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PubMed2002

Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study.

To further our understanding of the functional roles of different motor cortical areas, we made a quantitative comparison of the density of corticospinal projections from primary motor cortex (M1) and supplementary motor area (SMA) to spinal motor nuclei supplying hand and finger muscles in four macaque monkeys. We also compared the action of corticospinal outputs excited by electrical stimulation of these two areas on upper limb motoneurons recorded in three anaesthetized macaques. The hand representations of SMA and M1 were first identified using structural magnetic resonance imaging scans and intracortical microstimulation. In the anatomical study we then made focal injections of wheatgerm agglutinin- horseradish peroxidase into these representations, which were subsequently confirmed by analysis of retrograde cortical labelling. Densitometric analysis showed that corticospinal projections from M1 were denser and occupied a greater proportion of the hand muscle motor nuclei than did projections from SMA. In caudal Th1 the densest projections from M1 occupied 81% of this motoneuronal area, compared with only 6% from SMA. In the electrophysiological study, bipolar intracortical stimulation of the hand representation of M1 and SMA evoked direct (D) and indirect (I) corticospinal volleys. Volleys elicited by M1 stimulation had larger amplitudes and faster conduction velocities than those evoked from the SMA. Intracellular recordings were made from 84 contralateral upper limb motoneurons. M1 and SMA stimulation evoked markedly different responses in tested motoneurons: EPSPs were larger and more common from M1 (88% of motoneurons) than from SMA (48%). Some motoneurons (16/84) showed evidence of excitatory postsynaptic potentials mediated by monosynaptic action of the D-wave evoked from M1; these early effects were not observed from the SMA. In most motoneurons (74/84) EPSPs had segmental latencies indicating that they were due to monosynaptic action of the I-wave. The results are consistent with cortico-motoneuronal (CM) connections originating from both SMA and M1 converging upon single motoneurons, but those from M1 are far more numerous and exert stronger excitatory effects than from the SMA. Thus although they may function in parallel, the two CM projections probably make different contributions to upper limb motor control.

Animals↗
PubMed2001

Role of the human motor cortex in rapid motor learning.

Recent studies suggest that the human primary motor cortex (M1) is involved in motor learning, but the nature of that involvement is not clear. Here, learning-related changes in M1 excitability were studied with transcranial magnetic stimulation (TMS) while na subjects practiced either a ballistic or a ramp pinch task to the 0.5-Hz beat of a metronome. Subjects rapidly learned to optimize ballistic contractions as indicated by a significant increase in peak pinch acceleration and peak force after the 60-min practice epoch. The increase in force and acceleration was associated with an increase in motor evoked potential (MEP) amplitude in a muscle involved in the training (flexor policis brevis) but not in a muscle unrelated to the task (abductor digiti minimi). MEPs returned to their baseline amplitude after subjects had acquired the new skill, whereas no practice-induced changes in MEP amplitude were observed after subjects had overlearned the task, or after practicing slow ramp pinches. Since the changes in MEP amplitude were observed only after TMS of M1 but not after direct stimulation of the corticospinal tract, these findings indicate task- and effector-specific involvement of human M1 in rapid motor learning.

Adolescent↗
PubMed1992

Homotopic transplant of fetal cortex to lesioned motor cortex of adult rats. A comportamental and anatomical study.

Previous investigations have shown that the transplant of fetal nervous tissue in adult, formerly injured, brain induces an improvement of the neurological deficits. The process underlying this finding is not yet known. It has been proposed that this process is favourably supported by the reconstruction of the damaged circuitry, replacing the injured neurons with the transplanted fetal cells. In the present study we have investigated the relation between the improvement of the neurological deficits and the anatomical integration of the transplanted neurons within the host brain. The plan of the investigation included two steps: the first step consisted of inducing neurological deficits by kainic acid lesion of the motor cortex and then studying the changes in the motor learning following a homotopic transplant of fetal cortex in the side of the lesion. The second step consisted of studying the anatomical integration of the transplanted cortex with the thalamus of the host. The results showed that the rats with injury of the motor cortex followed by solid transplant of fetal cortex (E 17) had a significantly greater recovery of the motor learning with respect to non-transplanted rats with a lesioned motor cortex. In the same rats, the connections between the transplanted cerebral cortex and the thalamus of the host has been investigated. WGA-HRP solution was injected in the thalamus and both labeled fiber terminals and labeled cells were searched for in the transplants. The results showed that: 1) the host thalamus projects to the transplanted cortex with a lower density than to the host cortex surrounding the transplant; 2) the thalamic projection to the host cortex is topographically organized, whereas the projection to the transplant is arranged in patches without any topographical organization; 3) the transplant does not send a significant projection to the thalamus of the host. In conclusion, the experimental findings demonstrate that the reconstruction of an injured thalamo-cortical circuitry of adult rats transplanting fetal neurons is not possible. The improvement of the functional deficits by the transplant of fetal tissue may be referred to aspecific factors enhancing the functional activity of the host cortex undamaged by the initial injury. The identification of the nature of the hypothesized factors requires further investigation.

Animals↗
PubMed2002

Functional MRI evidence for motor cortex reorganization adjacent to a lesion in a primary motor cortex.

OBJECTIVE: The object of this study was to verify motor cortex reorganization in patients with primary motor cortex injury using functional magnetic resonance imaging. DESIGN: Ten control subjects and two patients with primary motor cortex injury, caused by a traumatic brain injury in patient 1 and meningioma in patient 2, were evaluated. Functional magnetic resonance imaging was performed using the blood oxygenation level-dependent technique at 1.5 T with hand movements. RESULTS: The contralateral primary sensorimotor cortex was activated by unaffected hand movements. However, only the contralateral primary sensory cortex in patient 1 and the premotor area in patient 2 were activated by affected hand movements, which were totally absent in control subjects. CONCLUSION: We believe that the hand motor function of injured primary motor cortex was shifted into the primary sensory cortex in patient 1 and premotor area in patient 2. In conclusion, this finding may reflect a functional reorganization of the motor area in patients with a primary motor cortex injury.

Adult↗
PubMed1996

Projection pattern of single corticocortical fibers from the parietal cortex to the motor cortex.

Arborization of single corticocortical (CC) axons projecting from the parietal cortex to the motor cortex (Mx) was analysed using an intraaxonal staining technique in the cat. Stem axons arising from cell bodies in area 5 ramified repeatedly into numerous terminal branches in the Mx, forming 2-6 patches (0.2-0.8 mm in diameter) separated by a terminal-free gap. Axon terminals were distributed mainly in layers II and III and sparsely in layers V, VI and I. This feature is quite similar to that of thalamocortical axons and other corticocortical fibres. Thus the patchy organization may be a basic input structure for afferents of the Mx and play a role in generation of adequate motor output patterns in the Mx.

Animals↗
PubMed2003

Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles.

We demonstrate that in the macaque monkey there is robust, short-latency facilitation by ventral premotor cortex (area F5) of motor outputs from primary motor cortex (M1) to contralateral intrinsic hand muscles. Experiments were carried out on two adult macaques under light sedation (ketamine plus medetomidine HCl). Facilitation of hand muscle electromyograms (EMG) was tested using arrays of fine intracortical microwires implanted, respectively, in the wrist/digit motor representations of F5 and M1, which were identified by previous mapping with intracortical microstimulation. Single pulses (70-200 microA) delivered to F5 microwires never evoked any EMG responses, but small responses were occasionally seen with double pulses (interval: 3 ms) at high intensity. However, both single- and double-pulse stimulation of F5 could facilitate the EMG responses evoked from M1 by single shocks. The facilitation was large (up to 4-fold with single and 12-fold with double F5 shocks) and occurred with an early onset, with significant effects at intervals of only 1-2 ms between conditioning F5 and test M1 stimuli. A number of possible pathways could be responsible for these effects, although it is argued that the most likely mechanism would be the facilitation, by cortico-cortical inputs from F5, of corticospinal I wave activity evoked from M1. This facilitatory action could be of considerable importance for the coupling of grasp-related neurons in F5 and M1 during visuomotor tasks.

Animals↗
PubMed2004

Is the human primary motor cortex involved in motor imagery?

Participation of the primary motor cortex (M1) in motor imagery was addressed using functional magnetic resonance imaging at 2.0 T and 2 x 2 x 4 mm3 resolution in six right-handed subjects. Paradigms comprised visually cued execution and imagination of a sequential finger-to-thumb opposition task (12 s) contrasted with motor rest and visual imagery (18 s), respectively. Motor execution activated M1 as well as other parts of the motor system including supplementary motor area (SMA) and premotor areas (PM). In contrast, motor imagery did not lead to activations in M1 except for 1/6 subjects but involved SMA and PM bilaterally as well as the anterior intraparietal cortex. Moreover, a region-of-interest analysis revealed a weak initial MRI signal increase in M1 in 4/6 subjects. This novel finding of a transient response reflecting the onset of imagination which does not lead to sustained M1 activation may explain previous contradictory reports.

Adult↗
PubMed2002

Timing of bimanual movements in human and non-human primates in relation to neuronal activity in primary motor cortex and supplementary motor area.

This study investigates the timing of bimanual movements in a combined behavioral and physiological approach. Human subjects and rhesus monkeys performed the same bimanual task. In monkeys, we simultaneously recorded neuronal activity in the two hemispheres of primary motor cortex (MI) or supplementary motor area (SMA), and related it to bimanual coordination in the temporal domain. Both for monkeys and humans, the reaction times of bimanual movements never significantly exceeded the reaction times of the slower arm in unimanual movements. Consistent with this, the longest delay between neural activity onset in SMA and MI and movement initiation was observed in unimanual movements of the slower arm and not in bimanual movements. Both results suggest that the programming of bimanual movements does not require more processing time than unimanual movements. They are also consistent with the view that bimanual movements are programmed in a single process, rather than by combining two separate unimanual movement plans. In both humans and monkeys, movement initiation was highly correlated between the arms. However, once movements began, the temporal correlation between the arms progressively declined. Movement decorrelation was accompanied by a net decorrelation of neuronal population activity in MI and SMA, suggesting a functional connection between neuronal interactions and the level of bimanual coupling and decoupling. The similarity of neuronal activities in MI and SMA in relationship to behavioral timing lends support to the idea that both areas are involved in the temporal coordination of the arms.

Adult↗
PubMed1995

Functional MRI evidence for adult motor cortex plasticity during motor skill learning.

Performance of complex motor tasks, such as rapid sequences of finger movements, can be improved in terms of speed and accuracy over several weeks by daily practice sessions. This improvement does not generalize to a matched sequence of identical component movements, nor to the contralateral hand. Here we report a study of the neural changes underlying this learning using functional magnetic resonance imaging (MRI) of local blood oxygenation level-dependent (BOLD) signals evoked in primary motor cortex (M1). Before training, a comparable extent of M1 was activated by both sequences. However, two ordering effects were observed: repeating a sequence within a brief time window initially resulted in a smaller area of activation (habituation), but later in larger area of activation (enhancement), suggesting a switch in M1 processing mode within the first session (fast learning). By week 4 of training, concurrent with asymptotic performance, the extent of cortex activated by the practised sequence enlarged compared with the unpractised sequence, irrespective of order (slow learning). These changes persisted for several months. The results suggest a slowly evolving, long-term, experience-dependent reorganization of the adult M1, which may underlie the acquisition and retention of the motor skill.

Adult↗
PubMed1991

Transcranial stimulation of motor cortex in upper motor neurone syndrome: its relation to the motor deficit.

The purpose of this investigation was to clarify the functional significance of the fastest cortico-motoneuronal connections in chronic upper motor neurone syndromes. Using magneto-electrical stimulation of motor cortex the intactness of cortico-motoneuronal connections was assessed in 51 patients presenting with variable degrees of impairment. There was a gross correlation between clinical impairment of the patient and the degree of pathology of cortico-motoneuronal efferents. Covariation of clinical data with transcranial stimulation was better than covariation with the size of lesion on CT scans. In some patients, however, definite clinical impairment, especially affecting distal fractionated movements, was associated with completely normal responses. There was no evidence of response abnormality in distal muscles ipsilateral to the hemispheric lesion. The data indicate that motor deficit can exist in the presence of normal cortico-motoneuronal conduction times, showing that intactness of these connections is not a sufficient condition for preservation of voluntary motor activities. This underlines the importance of other pathways for the pathogenesis of upper motor neurone syndromes.

Adult↗
PubMed2005

Modulation of motor cortex excitability by sustained peripheral stimulation: the interaction between the motor cortex and the cerebellum.

The excitability of cortical neurons in the motor cortex is determined by their membrane potential and by the level of intracortical inhibition. The excitability of the motor cortex as a whole is a function of single cell excitability, synaptic strength, and the balance between excitatory cells and inhibitory cells. It is now established that a sustained period of somatosensory stimulation increases the excitability of motor cortex areas controlling muscles in those body parts that received the stimulation prior to excitability testing. So far, it has been supposed that the sensorimotor cortex was the anatomical substrate of these excitability changes, which could represent an early change in cortical network function before structural plasticity occurs. Recent experimental studies highlight that the cerebellum, especially the interpositus nucleus, plays a key role in the adaptation of the motor cortex to repeated trains of stimulation. Interpositus neurons, which receive inputs from both sensorimotor cortex and the spinal cord, are involved in somesthetic reflex behaviors and assist the cerebral cortex in transforming sensory signals to motor-oriented commands by acting via the cerebello-thalamo-cortical projections. Moreover, climbing fibers originating in the inferior olivary complex and innervating the nucleus interpositus mediate highly integrated sensorimotor information derived from spinal modules. It appears that the interpositus nucleus is a main subcortical modulator of the excitability changes occurring in the motor cortex, which may be a substrate of early plasticity effective in motor learning and recovery from lesion.

Afferent Pathways↗
PubMed1998

Primary motor cortex isolation: complete paralysis with preserved primary motor cortex.

We present a left-sided hemiplegic patient with a cerebrovascular lesion involving the medial part of the right frontal and parietal lobes and the corpus callosum, but sparing the hand area of right primary motor cortex (M1). Several studies using transcranial magnetic stimulation demonstrated functional integrity of the efferent pathways from the right M1, intact sensory afferents to M1, an impairment of transcallosal connection between the bilateral motor cortices, and reduced ipsilateral cortico-cortical inhibition within the right M1. Based on these results, we conclude that the paralysis of this patient was caused by disconnection of the intact M1 from any structures requisite for initiation of movements. The present patient also suggests the importance of various afferents to M1 in voluntary movement. We propose a term of 'primary motor cortex isolation' to designate the paralysis reported here.

Electromyography↗
PubMed2001

On somatotopic representation centers for finger movements in human primary motor cortex and supplementary motor area.

We used functional magnetic resonance imaging to examine the representation pattern for repetitive voluntary finger movements in the primary motor cortex (M1) and the supplementary motor area (SMA) of humans. Healthy right-handed participants performed repetitive individuated flexion-extension movements of digits 1, 2, and 3 using the dominant hand. Contralateral functional labeling for the group indicated a largely overlapping activation pattern in M1 and SMA for the three digits. Consistent with recent findings, the geographic activation center in M1 for each finger differed, and we found some evidence of a homunculus organization pattern in M1 and SMA, but only for the central location of the representations. However, the statistical power for the homunculus pattern was weak, and the distance separating the digit geographical centers was typically less than 15% of the entire extent of digit representations in M1 or SMA. While separations for digit representations occurred, the entire data set provided more support for the concept of distributed, overlapping representations than for a classic homunculus organization for voluntary finger movements.

Adult↗
PubMed1993

Both primary motor cortex and supplementary motor area play an important role in complex finger movement.

In order to clarify the roles played by the primary motor cortex and the supplementary motor area in the execution of complex sequential and simple repetitive finger movements, regional cerebral blood flow (rCBF) was measured with PET using 15O-labelled water in five normal subjects. The PET data of each individual subject co-registered to his own MRI, was analysed. Compared with the resting condition, the mean rCBF was markedly increased in the contralateral sensorimotor cortex (M1-S1) and moderately increased in the contralateral cingulate gyrus and putamen in both the simple and complex motor tasks. During the complex motor task, in addition to the above, the mean rCBF was markedly increased in the supplementary motor area and the contralateral premotor area, and moderately increased in the ipsilateral M1-S1 and cerebellum. In the supplementary motor area, there was a moderate rCBF increase also during the simple task. However, comparison of the mean rCBF increase against the resting condition between the two tasks revealed a greater increase during the complex task than in the other only in the supplementary motor area and the ipsilateral M1-S1. Thus, in agreement with our previous electrophysiological findings, not only the supplementary motor area but also the M1-S1 seems to play an important role in the execution of complex sequential finger movements.

Adult↗
PubMed2005

Organization of multisynaptic inputs from prefrontal cortex to primary motor cortex as revealed by retrograde transneuronal transport of rabies virus.

The organization of multisynaptic projections from the prefrontal cortex to the primary motor cortex (MI) was examined in macaque monkeys by retrograde transneuronal transport of rabies virus. In the first series of experiments, the virus was injected into the MI forelimb region, and the time-dependent distribution patterns of transsynaptic labeling were analyzed in the frontal lobe with various survivals (2-4 d). Two days after the viral injection, neuronal labeling emerged in the caudal aspects of the nonprimary motor-related areas that are known to project to the MI directly. At the same time, the motor thalamus contained labeled neurons. On the third day, cortical labeling extended into the rostral motor-related areas and, also, prearcuate area 8. Moreover, a number of labeled neurons were located in the internal pallidum and the cerebellar nuclei. At the 4 d postinjection period, neuronal labeling occurred widely in prefrontal areas as well as in the putamen and the cerebellar cortex. In the second series of experiments, the viral injection was made into the MI hindlimb region, and the distribution pattern of prefrontal labeling on the fourth day was compared with that in the forelimb-injection case. The labeled neurons in each prefrontal area were much fewer in the hindlimb-injection case than in the forelimb-injection case. Whereas ventral area 46 was most densely labeled from the forelimb region, only sparse labeling from the hindlimb region was observed in this prefrontal area. The present results suggest the importance of ventral area 46 in the cognitive control of forelimb movements.

Animals↗
PubMed2000

Is there an optimal age for recovery from motor cortex lesions? II. behavioural and anatomical consequences of unilateral motor cortex lesions in perinatal, infant, and adult rats.

Purpose: The purpose of this study was to compare the behavioural and anatomical effects of unilateral motor cortex ablation in neonatal, infant, and adult rats. Methods: Rats were given unilateral lesions of the motor cortex on the day of birth (P1), at ten days of age (P10), or in adulthood. They were trained on several motor tasks (skilled forelimb reaching, beam traversing, tongue extension), general motor activity, and a test of spatial learning (Morris water task). Results: Although all lesion groups were equally impaired at skilled reaching with the forelimb contralateral to the lesion, rats with P1 lesions also were impaired at traversing a narrow beam and at learning the Morris task. Gross anatomical analyses revealed that the P1 rats had smaller brains than the other groups, a result that may account for the larger behavioural deficits in the P1 group. Analysis of Golgi-Cox stained neurons showed that relative to control groups, all lesion groups showed an increase in dendritic length in the basilar dendrites of layer III pyramidal cells and, paradoxically a decrease in length of the apical dendrites of the same cells. Conclusions: The bilateral alterations in dendritic organization following the motor cortex lesions suggest that there has been a bilateral reor-ganization of intrinsic cortical connectivity following motor cortex lesions at any age. These alterations in connectivity are likely not identical in the young and adult animals, however, because relative to controls, both the young operated groups, but not the adult group, showed a bilat-eral drop in spine density in the basilar dendrites of layer V pyramidal cells. These findings are discussed with respect to the idea that there may be critical ages in development in which animals can use anatomical modifications to compensate for deficits produced by cortical injury.

Journal Article↗
PubMed1988

Maturation of corticospinal tracts assessed by electromagnetic stimulation of the motor cortex.

The motor cortex can be excited in adults using electromagnetic stimulation, and the latency to the evoked muscle action potential allows an assessment of the integrity of corticospinal tracts. We applied this technique in children to describe the maturation of corticospinal tracts. The latency from cortical stimulation to the onset of the evoked muscle action potentials and the subject's height were recorded. The subject's height was divided by the latency to the onset of the evoked muscle action potential to provide an index of the conduction velocity within descending motor pathways (VI). It is possible to evoke muscle action potentials after electromagnetic stimulation of the motor cortex in children including preterm babies and there is a stepwise increase in the sensitivity to stimulation between 8 and 11 years of age. In addition there is a progressive increase in VI with age; adult values are attained at about 11 years. The successful application of this technique in children suggests that electromagnetic stimulation of the motor cortex has the potential to allow detection of abnormality in motor pathways in newborn babies and young children.

Adolescent↗