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Marc H Schieber

Publications and source records attributed to Marc H Schieber.

14 recordsLinked to original sources

Partial reconstruction of muscle activity from a pruned network of diverse motor cortex neurons.

Primary motor cortex (M1) neurons traditionally have been viewed as "upper motor neurons" that directly drive spinal motoneuron pools, particularly during finger movements. We used spike-triggered averages (SpikeTAs) of electromyographic (EMG) activity to select M1 neurons whose spikes signaled the arrival of input in motoneuron pools, and examined the degree of similarity between the activity patterns of these M1 neurons and their target muscles during 12 individuated finger and wrist movements. Neuron-EMG similarity generally was low. Similarity was unrelated to the strength of the SpikeTA effect, to whether the effect was pure versus synchrony, or to the number of muscles influenced by the neuron. Nevertheless, the sum of M1 neuron activity patterns, each weighted by the sign and strength of its SpikeTA effect, could be more similar to the EMG than the average similarity of individual neurons. Significant correlations between the weighted sum of M1 neuron activity patterns and EMG were obtained in six of 17 muscles, but showed R(2) values ranging from only 0.26 to 0.42. These observations suggest that additional factors-including inputs from sources other than M1 and nonlinear summation of inputs to motoneuron pools-also contributed substantially to EMG activity patterns. Furthermore, although each of these M1 neurons produced SpikeTA effects with a significant peak or trough 6-16 ms after the triggering spike, shifting the weighted sum of neuron activity to lead the EMG by 40-60 ms increased their similarity, suggesting that the influence of M1 neurons that produce SpikeTA effects includes substantial synaptic integration that in part may reach the motoneuron pools over less-direct pathways.

Action Potentials↗

Persistent hand motor commands in the amputees' brain.

The loss of a limb leads to sensorimotor modifications that are frequently accompanied by the vivid experience that the missing limb is still present, and that it can be moved at will. Furthermore, amputees can clearly distinguish between phantom movements of the fingers and of more proximal joints, like movements of the elbow. This phenomenon raises the question of whether these specific phantom movement experiences are translated into differentiated activity within the remaining muscles. We recorded stump muscle activity when above-elbow amputees voluntarily moved their phantom limb. Voluntary movements of the phantom hand triggered specific patterns of stump muscle activity, which differed from activity recorded in the same muscle groups during movements of the proximal limb. This result indicates that the brain's motor areas can be differentially activated according to the phantom movement the patient intends to perform, and suggests that hand motor commands are preserved after amputation. To further understand the interaction between central commands and sensory feedback in the perception of phantom movement we also measured stump muscle EMG activity in an amputee experiencing a frozen phantom limb, and in three below-elbow amputees with vivid phantom movements after inducing an ischaemic block. Failed attempts to move the paralysed phantom limb always resulted in the same EMG pattern, no matter what type of phantom movement was attempted, while ischaemic nerve block reduced or eliminated the ability to voluntarily move the phantom limb and produced a dramatic reduction in the amplitude of stump muscle EMG activity. Our data suggest that the experience of phantom hand movement involves the activation of hand motor commands. We propose that preserved hand movement representations re-target the stump muscles to express themselves and that when these representations are voluntarily accessible they can instruct the remaining muscles to move in such a way as if the limb is still there.

Amputation Stumps↗

Serial correlation in lateralized choices of hand and target.

We investigated how lateralized choices of hand and target are influenced by previous behavior. Three monkeys retrieved food pellets following cues indicating the location of available food pellet targets, and the hand that could be used to acquire a target. In pseudo-randomized trials, the monkeys could retrieve food pellet targets only on their right side, only on their left side, or their choice of either right or left side, using only their right hand, only their left hand, or their choice of either hand. We examined separately the patterns of serial correlation in target choices and hand choices. Although individual monkeys showed overall laterality preferences, instead of repeatedly using the preferred hand, we found that the monkeys tended to switch hands in successive trials. This serial correlation in hand choice was stronger and more robust than serial correlation in target choice. Furthermore, the pattern of serial correlation for target choice closely resembled that of serial correlation for hand choice when the animal was allowed to choose both target and hand, but only when the target cue was presented before the hand cue. These results suggest that when cued to choose a hand first, the monkeys tended to make a separate decision as to whether to switch their target choices or not, whereas their decisions to switch hands and targets were linked more tightly if the animal was cued to choose a target first.

Analysis of Variance↗

Interactions between lateralized choices of hand and target.

Few studies have examined interactions between hand preference and target laterality preference when subjects are permitted unrestricted choices of both hand and target at the same time. We therefore trained three monkeys to perform a task in which different types of choices were presented in different trials. In some trials the monkey chose between targets presented simultaneously to the right and left, while being required to use a specific hand. In these trials, the monkeys preferentially chose the target ipsilateral to the required hand. In other trials, the monkey chose between its right or left hand to retrieve a single target presented either on the right or on the left. In these trials, each monkey showed a consistent pattern of hand preference whether the target was presented on the right or left. In still other trials, the monkey chose both which hand to use and which target to retrieve. In these trials, the choices made by each monkey reflected its individual pattern of hand preference, plus a tendency to choose the target ipsilateral to the preferred hand, with little additional evidence of preference for target laterality. These patterns of laterality preference were similar regardless of whether a cue instructing which hand(s) the monkey could use preceded or followed a cue indicating on which side(s) the target(s) would appear. If the monkeys were permitted to use a strategy in which retrieving the target on a given side could increase the amount of food retrieved per trial, however, the choices made were biased strongly by that strategy. We conclude that when lateralized targets are equivalent, lateralized choices are biased primarily by hand preference and secondarily by a preference to retrieve a target ipsilateral to the preferred hand.

Animals↗

A spectrum from pure post-spike effects to synchrony effects in spike-triggered averages of electromyographic activity during skilled finger movements.

During individuated finger movements, a high proportion of synchrony effects was found in spike-triggered averages (SpikeTAs) of rectified electromyographic activity aligned on the spikes discharged by primary motor cortex (M1) neurons. Because synchrony effects can be produced even if the trigger neuron itself provides no direct synaptic connections to motoneurons, such nonoscillatory synchrony effects often are discounted when considering control of motoneuron pools. We therefore examined the distinctions between pure postspike effects and synchrony effects. The criteria usually applied to distinguish pure and synchrony effects-onset latency and peak width-failed to separate the present SpikeTA effects objectively into distinct subpopulations. Synchrony effects generally were larger than pure effects. Many M1 neurons produced pure effects in some muscles while producing synchrony effects in others. M1 neurons producing no effects, only pure effects, only synchrony effects, or both pure and synchrony effects did not fall into different groups based on discharge characteristics during finger movements. Nor were neurons producing different types of SpikeTA effects segregated spatially in M1. These observations suggest that neurons producing pure and synchrony SpikeTA effects come from similar M1 populations. We discuss potential mechanisms that might have produced a continuous spectrum of variation from pure to synchrony effects in the present monkeys. Although synchrony effects cannot be taken as evidence of mono- or disynaptic connections from the recorded neuron to the motoneuron pool, the functional linkages indicated by synchrony effects represent a substantial fraction of M1 input to motoneuron pools during skilled, individuated finger movements.

Action Potentials↗

Human finger independence: limitations due to passive mechanical coupling versus active neuromuscular control.

We studied the extent to which mechanical coupling and neuromuscular control limit finger independence by studying passive and active individuated finger movements in healthy adults. For passive movements, subjects relaxed while each finger was rotated into flexion and extension by a custom-built device. For active movements, subjects moved each finger into flexion and extension while attempting to keep the other, noninstructed fingers still. Active movements were performed through approximately the same joint excursions and at approximately the same speeds as the passive movements. We quantified how mechanical coupling limited finger independence from the passive movements, and quantified how neuromuscular control limited finger independence using an analysis that subtracted the indices obtained in the passive condition from those obtained in the active condition. Finger independence was generally similar during passive and active movements, but showed a trend toward less independence in the middle, ring, and little fingers during active, large-arc movements. Mechanical coupling limited the independence of the index, middle, and ring fingers to the greatest degree, followed by the little finger, and placed only negligible limitations on the independence of the thumb. In contrast, neuromuscular control primarily limited the independence of the ring, and little fingers during large-arc movements, and had minimal effects on the other fingers, especially during small-arc movements. For the movement conditions tested here, mechanical coupling between the fingers appears to be a major factor limiting the complete independence of finger movement.

Adult↗

Motor control: basic units of cortical output?

Observing movement evoked by stimulating a single cortical neuron has proven technically impossible - until now. A new study using intracellular stimulation has revealed that the basic unit of cortical output is not necessarily basic.

Animals↗

Short-term synchronization between motor units in different functional subdivisions of the human flexor digitorum profundus muscle.

The ability to independently move the digits is limited by peripheral as well as central factors. A central limitation to independent finger movements might arise from the inability of the human nervous system to activate motor units (MUs) that exert force on one finger without also activating MUs that exert force on adjacent fingers. Short-term synchronization between MU pairs is thought to be the result of the two motoneurons receiving common input from last-order neuronal projections. The human flexor digitorum profundus (FDP) muscle contains four subdivisions, one for each of the fingers. We hypothesized that the distribution of MU synchrony within and between subdivisions of FDP might parallel the ability to selectively activate different functional subdivisions within FDP, and the ability to flex one digit independently of another. We found that the degree of MU synchrony indeed was not uniform among the different functional subdivisions of FDP; MUs acting on ulnar digits (d5, d4) were more synchronized than MUs acting on radial digits (d2, d3). Furthermore, synchrony was observed between MU pairs where each unit acted on a different digit and was highest when both units of a pair acted on the least-independent digits (d4, d5). This indicates that the CNS does not exert completely independent control over the different functional subdivisions of FDP. The strength of synchrony appears related to the inability to produce completely independent forces or movements with the digits. These observations reflect widespread divergence of last-order inputs within the FDP motoneuron pool, and we suggest that the organization of the CNS drive to this muscle contributes to the limited ability of humans to flex one digit in isolation from other digits.

Action Potentials↗

Hand function: peripheral and central constraints on performance.

The hand is one of the most fascinating and sophisticated biological motor systems. The complex biomechanical and neural architecture of the hand poses challenging questions for understanding the control strategies that underlie the coordination of finger movements and forces required for a wide variety of behavioral tasks, ranging from multidigit grasping to the individuated movements of single digits. Hence, a number of experimental approaches, from studies of finger movement kinematics to the recording of electromyographic and cortical activities, have been used to extend our knowledge of neural control of the hand. Experimental evidence indicates that the simultaneous motion and force of the fingers are characterized by coordination patterns that reduce the number of independent degrees of freedom to be controlled. Peripheral and central constraints in the neuromuscular apparatus have been identified that may in part underlie these coordination patterns, simplifying the control of multi-digit grasping while placing certain limitations on individuation of finger movements. We review this evidence, with a particular emphasis on how these constraints extend through the neuromuscular system from the behavioral aspects of finger movements and forces to the control of the hand from the motor cortex.

Fingers↗

Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract.

We investigated how damage to the motor cortex or corticospinal tract affects the selective activation of finger muscles in humans. We hypothesized that damage relatively restricted to the motor cortex or corticospinal tract would result in unselective muscle activations during an individuated finger movement task. People with pure motor hemiparesis attributed to ischemic cerebrovascular accident were tested. Pure motor hemiparetic and control subjects were studied making flexion/extension and then abduction/adduction finger movements. During the abduction/adduction movements, we recorded muscle activity from 3 intrinsic finger muscles: the abductor pollicis brevis, the first dorsal interosseus, and the abductor digit quinti. Each of these muscles acts as an agonist for only one of the abduction/adduction movements and might therefore be expected to be active in a highly selective manner. Motor cortex or corticospinal tract damage in people with pure motor hemiparesis reduced the selectivity of finger muscle activation during individuated abduction/adduction finger movements, resulting in reduced independence of these movements. Abduction/adduction movements showed a nonsignificant trend toward being less independent than flexion/extension movements in the affected hands of hemiparetic subjects. These changes in the selectivity of muscle activation and the consequent decrease in individuation of movement were correlated with decreased hand function. Our findings imply that, in humans, spared cerebral motor areas and descending pathways that remain might activate finger muscles, but cannot fully compensate for the highly selective control provided by the primary motor cortex and the crossed corticospinal system.

Adult↗

Incomplete functional subdivision of the human multitendoned finger muscle flexor digitorum profundus: an electromyographic study.

The human flexor digitorum profundus (FDP) sends tendons to all 4 fingers. One might assume that this multitendoned muscle consists of 4 discrete neuromuscular compartments each acting on a different finger, but recent anatomical and physiological studies raise the possibility that the human FDP is incompletely subdivided. To investigate the functional organization of the human FDP, we recorded electromyographic (EMG) activity by bipolar fine-wire electrodes simultaneously from 2 or 4 separate intramuscular sites as normal human subjects performed isometric, individuated flexion, and extension of each left-hand digit. Some recordings showed EMG activity during flexion of only one of the 4 fingers, indicating that the human FDP has highly selective core regions that act on single fingers. The majority of recordings, however, showed a large amount of EMG activity during flexion of one finger and lower levels of EMG activity during flexion of an adjacent finger. This lesser EMG activity during flexion of adjacent fingers was unlikely to have resulted from recording motor units in neighboring neuromuscular compartments, and instead suggests incomplete functional subdivision of the human FDP. In addition to the greatest agonist EMG activity during flexion of a given finger, most recordings also showed EMG activity during extension of adjacent fingers, apparently serving to stabilize the given finger against unwanted extension. Paradoxically, the functional organization of the human FDP-with both incomplete functional subdivision and highly selective core regions-may contribute simultaneously to the inability of humans to produce completely independent finger movements, and to the greater ability of humans (compared with macaques) to individuate finger movements.

Adult↗

Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract.

The purpose of this study was to quantify the long-term loss of independent finger movements in humans with lesions relatively restricted to motor cortex or corticospinal tract. We questioned whether damage to the motor cortex or corticospinal tract would permanently affect the ability to move each finger to the same degree or would affect some fingers more than others. People with pure motor hemiparesis due to ischemic cerebrovascular accident were used as our experimental sample. Pure motor hemiparetic and control subjects were tested for their ability to make cyclic flexion/extension movements of each finger independently. We recorded their finger joint motion using an instrumented glove. The fingers of control subjects and of the unaffected hands (ipsilateral to the lesion) of hemiparetic subjects moved relatively independently. The fingers of the affected hands (contralateral to the lesion) of hemiparetic subjects were differentially impaired in their ability to make independent finger movements. The independence of the thumb was normal; the independence of the index finger was slightly impaired, while the independence of the middle, ring, and little fingers was substantially impaired. The differential long-term effects of motor cortical or corticospinal damage on finger independence may result from rehabilitative training emphasizing tasks requiring independent thumb and index movements, and from a greater ability of the spared components of the neuromuscular system to control the thumb independently compared with the other four fingers.

Adult↗

Training and synchrony in the motor system.

Two monkeys trained for >5 years to perform 12 finger and wrist movements had both a greater prevalence of motor cortex neurons with significant effects in spike-triggered averages and a greater ratio of synchrony effects to pure postspike effects than a monkey trained <1 year to perform six movements. By comparison, stimulus-triggered averages were generally similar in all three monkeys, indicating that the increased prevalence of synchrony in spike-triggered averages was a feature of voluntary motor system activity in the monkeys trained for a longer period of time. Synchronization among neurons with relatively direct connections to spinal alpha-motoneuron pools, including motor cortex neurons, may increase as a repertoire of skilled movements is acquired and practiced during long-term training.

Action Potentials↗

Motor cortex and the distributed anatomy of finger movements.

Voluntary movements are thought to be controlled via a well-ordered, spatially discrete, somatotopic map in the primary motor cortex (M1). We examined this hypothesis in monkeys trained to perform visually-cued, individuated flexion and extension movements of each digit and of the wrist. Single neurone recordings in M1 during such finger movements revealed two unexpected features. First, single M1 neurones often discharge during instructed movements of multiple digits. Second, neurones active during any particular instructed movement are distributed widely throughout the same M1 territory as neurones active during any other movement. Reversible, partial inactivation of the M1 hand representation produced by injection of 5-10 microg muscimol at one site impaired the monkeys' ability to perform finger movements, but no relationship was evident between the particular finger movements that were affected and the mediolateral location of the injection site along the central sulcus. Thus each finger movement is represented by activity distributed widely in the M1 upper extremity representation. If not controlled from spatially segregated M1 regions, movements of different fingers might be controlled by groups of spatially scattered but physiologically similar neurones. Cluster analysis of M1 neurones demonstrated a large group that discharged during most finger movements, and a small group that paused during most movements. Distinct functional groups of M1 neurones that might control particular finger movements were identified inconsistently. We therefore hypothesize that M1 neurones are a very diverse network controlling finger movements.

Animals↗