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Metabolic mapping of sensorimotor integration in the human brain.

Studies of regional cerebral flow and regional cerebral oxidative metabolism have revealed that humans have three major cortical motor areas: the premotor, supplementary motor and primary motor areas. The premotor area participates in organizing non-routine voluntary movements, especially those carried out contingent to or dependent on sensory information. The supplementary motor area participates in the planning of all motor subroutines. The primary motor area is the executive locus for voluntary movements. Subcortically the caudate nucleus, putamen, globus pallidus, parasagittal cerebellum and ventral thalamus are the main structures which increase their metabolism during voluntary movements of the upper limbs. All these cortical and subcortical structures except the primary motor area are bilaterally activated even during strictly unilateral movements of the upper limbs. However, recent studies of oxidative metabolism show that the caudate nucleus, putamen and lateral cerebellum also participate in cognitive functions and non-motor learning. Before any specific brain work is executed, voluntary movements included, the brain tunes and prepares cortical fields measuring a few square centimetres in the areas that are supposed to participate in information transmission. The superior prefrontal cortex has a special role in this recruitment of cortical fields. Depending on the information needed to execute the voluntary movements, cortical fields are activated in the anterior parietal lobe and the dysgranular frontal cortex.

Brain↗

Cerebellar long-term depression might normalize excitation of Purkinje cells: a hypothesis.

Long-term depression (LTD) of parallel-fibre (PF) synapses on Purkinje cells is usually interpreted in the context of a specific theory of motor learning by the cerebellum proposed by Marr, Albus and Ito. Several arguments suggest that this theory might be false. A new hypothesis about the role of cerebellar LTD proposes that, under physiological conditions, LTD is autoinduced by PF inputs. This proposal is based on the capacity of PF inputs to trigger influx of Ca2+ into the dendrite. Long-term depression and other forms of Purkinje-cell synaptic plasticity are part of a local negative feedback loop that prevents overstimulation of Purkinje cells by PF inputs. This theory explains why it is difficult to induce LTD when a normal level of inhibition is present, and why inhibitory inputs are potentiated by the same conditions that can induce LTD of PF synapses.

Animals↗

[Experimental research and new concepts of the role of the cerebellum].

It has been discovered recently--especially thanks to the experimental research on animals--that cerebellum is not only a co-ordinator of the motor functions but that it also participates in the higher functions of the central nervous system. In this research, models with genetically determined cerebellar degeneration (Lurcher, pcd. staggerer, hot-foot, weaver) or originally healthy animals after partial or complete artificial destruction of cerebellum are often used. The animals can be tested by specific methods of motor learning (rotating steel grid, rotorod, round wooden beam, bridge, coat-hanger, horizontal crossbar, vertical and inclined grid, ladder), spatial learning (Morris water maze, radial maze, hole board) and discriminative learning-type of passive avoidance (step through and step down). The experiments result in conclusion that an injury or degeneration of the cerebellum are associated with worse motor skills and cognitive functions. Nevertheless, the disorders of cerebellum do not prevent from motor learning completely: motor possibilities of Lurcher and hot-foot mutants can be improved by training in spite of the fact that they never reach the same level of motor abilities of healthy controls. Drug therapy of cerebellar degeneration and substitution of lost cells by transplantation are in the phase of new experiments.

Animals↗

Brain mechanisms for the formation of new movements during learning: the evolution of classical concepts.

Current concepts hold that the role of the motor cortex is limited to the control of the appropriate motoneurons on the "point-to-point" principle during the performance of specialized movements of the distal parts of the limbs. However, the last decade has seen the appearance of many data on the plasticity of the motor cortex and its active participation in the process of motor learning. Expression of fos genes has been observed in the motor cortex during the formation of specialized movements. Increases in intracortical horizontal connections in layers II-III during learning fine movements has been seen. The cholinergic input to layers II-III of the motor cortex plays a significant role in this. At the same time, data obtained by functional brain mapping have provided evidence that the activity of the motor cortex also increases during the practice of previously learned movements. This raises the question of the specific function of the motor cortex in the process of motor learning. During the formation of new movements during motor training, a number of previously used synergies interfere with the performance of newly formed coordinations and must be inhibited. The central mechanisms of interference of coordinations in humans have only just started to receive study. At the same time, there is an experimental model for the reorganization and inhibition of interfering synergies in animals. Reorganization of coordinations and inhibition of synergies interfering with the performance of a new movement have been shown to be a specific function of the motor area of the cortex. Cortical control persists during the automation of these synergies, which is not the case in other types of learned movements, though this in itself does not mean that conscious control of their performance also persists.

Animals↗

Impaired motor learning and diffuse axonal damage in motor and visual systems of the rat following traumatic brain injury.

Cognitive-motor functioning or motor skill learning is impaired in humans following traumatic brain injury. A more complete understanding of the mechanisms involved in disorders of motor skill learning is essential for any effective rehabilitation. The specific goals of this study were to examine motor learning disorders, and their relationship to pathological changes in adult rats with mild to moderate closed head injury. Motor learning deficits were determined by comparing the ability to complete a series of complex motor learning tasks with simple motor activity. The extent of neuronal damage was determined using silver impregnation. At all post-injury time points (day 1 to day 14), statistically significant deficits were observed in parallel bar traversing, foot placing, ladder climbing, and rope climbing. Performance improved with time, but never reached control levels. In contrast, no deficits were found in simple motor activity skills tested with beam balance and runway traverse. Histologically, axonal degeneration was widely distributed in several brain areas that relate to motor learning, including the white matter of sensorimotor cortex, corpus callosum, striatum, thalamus and cerebellum. Additionally, severely damaged axons were observed in the primary visual pathway, including the optic chiasm, optic tract, lateral geniculate nuclei, and superior colliculus. These findings suggest that motor learning deficits could be detected in mild or moderate brain injury, and this deficit could be attributed to a diffuse axonal injury distributed both in the motor and the visual systems.

Animals↗

Sleep forms memory for finger skills.

Practicing a motor skill triggers a process of memory consolidation that continues for hours after practice has ended, and becomes manifest in an improved skill at later testing. We used a sequential motor task (finger-to-thumb opposition task) to show that, in humans, the formation of motor skill memories essentially benefits from sleep. Independent of whether placed during daytime or nighttime, sleep after practice enhanced speed of sequence performance on average by 33.5% and reduced error rate by 30.1% as compared with corresponding intervals of wakefulness. The effect of sleep after learning proved to be stable when retesting was postponed for another night, to exclude effects of sleep loss and to assure that all subjects had sufficient sleep before retrieval testing. Also, the consolidating effect of sleep was specific for the motor sequence learned. It did not generalize to a similar sequence containing identical movement segments in a different order. Retention periods of wakefulness improved performance only moderately and only if placed during daytime. The observations demonstrate a critical role of sleep for storing and optimizing motor skills.

Adolescent↗

Disrupted motor learning and long-term synaptic plasticity in mice lacking NMDAR1 in the striatum.

Much research has implicated the striatum in motor learning, but the underlying mechanisms have not been identified. Although NMDA receptor (NMDAR)-dependent long-term potentiation has been observed in the striatum, its involvement in motor learning remains unclear. To examine the role of striatal NMDAR in motor learning, we created striatum-specific NMDAR1 subunit knockout mice, analyzed the striatal anatomy and neuronal morphology of these mice, evaluated their performance on well established motor tasks, and performed electrophysiological recordings to assay striatal NMDAR function and long-term synaptic plasticity. Our results show that deleting the NMDAR1 subunit of the NMDAR specifically in the striatum, which virtually abolished NMDAR-mediated currents, resulted in only small changes in striatal neuronal morphology but severely impaired motor learning and disrupted dorsal striatal long-term potentiation and ventral striatal long-term depression.

Animals↗

[Neural basis of learning new movements: evolution of classical concepts].

According to classical consepts, the role of the motor cortex in performance of skilled movements of distal parts of extremities is confined to control of appropriate motoneurons by the "point-to-point" principle. However, much evidence of plasticity of the motor cortex and its active role in motor learning appeared in last decade. Fos-gene expression in the motor cortex was found to accompany learning a skill. Strengthening of horizontal pathways in layers II-III was revealed, and cholinergic input to tese layers was found to be important. The imaging data show that activity of the motor cortex increases during motor practice as well. This raises the question of specificity of the motor cortex in the motor learning per se. During acquisition of new movements some previously used synergies prevent the necessary coordination from being learned, so they must be suppressed in the process of motor learning. Investigations of central mechanisms of coordination interference in humans are still at the beginning. However, there are some animal models of reorganization and suppression of interfering synergies. The reorganization and suppression of coordination preventing realization of a new movement is shown to be a specific function of the motor cortex. After automation of new synergies the cortical control is still present, as distinct from the learned movements, which do not require suppression of interfering synergies. However, it does not mean that the conscious control of the performance is still present.

Brain↗

Specific functions of the motor cortex in reorganizing coordinations during motor training in animals and humans.

The involvement of the motor cortex in learning movements has recently attracted much attention. One aspect of motor learning is the inhibition of innate synergies which interfere with performance of the acquired movement. Various models of operant responses in dogs have demonstrated the critical role of the motor cortex in the reorganization and inhibition of interfering synergies during learning. The role of the motor cortex and corticospinal influences in the formation of new coordinations in humans was studied here in patients with organic lesions of the cerebral circulation involving the internal capsule, using postural coordination and movements in a bimanual unloading response as an example. Formation of the forearm stabilization response was deeply lesioned on the afflicted side. Some degree of impairment was also seen on the ipsilateral side, but it was no different from the level of learning impairment in patients with lesions not involving the internal capsule or in patients with parkinsonism. The existence of specific contralateral influences of the motor cortex and non-specific descending influences on the process of motor learning is proposed.

Aged↗

Multiple motor learning experiences enhance motor adaptability.

Traditional motor learning theory emphasizes that skill learning is specific to the context and task performed. Recent data suggest, however, that subjects exposed to a variety of motor learning paradigms may be able to acquire general, transferable knowledge about skill learning processes. I tested this idea by having subjects learn five different motor tasks, three that were similar to each other and two that were not related. A group of experimental subjects first performed a joystick-aiming task requiring adaptation to three different visuomotor rotations, with a return to the null conditions between each exposure. They then performed the same joystick-aiming task but had to adapt to a change in display gain instead of rotation. Lastly, the subjects used the joystick-aiming task to learn a repeating sequence of movements. Two groups of control subjects performed the same number of trials, but learned only the gain change or the movement sequence. Experimental subjects showed generalization of learning across the three visuomotor rotations. Experimental subjects also exhibited transfer of learning ability to the gain change and the movement sequence, resulting in faster learning than that seen in the control subjects. However, transient perturbations affected the movements of the experimental subjects to a greater extent than those of the control subjects. These data demonstrate that humans can acquire a general enhancement in motor skill learning capacity through experience, but it comes with a cost. Although movement becomes more adaptable following multiple learning experiences, it also becomes less stable to external perturbation.

Adaptation, Physiological↗

Motor timing learned without motor training.

Improvements due to perceptual training are often specific to the trained task and do not generalize to similar perceptual tasks. Surprisingly, given this history of highly constrained, context-specific perceptual learning, we found that training on a perceptual task showed significant transfer to a motor task. This result provides evidence for a common neural architecture underlying analysis of sensory input and control of motor output, and suggests a potential role for perception in motor development and rehabilitation.

Adult↗

Impairment of LTD and cerebellar learning by Purkinje cell-specific ablation of cGMP-dependent protein kinase I.

The molecular basis for cerebellar plasticity and motor learning remains controversial. Cerebellar Purkinje cells (PCs) contain a high concentration of cGMP-dependent protein kinase type I (cGKI). To investigate the function of cGKI in long-term depression (LTD) and cerebellar learning, we have generated conditional knockout mice lacking cGKI selectively in PCs. These cGKI mutants had a normal cerebellar morphology and intact synaptic calcium signaling, but strongly reduced LTD. Interestingly, no defects in general behavior and motor performance could be detected in the LTD-deficient mice, but the mutants exhibited an impaired adaptation of the vestibulo-ocular reflex (VOR). These results indicate that cGKI in PCs is dispensable for general motor coordination, but that it is required for cerebellar LTD and specific forms of motor learning, namely the adaptation of the VOR.

Adaptation, Physiological↗

Effect of practice on performance of a skilled motor task in patients with Parkinson's disease.

Parkinson's disease leads to a breakdown in the execution of highly practised, skilled movements such as walking and handwriting. The improved execution of skilled movements with practice can be understood as a process of schema learning, the determining of the relevant parameters of the specific movement. The ability of patients with Parkinson's disease and age matched normal control subjects to improve their performance, with practice, on a skilled motor task, doing up buttons, was assessed. The task was assessed on its own and with simultaneous foot tapping. Both groups showed an initial improvement in the task on its own and deterioration in performance when buttoning with foot tapping. The amount of interference, however, decreased with practice, particularly in the patients with a 2 Hz tapping rate. The results suggest that patients with Parkinson's disease are capable of schema learning but require more practice than control subjects to achieve comparable levels of performance. This may be a reflection of the fundamental motor dysfunction of the disease rather than a specific learning deficit.

Adult↗

Motor control problems in patients with spinal pain: a new direction for therapeutic exercise.

Recent research into muscle dysfunction in patients with low back pain has led to discoveries of impairments in deep muscles of the trunk and back. These muscles have a functional role in enhancing spinal segmental support and control. The muscle impairments are not those of strength but rather problems in motor control. These findings call for a different approach in therapeutic exercise, namely a motor learning exercise protocol. The specific exercise approach has an initial focus on retraining the cocontraction of the deep muscles (ie, the transversus abdominis and lumbar multi-fidus Initial clinical trials point to the effectiveness of the approach in patients with both acute and chronic low back pain in terms of reducing the neuromuscular impairment and in control of pain.

Exercise Therapy↗

Learning surgical technical skills.

Training issues raised by the recent introduction of laparoscopic surgical techniques led to this analysis of motor-skill learning principles as they apply specifically to the learning of technical surgical skills. The most accepted theories of motor-skill learning are presented, not as opposing views, but as complementary constructs. The behaviourist school of thought's main contribution is the executive routine or knowledge of the steps of a procedure. Schmidt's schema theory and MacKay's node theory suggest that perceptual information may play an important role in the quality of the performance. The conclusions reached from neuropsychologic testing experiments on surgeons are that visuospatial perceptual skills (the ability to represent mentally the physical environment and the movement to be performed) are the major determinants of surgical technical performance. Learners should make use of learning strategies that improve mental representation of a skill and the corresponding anatomy. Specific strategies discussed include imagery, mental practice and a systematic review of performance that focuses on the perceptual feedback received by the learner.

General Surgery↗

Is the cerebellum ready for navigation?

Spatial navigation required the acquisition of at least two complementary processes: the organization of the spatial representation of the environment (declarative learning) and the acquisition of a motor behaviour adapted to the specific context (procedural learning). The potential role of the cerebellum in spatial navigation is part of the debate concerning its role in cognitive function. Experiments ranging from cerebellar patients to animal models have indicated that cerebellar damage affects the processing of spatial information. The main unresolved issue concern the interpretation of these deficits. Is the cerebellum involved in both declarative and procedural components of navigation? Could all deficits in navigation paradigms be interpreted by a deficit in a motor-dependant process? The purpose of this review is to examine different results coming from anatomical data, experimental paradigms and models in order to give a critical answer to this question.

Animals↗

Motor and non-motor sequence learning in patients with basal ganglia lesions: the case of serial reaction time (SRT).

In order to address the question of whether the basal ganglia are involved exclusively in regulation of motor sequence learning, or if they are involved in non-motor sequence learning as well, two versions of the serial reaction time (SRT) task were administered: First is the standard version of the SRT task in which the sequence is executed motorically, and the second is a non-motor version of the task which requires response only to a particular position of the sequence. Sixteen patients with damage restricted to the region of the basal ganglia and 16 matched control subjects participated in this study. In addition to the motor and non-motor SRT tasks, two declarative memory tests (Visual Paired Associates and Rey Auditory-Verbal Learning Test) were administered to the participants. Results indicate that the two groups did not differ either on learning rate of the two declarative tasks, or on the declarative component of the SRT tasks (i.e., 'generate'). However, the control group was significantly superior to the basal ganglia (BG) group in learning a specific sequence in the motor and non-motor SRT tasks. Results suggest that the basal ganglia are involved in the regulation of non- motor as well as motor sequence learning.

Adult↗

Habit and skill learning in schizophrenia: evidence of normal striatal processing with abnormal cortical input.

Different forms of nondeclarative learning involve regionally specific striatal circuits. The motor circuit (involving the putamen) has been associated with motor-skill learning and the dorsolateral prefrontal cortex (DLPFC) circuit (involving the caudate) has been associated with cognitive-habit learning. Efforts to differentiate functional striatal circuits within patient samples have been limited. Previous studies have provided mixed results regarding striatal-dependent nondeclarative learning deficits in patients with schizophrenia. In this study, a cognitive-habit learning task (probabilistic weather prediction) was used to assess the DLPFC circuit and a motor-skill learning task (pursuit rotor) was used to assess the motor circuit in 35 patients with schizophrenia and 35 normal controls. Patients with schizophrenia displayed significant performance differences from controls on both nondeclarative tasks; however, cognitive-habit learning rate in patients did not differ from controls. There were performance and learning-rate differences on the motor-skill learning task between the whole sample of patients and controls, however, analysis of a subset of patients and controls matched on general intellectual level eliminated learning rate differences between groups. The abnormal performance offset between patients with schizophrenia and controls in the absence of learning rate differences suggests that abnormal cortical processing provides altered input to normal striatal circuitry.

Adult↗