Participation of the motor cortex in the bimanual unloading task: a study by transcranial magnetic stimulation

Motor potentials of m. biceps brachii evoked by transcranial magnetic stimulation of the contralateral motor cortex have been recorded in postural adjustment during arm unloading in humans. During active unloading, the amplitude of the motor evoked potential decreases simultaneously with the decreasing of the muscle activity. During load keeping, the muscle response changes simultaneously with the load changes. When the other arm has lifted the other load during load keeping, the amplitude of the motor evoked potential decreases in the m. biceps of the keeping arm without muscle activity changes. Passive unloading results in the same changes of the motor evoked potential as active unloading. A possible role of the direct corticospinal volley and the motor command mediated by some subcortical structures in the decrease of the muscle activity preceding active unloading (postural adjustment) is discussed.     

Unitary activity in the cat motor cortex during a conditioned postural adjustment reflex

Unitary activity in the motor cortex (area 4) during a conditioned postural adjustment reflex was investigated in cats. Responses of the overwhelming majority of neurons connected with conditioned-reflex placing movements were activational in type. They consisted of several components and preceded the movements themselves by 50–600 msec. During realization of incorrect responses to presentation of a differential stimulus and of "spontaneous" interstimulus movements, the unitary responses were similar in direction but differed in their lower intensity and, in most cases, they appeared simultaneously with these movements. In the course of extinction both the conditioned-reflex movements and the corresponding unitary responses disappeared simultaneously. The technique of formation of a conditioned postural adjustment reflex suggested in this paper can be used to from natural, well-coordinated forelimb movements in animals in response to conditioned stimulation which are necessary initial components of more complex behavioral motor responses.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 745–753, November–December, 1984.     

Anticipatory activity in primary motor cortex codes memorized movement sequences

Movement sequences, defined both by the component movements and by the serial order in which they are produced, are fundamental building blocks of motor behavior. The serial order of sequence production is strongly encoded in medial motor areas. It is not known to what extent sequences are further elaborated or encoded in primary motor cortex. Here, we describe cells in the primary motor cortex of the monkey that show anticipatory activity exclusively related to a specific memorized sequence of upcoming movements. In addition, the injection of muscimol, a GABA agonist, into motor cortex resulted in an increase in the error rate during sequence production, without concomitant effects on nonsequenced motor performance. Our results challenge the role of medial motor areas in the control of well-practiced movement sequences and suggest that motor cortex contains a complete apparatus for the planning and production of this complex behavior.     

Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination

Single neuronal activity was recorded from the supplementary motor area (SMA-proper and pre-SMA) and primary motor cortex (M1) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated bimanual pull and grasp movements. The behavioural paradigm was designed to distinguish neuronal activity associated with bimanual coordination from that related to a comparable motor sequence but executed unimanually (left or right arm only). The bimanual and unimanual trials were instructed in a random order by a visual cue. Following the cue, there was a waiting period until presentation of a "go-signal", signalling the monkey to perform the instructed movement. A total of 143 task-related neurons were recorded from the SMA (SMA-proper, 62; pre-SMA, 81). Most SMA units (87%) were active in both unimanual contralateral and unimanual ipsilateral trials (bilateral neurons), whereas 9% of units were active only in unimanual contralateral trials and 3% were active only in unimanual ipsilateral trials. Forty-eight per cent of SMA task-related units were classified as bimanual, defined as neurons in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. For direct comparison, 527 neurons were recorded from M1 in the same monkeys performing the same tasks. The comparison showed that M1 contains significantly less bilateral neurons (75%) than the SMA, whereas the reverse was observed for contralateral neurons (22% in M1). The proportion of M1 bimanual cells (53%) was not statistically different from that observed in the SMA. The results suggest that both the SMA and M1 may contribute to the control of sequential bimanual coordinated movements. Interlimb coordination may then take place in a distributed network including at least the SMA and M1, but the contribution of other cortical and subcortical areas such as cingulate motor cortex and basal ganglia remains to be investigated.     

Comparison of postural and motor components in instrumental defense learning in dogs

In 6 dogs, during the period of a complete formation of the "co-ordination" program of defensive reflex associated with maintaining flexion of the left hind-limb, the diagonal pattern of posture readjustment occurred very infrequently. Only during the period of a complete automation of the motor habit, a constant occurrence of the diagonal pattern of posture readjustment was observed in all realisations. These findings suggest that the diagonal pattern of posture readjustment occurs much later than the motor pattern necessary for solving the instrumental task.     

Role of the motor area of the cortex in the performance of the postural escape reaction

It has been shown on three dogs that unilateral ablation of the cortical motor area temporally disturbs previously acquired and opposite to the innate postural escape reaction to electric stimulation of the contralateral forepaw by increasing its pressure on the support. After 3-4 months of repeated training, compensation is possible. Bilateral ablation of the motor cortex elicits stable and unreversible disturbance of the acquired reaction. In reorganization of postural coordinations, motor cortex functions are connected with the inhibition of innate coordinations preventing performance of the reaction.     

Anticipatory postural adjustments in children with hemiplegia and diplegia

Anticipatory postural adjustments (APAs) play an important role in the performance of many activities requiring the maintenance of standing posture. However, little is known about if and how children with cerebral palsy (CP) generate APAs. Two groups of children with CP (hemiplegia and diplegia) and a group of children with typical motor development performed arm flexion and extension movements while standing on a force platform. Electromyographic activity of six trunk and leg muscles and displacement of center of pressure (COP) were recorded. Children with CP were able to generate anticipatory postural adjustments and produce directionally specific APAs and COP displacements similar to those described in adults and typically developing children. However, children with diplegia were unable to generate APAs of the same magnitude as children with typical development and hemiplegia and had higher baseline muscle activity prior to movement. In children with diplegia, COP was posteriorly displaced and peak acceleration was smaller during bilateral extension compared to children with hemiplegia. The outcomes of the study highlight the role of APAs in the control of posture of children with CP and point out the similarities and differences in anticipatory control in children with diplegia and hemiplegia. These differences may foster ideas for treatment strategies to enhance APAs in children with CP.     

Neural integration of movement: role of motor cortex in reaching

The study of the motor cortex in behaving monkeys during the past 20 years has provided important information on the brain mechanisms underlying motor control. With respect to reaching movement in space, a key role of motor cortex in specifying the direction of reaching has been proposed on the basis of results from studies of the activity of cells and cell populations during reaching. These results and ideas are reviewed and discussed in the context of recent findings concerning the spinal mechanisms underlying reaching movements.     

Reevaluating the role of LTD in cerebellar motor learning

Long-term depression at parallel fiber-Purkinje cell synapses (PF-PC LTD) has been proposed to be required for cerebellar motor learning. To date, tests of this hypothesis have sought to interfere with receptors (mGluR1) and enzymes (PKC, PKG, or αCamKII) necessary for induction of PF-PC LTD and thereby determine if cerebellar motor learning is impaired. Here, we tested three mutant mice that target the expression of PF-PC LTD by blocking internalization of AMPA receptors. Using three different cerebellar coordination tasks (adaptation of the vestibulo-ocular reflex, eyeblink conditioning, and locomotion learning on the Erasmus Ladder), we show that there is no motor learning impairment in these mutant mice that lack PF-PC LTD. These findings demonstrate that PF-PC LTD is not essential for cerebellar motor learning.     

Mirror symmetric bimanual movement priming can increase corticomotor excitability and enhance motor learning

Repetitive mirror symmetric bilateral upper limb may be a suitable priming technique for upper limb rehabilitation after stroke. Here we demonstrate neurophysiological and behavioural after-effects in healthy participants after priming with 20 minutes of repetitive active-passive bimanual wrist flexion and extension in a mirror symmetric pattern with respect to the body midline (MIR) compared to an control priming condition with alternating flexion-extension (ALT). Transcranial magnetic stimulation (TMS) indicated that corticomotor excitability (CME) of the passive hemisphere remained elevated compared to baseline for at least 30 minutes after MIR but not ALT, evidenced by an increase in the size of motor evoked potentials in ECR and FCR. Short and long-latency intracortical inhibition (SICI, LICI), short afferent inhibition (SAI) and interhemispheric inhibition (IHI) were also examined using pairs of stimuli. LICI differed between patterns, with less LICI after MIR compared with ALT, and an effect of pattern on IHI, with reduced IHI in passive FCR 15 minutes after MIR compared with ALT and baseline. There was no effect of pattern on SAI or FCR H-reflex. Similarly, SICI remained unchanged after 20 minutes of MIR. We then had participants complete a timed manual dexterity motor learning task with the passive hand during, immediately after, and 24 hours after MIR or control priming. The rate of task completion was faster with MIR priming compared to control conditions. Finally, ECR and FCR MEPs were examined within a pre-movement facilitation paradigm of wrist extension before and after MIR. ECR, but not FCR, MEPs were consistently facilitated before and after MIR, demonstrating no degradation of selective muscle activation. In summary, mirror symmetric active-passive bimanual movement increases CME and can enhance motor learning without degradation of muscle selectivity. These findings rationalise the use of mirror symmetric bimanual movement as a priming modality in post-stroke upper limb rehabilitation.     

Enhancing motor learning by increasing the stability of newly formed dendritic spines in the motor cortex

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Anticipatory postural adjustments during sitting reach movement in post-stroke subjects

The study assessed the effect of velocity of arm movement on anticipatory postural adjustments (APAs) generation in the contralateral and ipsilateral muscles of individuals with stroke in seating. Ten healthy and eight post-stroke subjects were studied in sitting. The task consisted in reaching an object placed at scapular plane and mid-sternum height at self-selected and fast velocities. Electromyography was recorded from anterior deltoid (AD), upper (UT) and lower trapezius (LT) and latissimus dorsi (LD). While kinematic analysis was used to assess peak velocity and trunk displacement. Differences were found between the timing of APAs on ipsi and contralateral LD and LT in both movement speeds and in ipsilateral UT during movement of the non-affected arm at a self-selected velocity. A delay on the contralateral LD to reach movement with the non-affected arm at fast velocity was also observed. The trunk displacement was greater in post-stroke subjects. Individuals with stroke demonstrated a delay of APAs in the muscles on both sides of the body compared to healthy subjects. The delay was observed during performance of the reaching task with the fast and self-selected velocity.     

The role of GABA in human motor learning

GABA modification plays an important role in motor cortical plasticity. We therefore hypothesized that interindividual variation in the responsiveness of the GABA system to modification influences learning capacity in healthy adults. We assessed GABA responsiveness by transcranial direct current stimulation (tDCS), an intervention known to decrease GABA. The magnitude of M1 GABA decrease induced by anodal tDCS correlated positively with both the degree of motor learning and the degree of fMRI signal change within the left M1 during learning. This study therefore suggests that the responsiveness of the GABAergic system to modification may be relevant to short-term motor learning behavior and learning-related brain activity.     

Maximization of learning speed in the motor cortex due to neuronal redundancy

Many redundancies play functional roles in motor control and motor learning. For example, kinematic and muscle redundancies contribute to stabilizing posture and impedance control, respectively. Another redundancy is the number of neurons themselves; there are overwhelmingly more neurons than muscles, and many combinations of neural activation can generate identical muscle activity. The functional roles of this neuronal redundancy remains unknown. Analysis of a redundant neural network model makes it possible to investigate these functional roles while varying the number of model neurons and holding constant the number of output units. Our analysis reveals that learning speed reaches its maximum value if and only if the model includes sufficient neuronal redundancy. This analytical result does not depend on whether the distribution of the preferred direction is uniform or a skewed bimodal, both of which have been reported in neurophysiological studies. Neuronal redundancy maximizes learning speed, even if the neural network model includes recurrent connections, a nonlinear activation function, or nonlinear muscle units. Furthermore, our results do not rely on the shape of the generalization function. The results of this study suggest that one of the functional roles of neuronal redundancy is to maximize learning speed.     

Different motor learning effects on excitability changes of motor cortex in muscle contraction state

Abstract

We aimed to investigate whether motor learning induces different excitability changes in the human motor cortex (M1) between two different muscle contraction states (before voluntary contraction [static] or during voluntary contraction [dynamic]). For the same, using motor evoked potentials (MEPs) obtained by transcranial magnetic stimulation (TMS), we compared excitability changes during these two states after pinch-grip motor skill learning. The participants performed a force output tracking task by pinch grip on a computer screen. TMS was applied prior to the pinch grip (static) and after initiation of voluntary contraction (dynamic). MEPs of the following muscles were recorded: first dorsal interosseous (FDI), thenar muscle (Thenar), flexor carpi radialis (FCR), and extensor carpi radialis (ECR) muscles. During both the states, motor skill training led to significant improvement of motor performance. During the static state, MEPs of the FDI muscle were significantly facilitated after motor learning; however, during the dynamic state, MEPs of the FDI, Thenar, and FCR muscles were significantly decreased. Based on the results of this study, we concluded that excitability changes in the human M1 are differentially influenced during different voluntary contraction states (static and dynamic) after motor learning.     

Specificity of sensorimotor learning and the neural code: Neuronal representations in the primary motor cortex

Human studies show that the learning of a new sensorimotor mapping that requires adaptation to directional errors is local and generalizes poorly to untrained directions. We trained monkeys to learn new visuomotor rotations for only one target in space and recorded neuronal activity in the primary motor cortex before, during and after learning. Similar to humans, the monkeys showed poor transfer of learning to other directions, as observed by behavioral aftereffects for untrained directions. To test for internal representations underlying these changes, we compared two features of neuronal activity before and after learning: changes in firing rates and changes in information content. Specific elevations of firing rate were only observed in a subpopulation of cells in the motor cortex with directional properties corresponding to the locally learned rotation; namely cells only showed plasticity if their preferred direction was near the training one. We applied measures from information theory to probe for learning-related changes in the neuronal code. Single cells conveyed more information about the direction of movement and this specific improvement in encoding was correlated with an increase in the slope of the neurons' tuning curve. Further, the improved information after learning enabled a more accurate reconstruction of movement direction from neuronal populations. Our findings suggest a neural mechanism for the confined generalization of a newly acquired internal model by showing a tight relationship between the locality of learning and the properties of neurons. They also provide direct evidence for improvement in the neural code as a result of learning.     

On the role of anatomy in learning by the cerebellar cortex

The properties due to the location of neurons, synapses, and possibly even synaptic channels, in neuron networks are still unknown. Our preliminary results suggest that not only the interconnections but also the relative positions of the different elements in the network are of importance in the learning process in the cerebellar cortex. We have used neural field equations to investigate the mechanisms of learning in the hierarchical neural network. The numerical resolution of these equations reveals two important properties: (i) The hierarchical structure of this network has the expected effect on learning because the flow of information at the neuronal level is controlled by the heterosynaptic effect through the synaptic density-connectivity function, i.e. the action potential field variable is controlled by the synaptic efficacy field variable at different points of the neuron. (ii) The geometry of the system involves different velocities of propagation along different fibers, i.e. different delays between cells, and thus has a stabilizing effect on the dynamics, allowing the Purkinje output to reach a given value. The field model proposed should be useful in the study of the spatial properties of hierarchical biological systems.     

A specific function of the motor cortex in the reorganization of coordination in motor learning in animals and humans

The findings suggest that a particular function of MCx in motor learning involves suppression of synergies and co-ordination which interferes with acquisition of new motor patterns. Experimental animal models based on inhibition of certain natural synergies or reflexes in the process of learning new co-ordination have been developed where the MCx is responsible for inhibition of natural motor patterns. Following the MCx lesion the natural synergies dominate again and the learned movement cannot be adequately performed. Similar disturbances occur after combined lesions of the premotor and parietal associative cortex or after lesions of the cerebellar nuclei. However, after the associative cortex or cerebellar lesions the recovery of learned co-ordinations is possible. This suggests the inhibition of inappropriate synergies or co-ordination during motor learning is a specific function of the MCx, the latter taking part in organisation of new co-ordination between posture and movement in humans as well.     

Neuron activity in the motor cortex of a cat with inhibition of a conditioned postural change reflex

A study was made of the neuron spike reactions in the primary motor cortex of the cat in the projection zone of the contralateral forelimb with external and internal inhibition of the conditioned reflex for posture change that consisted of shifting the body weight to the forelimb being studied. Spike responses of the neurons to extraneous stimuli and the conditioned signal were determined to a significant degree by the condition of the animal and its habituation to the signal used. In trained animals, the duration of responses to extraneous stimulation was shorter than in the nontrained. With external and internal inhibition, we observed simultaneous disappearance of conditioned reflex movements and the trace spike discharges connected with them. Frequently extraneous stimulations could suppress trace discharges even when learned movement was present. Extraneous stimulations of a different modality inhibited the reflex to different degrees. The change in neuron spike reaction connected with a conditioned reflex change in posture was similar to well-learned local reflex phenomena.A. A. Bogomol'ets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 17, No. 4, pp. 489–500, July–August, 1985.