Encoding of motor skill in the corticomuscular system of musicians

How motor skills are stored in the nervous system represents a fundamental question in neuroscience. Although musical motor skills are associated with a variety of adaptations [1-3], it remains unclear how these changes are linked to the known superior motor performance of expert musicians. Here we establish a direct and specific relationship between the functional organization of the corticomuscular system and skilled musical performance. Principal component analysis was used to identify joint correlation patterns in finger movements evoked by transcranial magnetic stimulation over the primary motor cortex while subjects were at rest. Linear combinations of a selected subset of these patterns were used to reconstruct active instrumental playing or grasping movements. Reconstruction quality of instrumental playing was superior in skilled musicians compared to musically untrained subjects, displayed taxonomic specificity for the trained movement repertoire, and correlated with the cumulated long-term training exposure, but not with the recent past training history. In violinists, the reconstruction quality of grasping movements correlated negatively with the long-term training history of violin playing. Our results indicate that experience-dependent motor skills are specifically encoded in the functional organization of the primary motor cortex and its efferent system and are consistent with a model of skill coding by a modular neuronal architecture [4].     

Neural Coding of Finger and Wrist Movements

Previous work (Schieber and Hibbard, 1993) has shown that single motor cortical neurons do not discharge specifically for a particular flexion-extension finger movement but instead are active with movements of different fingers. In addition, neuronal populations active with movements of different fingers overlap extensively in their spatial locations in the motor cortex. These data suggested that control of any finger movement utilizes a distributed population of neurons. In this study we applied the neuronal population vector analysis (Georgopoulos et al., 1983) to these same data to determine (1) whether single cells are tuned in an abstract, three-dimensional (3D) instructed finger and wrist movement space with hand-like geometry and (2) whether the neuronal population encodes specific finger movements. We found that the activity of 132/176 (75%) motor cortical neurons related to finger movements was indeed tuned in this space. Moreover, the population vector computed in this space predicted well the instructed finger movement. Thus, although single neurons may be related to several disparate finger movements, and neurons related to different finger movements are intermingled throughout the hand area of the motor cortex, the neuronal population activity does specify particular finger movements.     

Functional magnetic resonance imaging as a tool for investigating human cortical motor function.

Non-invasive functional magnetic resonance imaging (fMRI) mapping techniques sensitive to the local changes of blood flow, blood volume, and blood oxygenation which accompany neuronal activation have been widely used over the last few years to investigate the functional organization of human cortical motor systems, and specifically of the primary motor cortex. Validation studies have demonstrated a good correspondence between quantitative and topographic aspects of data acquired by fMRI and positron emission tomography. The spatial and temporal resolution affordable by fMRI has allowed to achieve new important information on the distributed representation of hand movements in multiple functional modules, and on the intensity and spatial extent of neural activation in the contralateral and ipsilateral primary motor cortex in relation to parametric and nonparametric aspects of movement and to the degree of handedness. Neural populations with different functional characteristics have been identified in anatomically defined regions, and the temporal aspects of the activation during voluntary movement tracked in different components of the motor system. Finally, this technique has proved useful to deepen our understanding of the neural basis of motor imagery, demonstrating increased activity in the primary motor cortex during mental representation of sequential finger movements.     

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.     

Movement-related cortical potentials preceding sequential and goal-directed finger and arm movements in patients with cerebellar atrophy

To determine the influence of cerebellar involvement on the preparatory state of the cerebral cortex for voluntary movements, we studied the movement-related cortical potentials (Bereitschaftspotential, BP) preceding sequential and goal-directed finger and arm movements in patients with cerebellar atrophy (CA). The first task (paradigm 1) consisted of a sequential finger movement at a self-placed rate of every 3 sec or longer, in which patients and control subjects pushed rapidly 7 keys on a keyboard in a sequence visually predetermined on a screen. The second task (paradigm 2) consisted of a goal-directed self-paced movement with visual feedback on a screen. In both paradigms, control subjects and patients had distinct movement-related cortical potentials, but peak amplitudes (close to movement onset) were reduced in the patient group (paradigm 2), whereas in the overall analysis the mean amplitude 600–800 msec before movement onset (NS1) was larger in the patient group (paradigms 1 and 2). Accordingly, the difference (NS2) between peak amplitude and NS1 was smaller in the patient group (paradigms 1 and 2). Whereas control subjects' peak amplitude (paradigm 2) and NS2 (paradigm 1) were focused at Cz, this topographical differentiation was abolished in the patient group. The onset of the BP was earlier in the patients than in the control subjects (paradigms 1 and 2). Our results suggest that pathways from the cerebellum to the cortex do play a role in generating movement-related cortical potentials. A strong input from the cerebellum seems to be crucial for the generation of a normal motor potential close to the movement onset, reflecting a specific deficit in patients with CA. Patients with CA may try to compensate for their motor deficits by a longer cortical activation preceding voluntary movements (earlier onset of the BP). The increased NS1 could be the result of larger effort, by which patients try to compensate for their motor deficits as well.     

Distinct cortical circuit mechanisms for complex forelimb movement and motor map topography

Cortical motor maps are the basis of voluntary movement, but they have proven difficult to understand in the context of their underlying neuronal circuits. We applied light-based motor mapping of Channelrhodopsin-2 mice to reveal a functional subdivision of the forelimb motor cortex based on the direction of movement evoked by brief (10?ms) pulses. Prolonged trains of electrical or optogenetic stimulation (100-500?ms) targeted to anterior or posterior subregions of motor cortex evoked reproducible complex movements of the forelimb to distinct positions in space. Blocking excitatory cortical synaptic transmission did not abolish basic motor map topography, but the site-specific expression of complex movements was lost. Our data suggest that the topography of?movement maps arises from their segregated output projections, whereas complex movements evoked by prolonged stimulation require intracortical synaptic transmission.     

Control of voluntary movements mediated via propriospinal neurons

Cortico- and rubrospinal tracts play an important role in controlling voluntary movements. Transection of these tracts in different spinal cord layers gives different effects that may be explained by the influence of different spinal cord neuronal networks. The aim of the present work was to study the role of C3/C4 propriospinal system in movement control and processes of motor recovery. It was shown that propriospinal system C3/C4 play crucial role in motor recovery after lesion of cortico- and rubrospinal tracts in C5, whereas ventrally located tracts are important after the same lesion in C2. More over, propriospinal system C3/C4 can mediate the command for some voluntary movements in cats.     

Functional organization of the cortex of the large hemispheres during voluntary movement performance: Age aspect

The method of estimation of the coherence (Coh) function values of EEG rhythmic components disclosed the specific features of functional associations of cortical regions during the performance of voluntary graphic cyclic movements under usual and unusual conditions. A significant increase in the Coh function values of the α-rhythm was observed both in the contralateral hemisphere and the symmetrical central and parietal cortical regions in adult subjects during right-hand movement performance with open eyes (usual conditions); in this case the resulting functional associations included motor zone and cortical regions responsible for visual information analysis and perception. During right- and left-hand movement performance with closed eyes (unusual conditions), the mature-type functional organization had a bilateral character with interrelated activity focused in the frontal regions that clearly demonstrated the function of these structures during formation of new motor programs. The significant changes in cortical mechanisms of voluntary graphic movements were disclosed in young 7- to 8- and 9- to 10-year-old schoolchildren.     

The impact of brain imaging technology on our understanding of motor function and dysfunction

Brain imaging techniques have demonstrated functional specialisation of multiple areas within the motor system. They have also defined the patterns of interactions between these regions during normal motor function and in motor disorders. Functional imaging makes visible the changes in cortical activity that take place over time during motor functions, from the activations a fraction of a second before voluntary action to cortical neuronal plasticity several weeks after injury. Recently, the functional abnormalities underlying various acquired and developmental motor disorders have been described, as well as the effects of therapeutic intervention.     

Motor-cortical interaction in Gilles de la Tourette syndrome

Background

In Gilles de la Tourette syndrome (GTS) increased activation of the primary motor cortex (M1) before and during movement execution followed by increased inhibition after movement termination was reported. The present study aimed at investigating, whether this activation pattern is due to altered functional interaction between motor cortical areas.

Methodology/Principal Findings

10 GTS-patients and 10 control subjects performed a self-paced finger movement task while neuromagnetic brain activity was recorded using Magnetoencephalography (MEG). Cerebro-cerebral coherence as a measure of functional interaction was calculated. During movement preparation and execution coherence between contralateral M1 and supplementary motor area (SMA) was significantly increased at beta-frequency in GTS-patients. After movement termination no significant differences between groups were evident.

Conclusions/Significance

The present data suggest that increased M1 activation in GTS-patients might be due to increased functional interaction between SMA and M1 most likely reflecting a pathophysiological marker of GTS. The data extend previous findings of motor-cortical alterations in GTS by showing that local activation changes are associated with alterations of functional networks between premotor and primary motor areas. Interestingly enough, alterations were evident during preparation and execution of voluntary movements, which implies a general theme of increased motor-cortical interaction in GTS.     

Neuronal mechanisms of motor signal transmission in the thalamic ventrooral nucleus in spasmodic torticollis patients

A microelectrode technique was used to study the neuronal mechanisms of motor signal transmission in the ventrooral internus nucleus (Voi) of the motor thalamus during voluntary and involuntary pathological (dystonic) movements in patients with spasmodic torticollis. Voi cell elements proved highly reactive to various functional (mostly motor) tests. An activity analysis of 55 Voi neurons detected during nine stereotactic operations revealed, first, a difference in neuronal mechanisms of motor signal transmission for voluntary movements that do or do not involve the affected axial muscles of the neck and for passive and abnormal involuntary dystonic movements. Second, a sensory component was found to play a key role in the mechanisms of sensorimotor interactions during voluntary and involuntary dystonic head and neck movements activating the axial muscles of the neck. Third, rhythmic and synchronized activity of Voi neurons was shown to play an important role in motor signal transmission during voluntary and passive movements. The Voi nucleus was directly implicated in the mechanisms of involuntary head movements and tension of the neck muscles in spasmodic torticollis. The results can be used to identify the Voi nucleus of the thalamus during stereotactic neurosurgery in order to select the optimal destruction or stimulation target and to reduce the postoperative effects in spasmodic torticollis patients.     

Covert shift of attention modulates the ongoing neural activity in a reaching area of the macaque dorsomedial visual stream

Background

Attention is used to enhance neural processing of selected parts of a visual scene. It increases neural responses to stimuli near target locations and is usually coupled to eye movements. Covert attention shifts, however, decouple the attentional focus from gaze, allowing to direct the attention to a peripheral location without moving the eyes. We tested whether covert attention shifts modulate ongoing neuronal activity in cortical area V6A, an area that provides a bridge between visual signals and arm-motor control.

Methodology/Principal Findings

We performed single cell recordings from 3 Macaca Fascicularis trained to fixate straight-head, while shifting attention outward to a peripheral cue and inward again to the fixation point. We found that neurons in V6A are influenced by spatial attention. The attentional modulation occurs without gaze shifts and cannot be explained by visual stimulations. Visual, motor, and attentional responses can occur in combination in single neurons.

Conclusions/Significance

This modulation in an area primarily involved in visuo-motor transformation for reaching may form a neural basis for coupling attention to the preparation of reaching movements. Our results show that cortical processes of attention are related not only to eye-movements, as many studies have shown, but also to arm movements, a finding that has been suggested by some previous behavioral findings. Therefore, the widely-held view that spatial attention is tightly intertwined with—and perhaps directly derived from—motor preparatory processes should be extended to a broader spectrum of motor processes than just eye movements.     

Synaptic integration in motoneurons with hyper-excitable dendrites

Motoneurons have extensive dendritic trees that receive the numerous inputs required to produce movement. These dendrites are highly active, containing voltage-sensitive channels that generate persistent inward currents (PICs) that can enhance synaptic input 5-fold or more. However, this enhancement is proportional to the level of activity of monoaminergic inputs from the brainstem that release serotonin and noradrenalin. The higher this activity, the larger the dendritic PIC and the higher the firing rate evoked by a given amount of excitatory synaptic input. This brainstem control of motoneuron input-output gain translates directly into control of system gain of a motor pool and its muscle. Because large dendritic PICs are probably necessary for motoneurons to have sufficient gain to generate large forces, it is possible that descending monoaminergic inputs scale in proportion to voluntary force. Inhibition from sensory inputs has a strong suppressive effect on dendritic PICs: the stronger the inhibition, the smaller the PIC. Thus, local inhibitory inputs within the cord may oppose the descending monoaminergic control of PICs. Most motor behaviors evoke a mixture of excitation and inhibition (e.g., the reciprocal inhibition between antagonists). Therefore, normal joint movements may involve constant adjustment of PIC amplitude.     

Parabolic movement primitives and cortical states: merging optimality with geometric invariance

Previous studies have suggested that several types of rules govern the generation of complex arm movements. One class of rules consists of optimizing an objective function (e.g., maximizing motion smoothness). Another class consists of geometric and kinematic constraints, for instance the coupling between speed and curvature during drawing movements as expressed by the two-thirds power law. It has also been suggested that complex movements are composed of simpler elements or primitives. However, the ability to unify the different rules has remained an open problem. We address this issue by identifying movement paths whose generation according to the two-thirds power law yields maximally smooth trajectories. Using equi-affine differential geometry we derive a mathematical condition which these paths must obey. Among all possible solutions only parabolic paths minimize hand jerk, obey the two-thirds power law and are invariant under equi-affine transformations (which preserve the fit to the two-thirds power law). Affine transformations can be used to generate any parabolic stroke from an arbitrary parabolic template, and a few parabolic strokes may be concatenated to compactly form a complex path. To test the possibility that parabolic elements are used to generate planar movements, we analyze monkeys’ scribbling trajectories. Practiced scribbles are well approximated by long parabolic strokes. Of the motor cortical neurons recorded during scribbling more were related to equi-affine than to Euclidean speed. Unsupervised segmentation of simulta- neously recorded multiple neuron activity yields states related to distinct parabolic elements. We thus suggest that the cortical representation of movements is state-dependent and that parabolic elements are building blocks used by the motor system to generate complex movements.     

Internally generated preactivation of single neurons in human medial frontal cortex predicts volition

Understanding how self-initiated behavior is encoded by neuronal circuits in the human brain remains elusive. We recorded the activity of 1019 neurons while twelve subjects performed self-initiated finger movement. We report progressive neuronal recruitment over ～1500 ms before subjects report making the decision to move. We observed progressive increase or decrease in neuronal firing rate, particularly in the supplementary motor area (SMA), as the reported time of decision was approached. A population of 256 SMA neurons is sufficient to predict in single trials the impending decision to move with accuracy greater than 80% already 700 ms prior to subjects' awareness. Furthermore, we predict, with a precision of a few hundred ms, the actual time point of this voluntary decision to move. We implement a computational model whereby volition emerges once a change in internally generated firing rate of neuronal assemblies crosses a threshold.     

Premotor interneurons in generation of adaptive leg reflexes and voluntary movements in stick insects

We investigated the role of local nonspiking interneurons involved in motor control of legs in the stick insect, Carausius morosus. In a preparation that allowed the animals to perform active leg movements such as adaptive tactile reflexes, proprioceptive reflexes, and walking, we gathered the following results. Almost all tested nonspiking interneurons that provide synaptic drive onto motoneurons of the proximal leg muscles contribute to all of the motor programs underlying tactile reflexes and voluntary leg movements such as walking, searching, and rocking. Most of them are also involved in the generation of proprioceptive reflexes. All motor programs for coactivation, avoidance reflexes, resistance reflexes, and voluntary leg movements result from parallel pathways including nonspiking interneurons that support and others that oppose the motoneuronal activity. The contribution of a single interneuron to the different motor programs is specific: it can be supporting for one motor program but opposing for the other. Even for the same motor program, for example, coactivation, the contribution of an individual interneuron can depend on the stimulus site from where the response is elicited. Our results support the idea that the different motor patterns for adaptive tactile reflexes, resistance reflexes, and voluntary leg movements emerge from a multifunctional neuronal circuit that is reorganized corresponding to the motor behavior performed. The actual motor pattern is then shaped by distributed information processing in parallel supporting and opposing pathways. © 1996 John Wiley & Sons, Inc.     

Are interlimb interactions disturbed in patients with Parkinson’s disease? A study under unloading conditions

During natural human locomotion, neural connections are activated that are typical of regulation of the quadrupedal walking. The interaction between the neural networks generating rhythmic movements of the upper and lower limbs depends on tonic state of each of these networks regulated by motor signals from the brain. Distortion of these signals in patients with Parkinson’s disease (PD) may lead to disruption of the interlimb interactions. We examined the effect of movements of the limbs of one girdle on the parameters of the motor activity of another limb girdle at their joint cyclic movements under the conditions of arm and leg unloading in 17 patients with PD and 16 healthy subjects. We have shown that, in patients, the effect of voluntary and passive movements of arms, as well as the active movement of the distal parts of arms, on the voluntary movement of legs is weak, while in healthy subjects, the effect of arm movements on the parameters of voluntary stepping is significant. The effect of arm movements on the activation of the involuntary stepping by vibrational stimulation of-legs in patients was absent, while in healthy subjects, the motor activity of arms increased the possibility of involuntary rhythmic movements activation. Differences in the effect of leg movements on the rhythmic movements of arms were found in both patients and healthy subjects. The interlimb interaction appeared after drug administration. However, the effect of the drug was not sufficient for the recovery of normal state of the neural networks in patients. In PD patients, neural networks generating stepping rhythm have an increased tonic activity, which prevents the activation and appearance of involuntary rhythmic movements facilitating the effects of arms on legs.     

Mere expectation to move causes attenuation of sensory signals

When a part of the body moves, the sensation evoked by a probe stimulus to that body part is attenuated. Two mechanisms have been proposed to explain this robust and general effect. First, feedforward motor signals may modulate activity evoked by incoming sensory signals. Second, reafferent sensation from body movements may mask the stimulus. Here we delivered probe stimuli to the right index finger just before a cue which instructed subjects to make left or right index finger movements. When left and right cues were equiprobable, we found attenuation for stimuli to the right index finger just before this finger was cued (and subsequently moved). However, there was no attenuation in the right finger just before the left finger was cued. This result suggests that the movement made in response to the cue caused 'postdictive' attenuation of a sensation occurring prior to the cue. In a second experiment, the right cue was more frequent than the left. We now found attenuation in the right index finger even when the left finger was cued and moved. This attenuation linked to a movement that was likely but did not in fact occur, suggests a new expectation-based mechanism, distinct from both feedforward motor signals and postdiction. Our results suggest a new mechanism in motor-sensory interactions in which the motor system tunes the sensory inputs based on expectations about future possible actions that may not, in fact, be implemented.     

The effects of short-term hypoxia on motor cortex excitability and neuromuscular activation.

The effects of acute hypoxia on motor cortex excitability, force production, and voluntary activation were studied using single- and double-pulse transcranial magnetic stimulation techniques in 14 healthy male subjects. Electrical supramaximal stimulations of the right ulnar nerve were performed, and transcranial magnetic stimulations were delivered to the first dorsal interosseus motor cortex area during short-term hypoxic (HX) and normoxic (NX) condition. M waves, voluntary activation, F waves, resting motor threshold (rMT), recruitment curves (100-140% of rMT), and short-interval intracortical inhibition and intracortical facilitation were measured. Moreover, motor-evoked potentials (MEPs) and cortical silent periods were determined during brief isometric maximum right index finger abductions. Hypoxia was induced by breathing a fraction of inspired oxygen of 12% via a face mask. M waves, voluntary activation, and F waves did not differ between NX and HX. The rMT was significantly lower in HX (55.79 +/- 9.40%) than in NX (57.50 +/- 10.48%) (P < 0.01), whereas MEP recruitment curve, short-interval intracortical inhibition, intracortical facilitation, maximum right index finger abduction, and MEPs were unaffected by HX. In contrast, the cortical silent periods in HX (158.21 +/- 33.96 ms) was significantly shortened compared with NX (169.42 +/- 39.69 ms) (P < 0.05). These data demonstrate that acute hypoxia results in increased cortical excitability and suggest that acute hypoxia alters motor cortical ion-channel function and GABAergic transmission.