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Motor skills and motor learning in Lurcher mutant mice during aging.

Motor learning abilities on the rotorod and motor skills (muscular strength, motor coordination, static and dynamic equilibrium) were investigated in three-, nine-, 15- and 21-month-old Lurcher and control mice. Animals were subjected to motor training on the rotorod before being subjected to motor skills tests. The results showed that control mice exhibited decrease of muscular strength and specific equilibrium impairments in static conditions with age, but were still able to learn the motor task on the rotorod even in old age. These results suggest that, in control mice, efficiency of the reactive mechanisms, which are sustained by the lower transcerebellar loop (cerebello-rubro-olivo-cerebellar loop), decreased with age, while the efficiency of the proactive adjustments, which are sustained by the upper transcerebellar loop (cerebello-thalamo-cortico-ponto-cerebellar loop), did not. In spite of their motor deficits, Lurcher mutants were able to learn the motor task at three months, but exhibited severe motor learning deficits as soon as nine months. Such a deficit seems to be associated with dynamic equilibrium impairments, which also appeared at nine months in these mutants. By two months of age, degeneration of the cerebellar cortex and the olivocerebellar pathway in Lurcher mice has disrupted both lower and upper transcerebellar loops. Disruption of the lower loop could well explain precocious static equilibrium deficits. However, in spite of disruption of the upper loop, motor learning and dynamic equilibrium were preserved in young mutant mice, suggesting that either deep cerebellar nuclei and/or other motor structures involved in proactive mechanisms needed to maintain dynamic equilibrium and to learn motor tasks, such as the striatopallidal system, are sufficient. The fact that, in Lurcher mutant mice, motor learning decreased by the age of nine months suggests that the above-mentioned structures are less efficient, likely due to degeneration resulting from precocious and focused neurodegeneration of the cerebellar cortex. From this behavioral approach of motor skills and motor learning during aging in Lurcher mutant mice, we postulated the differential involvement of two transcerebellar systems in equilibrium maintenance and motor learning. Moreover, in these mutants, we showed that motor learning abilities decreased with age, suggesting that the precocious degeneration of the cerebellar Purkinje cells had long-term effects on motor structures which are not primarily affected. Thus, from these results, Lurcher mutant mice therefore appear to be a good model to study the pathological evolution of progressive neurodegeneration in the central nervous system during aging.

Aging↗

Distinct neural systems underlie learning visuomotor and spatial representations of motor skills.

Motor skill learning depends upon acquiring knowledge about multiple features of sequential behaviors, including their visuomotor and spatial properties. To investigate the neural systems that distinguish these representations, we carried out functional magnetic resonance imaging (fMRI) as healthy adults learned to type sequences on a novel keyboard. On the initial training day, learning-related changes in brain activation were found in distributed cortical regions, only a subset of which correlated with improvements in movement time (MT), suggesting their preeminence in controlling movements online. Subjects received extended training on the sequences during the ensuing week, after which they returned to the scanner for another imaging session. Relative to performance at the end of the first training day, continued plasticity was most striking in the inferior parietal cortex and new areas of plasticity were uncovered in the caudate and cerebellum. Plasticity in these regions correlated with reaction time (RT), suggesting their role in planning sequences before movement onset. Two transfer conditions probed for "what" subjects learned. The probe for visuomotor learning produced increased activation in visual analysis (left inferior visual cortex) and advance planning (left caudate) systems. The probe for spatial learning produced increased activation in visuomotor-transformation (left dorsal visual pathway) and retrieval (left precuneus) systems. Increased activity in all of these regions correlated with increased RT, but not MT, indicating that both transfer conditions interfered with the neural representation of plans for the sequences, but not processes that controlled their implementation. These findings demonstrated that neuroanatomically dissociable systems support the acquisition of visuomotor and spatial representations of actions.

Adolescent↗

Role of the inferior olivary complex in motor skills and motor learning in the adult rat.

The inferior olivary complex of adult rats was chemically destroyed using intraperitoneal injection of 3-acetylpyridine. Animals were submitted to different motor tasks: hanging test, equilibrium test and motor co-ordination test. The different scores show that 3-acetylpyridine-treated rats had motor co-ordination and static equilibrium deficiencies, whereas their rod suspension capabilities were intact. Animals were also trained on an unrotated rod or on a rod rotating at 5, 10 or 20 r.p.m. 3-Acetylpyridine-treated rats were able to maintain their equilibrium on the unrotated rod and at 5 r.p.m. Moreover, after motor training at 5 r.p.m., rats were able to improve their motor skills and reached the same score as controls. Despite their good motor skills, animals were unable to maintain their equilibrium when rotated at 10 and 20 r.p.m. These results suggest that the inferior olivary complex is needed for motor learning involving the temporal organization of movement.

Age Factors↗

Influence of a motor skill intervention on fundamental motor skill development of disadvantaged preschool children.

The influence of a 12-week (24, 45-min motor sessions) motor skill intervention on fundamental motor skill (FMS) development of disadvantaged preschools was examined. Pre-and postintervention measures of the object control (OC) and locomotor subscales of the Test of Gross Motor Development were obtained for both groups. Prior to the intervention, developmental delays in FMS were reported. Two separate 2 x 2 (Group x Pre-Postintervention) analyses of variance with repeated measures yielded a significant Group x Pre-Postintervention interaction for locomotor, F(1, 57) = 134.23, p = .000, h2 = .70, and OC, F(1, 57) = 161.55, p = .000, h2 = .74) skills. Compared to the Control group, the motor skill intervention group revealed significant higher locomotor and OC scores following the intervention than prior to the intervention.

Child, Preschool↗

Skilled motor learning does not enhance long-term depression in the motor cortex in vivo.

Learning of motor skills may occur as a consequence of changes in the efficacy of synaptic connections in the primary motor cortex. We investigated if learning in a reaching task affects the excitability, short-term plasticity, and long-term plasticity of horizontal connections in layers II-III of the motor cortex. Because training in this task requires animals to be food-deprived, we compared the trained animals with similarly food-deprived untrained animals and normal controls. The results show that the excitability, short-term plasticity, and long-term plasticity of the studied horizontal connections were unaffected by motor learning. However, stress-related effects produced by food deprivation and handling significantly enhanced the expression of long-term depression in these pathways. These results are compatible with the hypothesis that the acquisition of a complex motor skill produces bi-directional changes in synaptic strength that are distributed throughout the complex neural networks of motor cortex, which remains synaptically balanced during learning. The results are incompatible with the idea that learning causes large unidirectional changes in the population response of these neural networks, which may occur instead during certain behavioral states, such as stress.

6-Cyano-7-nitroquinoxaline-2,3-dione↗

Imaging brain plasticity during motor skill learning.

The search for the neural substrates mediating the incremental acquisition of skilled motor behaviors has been the focus of a large body of animal and human studies in the past decade. Much less is known, however, with regard to the dynamic neural changes that occur in the motor system during the different phases of learning. In this paper, we review recent findings, mainly from our own work using fMRI, which suggest that: (i) the learning of sequential finger movements produces a slowly evolving reorganization within primary motor cortex (M1) over the course of weeks and (ii) this change in M1 follows more dynamic, rapid changes in the cerebellum, striatum, and other motor-related cortical areas over the course of days. We also briefly review neurophysiological and psychophysical evidence for the consolidation of motor skills, and we propose a working hypothesis of its underlying neural substrate in motor sequence learning.

Brain↗

EMG changes during acquisition of a motor skill.

Currently there are only a few studies which attempt to explain the neuromuscular changes which accompany skilled motor learning. Conflicting results have created the need for further research concerned with the electromyographical correlates of motor skill acquisition. A shuffleboard task was devised that isolated the triceps as the major agonist and the biceps as the major antagonist. Ten undergraduate males enrolled at Iowa State University participated in the study. Multivariate analysis and single degree of freedom components based on polynomial regression were used to test linear, quadratic and cubic trends for eight EMG characteristics plus movement time obtained from a systematic sampling of practice trials. Results indicated that trial period means for movement time, latency period and time to peak activity for the triceps exhibited significant linear trends (negative) during practice. No changes were seen in the integrated electromyograms for either the triceps or biceps. It was concluded that force parameters as measured by integrated EMG activity could be determined very early in the learning process and the distribution of these forces through various aspects of timing characterized learning.

Adolescent↗

Lesions of the Basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning.

The contribution of the basal forebrain cholinergic system in mediating plasticity of cortical sensorimotor representations was examined in the context of normal learning. The effects of specific basal forebrain cholinergic lesions upon cortical reorganization associated with learning a skilled motor task were investigated, addressing, for the first time, the functional consequences of blocking cortical map plasticity. Results demonstrate that disrupting basal forebrain cholinergic function disrupts cortical map reorganization and impairs motor learning. Cholinergic lesions do not impair associative fear learning or overall sensorimotor function. These results support the hypothesis that the basal forebrain cholinergic system may be specifically implicated in forms of learning requiring plasticity of cortical representations.

Acetylcholine↗

Patients with Alzheimer's disease who cannot perform some motor skills show normal learning of other motor skills.

Previous researchers have claimed that patients with Alzheimer's disease (AD) learn new motor skills normally, although many AD patients cannot perform the tasks and must be eliminated from the analysis. Excluding them assumes that they have a deficit of motor performance (competence to perform the task), but not of motor learning (ability to improve performance). The present study administered 4 motor tasks to 20 AD patients and 20 controls. The results showed that the ability to complete 1 task (performance) did not predict the rate of improvement (learning) on another task, which indicates that AD patients do indeed have a performance deficit and not a general deficit of motor skill learning. Dementia ratings predicted the ability to perform tasks but not the ability to learn them. It is concluded that it is defensible to claim that AD patients learn a motor skill normally, even if some of the patients are unable to perform the task.

Aged↗

Becoming aware of motor skill.

Conscious processes have a complex relationship to skilled motor performance. Past work has shown that some types of motor skill can be learned without any contribution from conscious processes. New work indicates that if those unconscious processes are disabled, conscious processes might step in to make up for the deficit.

Journal Article↗

Role of the striatum and the cerebellum in motor skill acquisition.

Motor skill acquisition was investigated in patients with Parkinson's disease (PD) or cerebellar dysfunction using two sensory-guided tracking tasks. The subjects had to learn to track a visual target (a square) on a computer screen by moving a joystick under two different conditions. In the unreversed task, the horizontal target movements were semi-predictable and could be anticipated. In the reversed task, the horizontal movements of a pointer which had to be kept within the target square were mirror-reversed to the joystick movements. PD patients showed intact learning of the semi-predictable task and reduced learning of the mirror-reversed task; patients with cerebellar dysfunction showed the opposite pattern. These findings are discussed in relation to the differential contribution of the cerebellum and the striatum to motor skill acquisition: the cerebellum appears to participate in the implementation of anticipatory movements, whereas the striatum may be critically involved in types of motor learning which require a high degree of internal elaboration.

Journal Article↗

Proactive interference as a result of persisting neural representations of previously learned motor skills in primary motor cortex.

Learning to control movements in different dynamic environments is marked by proactive interference; learning a first skill interferes with the subsequent learning of a second one. The neural basis of this effect is poorly understood. We tested the idea that proactive interference results from persisting neural representations of previously learned skills in the primary motor cortex (M1). We used repetitive transcranial magnetic stimulation (rTMS) of M1 to disrupt retention of a recently learned motor skill. If interference results from the retention of this skill then its disruption should be associated with reduced interference. Subjects reached to targets while interacting with a robotic arm that applied force fields to the limb. Fifteen minutes of 1-Hz rTMS to M1 impaired the retention of a first force field, and more importantly, reduced proactive interference when subjects learned a second one. Our findings suggest that retention and interference are linked at the level of M1.

Algorithms↗

Reduction of single-neuron firing uncertainty by cortical ensembles during motor skill learning.

Motor skill learning is usually characterized by shortening of response time and performance of faster, more stereotypical movements. However, little is known about the changes in neural activity that underlie these behavioral changes. Here we used chronically implanted electrode arrays to record neuronal activity in the rat primary motor cortex (MI) as animals learned to execute movements in two directions. Strong modulation of MI single-neuron activity was observed while movement duration of the animal decreased. Despite many learning-induced changes, the precision with which single neurons fire did not improve with learning. Hence, prediction of movement direction from single neurons was bounded. In contrast, prediction of movement direction using neuronal ensembles improved significantly with learning, suggesting that, with practice, neuronal ensembles learn to overcome the uncertainty introduced by single-neuron stochastic activity.

Acoustic Stimulation↗

Nicotine stimulates dendritic arborization in motor cortex and improves concurrent motor skill but impairs subsequent motor learning.

The effect of the premature commitment of neurons to exuberant growth by nicotine on concurrent and subsequent learning is unknown and was the focus of the present study. Animals were trained on a tray reaching for food task (where lots of pieces of chicken feed were available) for 3 weeks before they received two daily injections of nicotine (0.3 mg/kg) or 0.9% saline for 12 days. Measures of tray-reaching performance were obtained before the administration of nicotine and every other week for a total of 7 weeks. Starting on week 8, animals were given a novel motor skill problem that required them to learn to use a forepaw to reach through a slot in a cage for single food pellets located on an external shelf. Pyramidal cells in the forelimb area of both hemispheres were then examined for dendritic length and branching using a Golgi-Cox procedure. Animals treated with saline displayed excellent performance in both reaching tasks and an increase in neuronal branching in Layer V pyramidal cells in the motor cortex contralateral to the reaching paw. In contrast, animals treated with nicotine showed bilateral increases in neuronal branching. Behavioral results showed that nicotine improved forelimb use in the concurrently administered tray-reaching task, but severely degraded quantitative and qualitative scores of skilled forelimb use in the subsequently administered single-pellet reaching task. The results suggest that plasticity coincidence with skilled training is essential to skilled motor learning, but this expenditure can impair subsequent learning.

Animals↗

What is the role of the corpus callosum in intermanual transfer of motor skills? A study of three cases with callosal pathology.

Intermanual transfer for a skilled motor task was studied in two patients with total callosal agenesis, and one with an acquired partial callosal lesion and clinical evidence for disturbed transfer of motor signals. Patients had to draw meaningless figures with one upper extremity (original learning, OL) and to reproduce their mirror-reversals thereafter with the other side (transfer learning, TL). Both directions of intermanual transfer were tested in two conditions, that is, between either proximal or distal muscle groups. Transfer was evaluated by comparing OL and TL performance at the same effector. The main variable of interest was movement time during the first eight trials of OL and TL. All three patients displayed a significant benefit for transfer from the dominant to the non-dominant hand but not vice versa during proximal motor activity. When compared with the performance of healthy subjects tested in almost identical conditions in a previously reported study, the proximal transfer behavior was found to be similar for all patients and the normal group. Although patients exhibited no significant benefit for distal transfer, their non-dominant-to-dominant distal transfer was above the normal range. The similar transfer pattern of the patients and healthy subjects when using proximal musculature suggests that proximal transfer may be subserved by identical extracallosal pathways, most probably by the ipsilaterally descending motor systems. Since non-dominant-to-dominant distal transfer was found to be disadvantageous in healthy subjects, the patients' relative superiority in this condition may reflect missing callosal influences of an inhibitory nature.

Adult↗