictions of the equilibrium-point hypothesis, but not with the predictions of the force-pattern control approach.     

Single-Trial Analysis of Cortical Oscillatory Activities During Voluntary Movements Using Empirical Mode Decomposition (EMD)-Based Spatiotemporal Approach

This study presents a method based on empirical mode decomposition (EMD) and a spatial template-based matching approach to extract sensorimotor oscillatory activities from multi-channel magnetoencephalographic (MEG) measurements during right index finger lifting. The longitudinal gradiometer of the sensor unit which presents most prominent SEF was selected on which each single-trial recording was decomposed into a set of intrinsic mode functions (IMFs). The correlation between each IMF of the selected channel and raw data on other channels were created and represented as a spatial map. The sensorimotor-related IMFs with corresponding correlational spatial map exhibiting large values on primary sensorimotor area (SMI) were selected via spatial-template matching process. Trial-specific alpha and beta bands were determined in sensorimotor-related oscillatory activities using a two-spectrum comparison between the spectra obtained from baseline period (−4 to −3 s) and movement-onset period (−0.5 to 0.5 s). Sensorimotor-related oscillatory activities were filtered within the trial-specific frequency bands to resolve task-related oscillatory activities. Results demonstrated that the optimal phase and amplitude information were preserved not only for alpha suppression (event-related desynchronization) and beta rebound (event-related synchronization) but also for profound analysis of subtle dynamics across trials. The retention of high SNR in the extracted oscillatory activities allow various methods of source estimation that can be applied to study the intricate brain dynamics of motor control mechanisms. The present study enables the possibility of investigating cortical pathophysiology of movement disorder on a trial-by-trial basis which also permits an effective alternative for participants or patients who can not endure lengthy procedures or are incapable of sustaining long experiments.     

Independent movements of the digits in grasping

Reaching out for an object is often considered to consist of the control of two components: transporting the hand to the object's position, and scaling the grip to the object's size. We recently proposed an alternative view. According to this view, grasping consists of controlling the digits, not the hypothetical transport and grip. This alternative view assumes that the opening of the hand emerges from the trajectories of the digits. We therefore studied the movements of the digits in grasping. We asked subjects to grasp disks (diameters ranging from 5 to 8 cm) at marked positions with two digits. The positions were at opposite sides of the disk, at the same distance from the starting position, so that the orientation of the surface was the same for both digits. The subjects grasped the disks either with the index finger and thumb of the dominant hand, with the same digits of the non-dominant hand, or bimanually with both index fingers. Our predictions are: that the well-known relation between object size and grip aperture holds for each digit; that the same relation holds if the object is grasped with two hands instead of with the thumb and finger of one hand; that maximum deviation, variability and duration of the digit movements are related; and that variations in the timing of the maximum deviation of one digit are independent of those in the other digit. In accordance with our predictions, we found that the maximum deviation of both digits increased with 0.75 times the object radius, independent of the hand(s) used. The movements of the thumb were more variable than those of the index finger, which was reflected by a larger deviation earlier in the movement. The timing of the maximum deviation of the two digits was independent. These results on the digits' movements are consistent with our view that grasping can be understood as the largely independent movements of the digits. The results are not in conflict with the hypothesis that the grip is controlled during grasping, but can only be explained by extending that hypothesis post hoc. Electronic Publication     

Effects of practice on final position reproduction

Summary Three subjects practiced fast, accurate 36° elbow flexion movements to a 2.5° target for 14 sessions of 100 trials (total, 1400 trials). Subjects then returned for a 15th experimental session in which they were asked to perform 15 movements under identical conditions to the practice condition. They were then tested under three experimental conditions without visual feedback: (1) identical to the practice conditions, (2) with small shifts in starting position (± 3° of the practiced starting position), that were insufficient for subjective discrimination and, therefore, subjects were instructed to repeat the practiced movements; and (3) with a large shift in starting position (range, ± 15° of the practiced starting position), under the instruction to move to the same target. Experimental conditions 2 and 3 demonstrated that shifts in starting position were partially correlated with shifts in final position. These results are interpreted from the point of view of the equilibrium-point hypothesis of motor control.     

Antagonist muscle activation preceding rapid flexion movements of the elbow joint in human subjects

Our study was designed to look for interactions between fast movements and pre-existing voluntary tonic motor activity when both motor acts employ the same muscles. Five normal subjects performed a continuous sequence of two motor tasks about their right elbow joint: A tonic isometric extension (slowly increasing or decreasing) against a force transducer, followed immediately after a "go" tone by a fast isotonic flexion. The position of the lower arm was recorded using a search coil system. Signals (force, position, and surface EMGs of triceps and biceps brachii muscles) were A/D converted and sampled at 1 kHz. A premovement silence in the tonically active triceps muscle (extensor) usually preceded the fast flexion movement if the triceps' tonic force was either constant or decreased slowly. If the tonic triceps activity had been increasing before the fast flexion began, this classical picture disappeared, and the premovement silence was replaced by a phasic premovement excitation. Subjects were unaware of this transient EMG and force increase in the unintended direction. Our results demonstrate unconscious reciprocal interactions between commands governing evolving movements (and tuning the motor system accordingly) and those concerned with ongoing motor acts.     

Role of the sensorimotor cortex in postural adjustments accompanying a conditioned paw lift in the standing cat

Summary The role of the sensorimotor cortex in the postural adjustments associated with conditioned paw lifting movements was investigated in the cat. Cats were trained to stand quietly on four strain gauge equipped platforms and to perform a lift-off movement with one forelimb when a conditioned tone was presented. The parameters recorded were the vertical forces exerted by the paws on each platform, the lateral and antero-posterior displacements of rods implanted on the T2, T12, L5 vertebrae as well as their rotation, and the EMG of triceps and biceps of both forelimbs. Before lesion, the postural adjustment consisted of a nondiagonal pattern where the CG was displaced laterally inside the triangle formed by the three remaining supporting limbs. Here a lateral bending of the thoracic column toward the supporting forelimb could be observed. The associated EMG pattern consisted of an early activation of the triceps lateral head in the moving limb which was probably responsible for the body displacement toward the opposite side, and a late biceps activation associated with the lift. In the supporting forelimb, a coactivation of the biceps and triceps was usually present. After contralateral sensorimotor lesion, the conditioned lifting movements were lost for 4–15 days after the lesion, before being subsequently recovered. The same lateral CG displacement and bending of the back was seen after lesion as before, which indicates that the goal of postural adjustment was preserved. However, the means of reaching it were modified. In most of the intact animals, the CG displacement was achieved in one step, whereas in the animals with lesions, the displacement was made either according to a slow ramp mode or in a discontinuous manner involving several steps. The mechanisms responsible for this disturbance are discussed.     

Multi-compartment model can explain partial transfer of learning within the same limb between unimanual and bimanual reaching

Multi-limb motor skills, such as swimming and rowing, often involve isolated practice of each limb (unimanual) followed by practice with both limbs together (bimanual). We recently demonstrated that learning a novel load during unimanual reaching is partially, but not completely transferred to the same limb during bimanual reaching (and vice versa), learning can remain hidden and only revealed by the original context, and the ability to learn two conflicting force fields if each was separately associated with unimanual and bimanual reaching (Nozaki et al. 2006). The purpose of the present article is to develop a formal state-space model to conceptualize and interpret these complex experimental results. The model contains three separate compartments for learning, a unimanual-specific, a bimanual-specific, and an overlapping compartment, and the internal state of each compartment is updated context-dependently according to motor errors. The model was able to capture all major aspects of motor learning across these two behaviours and predict further complexities during washout trials when bimanual and unimanual trials are interleaved. We propose that partial, but not complete transfer of motor learning is due to a corresponding partial overlap in neural control processes across these behaviours, and is a general feature of different classes of voluntary motor behaviour, such as postural control, point-to-point reaching, manual tracking and oscillatory movements. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex

It is an important issue to address the mode of information processing in the somatic motor circuit linking the frontal cortex and the basal ganglia. In the present study, we investigated the extent to which corticostriatal input zones from the primary motor cortex (MI), the supplementary motor area (SMA), and the premotor cortex (PM) of the macaque monkey might overlap in the putamen. Intracortical microstimulation was performed to map the MI, SMA, and dorsal (PMd) and ventral (PMv) divisions of the PM. Then, two different anterograde tracers were injected separately into somatotopically corresponding regions of two given areas of the MI, SMA, PMd, and PMv. With respect to the PMd and PMv, tracer injections were centered on their forelimb representations. Corticostriatal input zones from hindlimb, forelimb, and orofacial representations of the MI and SMA were, in this order, arranged from dorsal to ventral within the putamen. Dense input zones from the MI were located predominantly in the lateral aspect of the putamen, whereas those from the SMA were in the medial aspect of the putamen. On the other hand, corticostriatal inputs from forelimb representations of the PMd and PMv were distributed mainly in the dorsomedial sector of the putamen. Thus, the corticostriatal input zones from the MI and SMA were considerably segregated though partly overlapped in the mediolateral central aspect of the putamen, while the corticostriatal input zone from the PM largely overlapped that from the SMA, but not from the MI. Received: 30 June 1997 / Accepted: 2 October 1997     

Visual feedback alters the variations in corticospinal excitability that arise from rhythmic movements of the opposite limb

Augmented visual feedback can have a profound bearing on the stability of bimanual coordination. Indeed, this has been used to render tractable the study of patterns of coordination that cannot otherwise be produced in a stable fashion. In previous investigations (Carson et al. 1999), we have shown that rhythmic movements, brought about by the contraction of muscles on one side of the body, lead to phase-locked changes in the excitability of homologous motor pathways of the opposite limb. The present study was conducted to assess whether these changes are influenced by the presence of visual feedback of the moving limb. Eight participants performed rhythmic flexion–extension movements of the left wrist to the beat of a metronome (1.5 Hz). In 50% of trials, visual feedback of wrist displacement was provided in relation to a target amplitude, defined by the mean movement amplitude generated during the immediately preceding no feedback trial. Motor potentials (MEPs) were evoked in the quiescent muscles of the right limb by magnetic stimulation of the left motor cortex. Consistent with our previous observations, MEP amplitudes were modulated during the movement cycle of the opposite limb. The extent of this modulation was, however, smaller in the presence of visual feedback of the moving limb (FCR ²=0.41; ECR ²=0.29) than in trials in which there was no visual feedback (FCR ²=0.51; ECR ²=0.48). In addition, the relationship between the level of FCR activation and the excitability of the homologous corticospinal pathway of the opposite limb was sensitive to the vision condition; the degree of correlation between the two variables was larger when there was no visual feedback of the moving limb. The results of the present study support the view that increases in the stability of bimanual coordination brought about by augmented feedback may be mediated by changes in the crossed modulation of excitability in homologous motor pathways.     

Voluntary Control of Pulse Transmission Time to the Ear

Two experiments involving voluntary control of pulse transmission time (PTT) to the ear were performed. In Experiment I (within-subject, 3 sessions), 12 male subjects attempting to control PTT with feedback showed significant bidirectional PTT changes in the target directions accompanied by parallel changes in pre-ejection period (PEP). There was no evidence of concomitant changes in respiration rate or general somatic activity. PTT control deteriorated across sessions. In Experiment II (between-subjects, 3 sessions), 10 male subjects attempting to decrease PTT with feedback produced significant PTT decreases accompanied by PEP decreases. There was marginal evidence of increases in respiration rate but no changes in general somatic activity in this condition. Five subjects attempting to increase PTT with feedback and 5 subjects attempting bidirectional PTT control without feedback showed no significant changes in PTT or PEP. The results from these experiments indicate that subjects demonstrate a modest degree of control over PTT to the ear when provided with feedback. This control of PTT is accompanied by parallel changes in PEP but is relatively free of somatic and respiratory concomitance.