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Reorganization of activity in the supplementary motor area associated with motor learning and functional recovery.

The supplementary motor area (SMA) of primates has been implicated in the initiation and execution of limb movements. However, when a motor task was extensively overlearned, few SMA neurons, if any, were active before the movement onset. Subsequent lesions of the primary motor cortex gave rise to the appearance of premovement activity changes, indicating usedependent reorganization of the neuronal activity in SMA.

Animals↗

Scaling down motor memories: de-adaptation after motor learning.

Although adaptation to novel motor tasks is sometimes a very slow process, de-adaptation is usually extremely rapid. Such rapid de-adaptation is seen in dynamic learning in which subjects can take hundreds of movements to learn a novel force environment but only a few movements to de-adapt back to a normal or "null" force environment. We investigated whether this effect is unique to the null environment or reveals a more general rapid adaptation mechanism by studying how subjects behave when their dynamic environment changes. We observed that after learning a dynamic force field, subjects took longer to de-adapt when the forces were turned off than to adapt to a novel scaled-down version of the experienced field. This demonstrates that rapid adaptation is not unique to the "null" force environment. Moreover, we examined subjects' ability to adapt from a learned field to either a scaled down field or to a field in which the sign of the forces changed. Even though in both conditions the required change in force output was identical, subjects were significantly faster at adapting to the scaled down field. The result suggests that rapid de-adaptation reflects a capacity to scale down the relative contribution of existing control modules to the motor output.

Adaptation, Physiological↗

Central regulation of cerebellar climbing fibre input during motor learning.

A forelimb-withdrawal classical conditioning paradigm was used in awake cats (n = 4) to investigate changes in transmission in climbing fibre (CF) pathways during motor learning. The conditioned stimulus was an auditory tone, while the unconditioned stimulus was a low-intensity, single or double (0.1 ms) electrical pulse applied to the ipsilateral superficial radial nerve. Microwires chronically implanted into the paravermal cerebellar cortex (lobule V) were used to record the CF field potentials evoked by nerve stimulation, and fields at 22 recording sites (9 C1, 7 C2 and 6 C3 zone sites) were monitored during the complete sequence of at least one training run (i.e. over a period of about 2-3 weeks of conditioning). At 19 sites (86 %) conditioning led to a significant reduction in mean size of field. Similar reductions occurred at four sites studied over two successive training runs. At 10 sites (45 %) there was a statistically significant increase prior to the reduction. The three sites that failed to exhibit a significant reduction were all located in the C1 zone. Controls showed that the changes in CF transmission were dependent on the animal being conditioned. The mean size of CF field for trials in which a conditioned EMG response was present (in either the cleidobrachialis or biceps muscle) was not significantly different from the mean size for trials in which a conditioned response was absent. Similarly, on a trial-by-trial basis, CF pathway excitability was not correlated with the conditioned EMG activity in the flexor muscles under study. Overall, the results demonstrate that (1) the capacity of spino-olivocerebellar pathways (SOCPs) to forward information to the cerebellar cortex can be altered by recent experience, (2) establishment of a conditioned forelimb flexor reflex to a tone reduces SOCP excitability at most but not all sites within a forelimb-related region of the cerebellar cortex, (3) the extent of reductions differ at different sites and some are preceded by transient increases, and (4) the changes in transmission may not be related to the conditioned movement. The implications of these findings for some key theories of cerebellar cortical function are discussed.

Acoustic Stimulation↗

On the dynamics of motor learning research.

In this paper I have attempted to conceptualize the dynamical pattern view of learning (Zanone & Kelso, 1992, 1994, 1997) in terms of some historical similarities to the dynamic pattern perspective, unique contributions, and potential problems to be addressed in future research and theory. For researchers interested in motor learning issues, all three of these points can be viewed only as positive advances to the field of study.

Behavior↗

Striatal synaptic plasticity: implications for motor learning and Parkinson's disease.

Changing the strength of synaptic connections between neurons is widely assumed to be the mechanism by which memory traces are encoded and stored in the central nervous system. Plastic changes appear to follow a regional specialization and underlie the specific type of memory mediated by the brain area in which plasticity occurs. Thus, long-term changes occurring at excitatory corticostriatal synapses should be critically involved in motor learning. Indeed, repetitive stimulation of the corticostriatal pathway can cause either a long-lasting increase or an enduring decrease in synaptic strength, respectively referred to as long-term potentiation (LTP), and long-term depression, both requiring a complex sequence of biochemical events. Once established, LTP can be reversed to control levels by a low-frequency stimulation protocol, an active phenomenon defined "synaptic depotentiation," required to erase redundant information. In the 6-hydroxydopamine rat model of Parkinson's disease (PD), striatal synaptic plasticity has been shown to be impaired, although chronic treatment with levodopa was able to restore it. Of interest, a consistent number of L-dopa-treated animals developed involuntary movements, resembling human dyskinesias. Strikingly, electrophysiological recordings from the dyskinetic group of rats demonstrated a selective impairment of synaptic depotentiation. This survey will provide an overview of plastic changes occurring at striatal synapses. The potential relevance of these findings in the control of motor function and in the pathogenesis both of PD and L-dopa-induced motor complications will be discussed.

Animals↗

The utility of connectionism for motor learning: a reinterpretation of contextual interference in movement schemas.

Using the general framework of schema theory, and building on it, the present article takes a connectionist approach to motor learning and to contextual interference effects. These phenomena were simulated in an exploratory manner in neural networks. The outcome closely reflects previous research with humans. In a simulated ballistic movement task, networks performed worse during practice but showed better transfer when target movement distances were presented in a random rather than a blocked fashion. Connectionism provides a parsimonious account of the effect in terms of properties inherent in the parallel distributed network.

Journal Article↗

Role of the flocculus of the cerebellum in motor learning of the vestibulo-ocular reflex.

Structure-function studies at the systems level are an effective method for understanding the relationship of the central nervous system to behavior. Motor learning or adaptation of the vestibulo-ocular reflex is a clear example wherein this approach has been productive. During a vestibulo-ocular reflex the brain converts a head velocity signal, transduced through the vestibular semicircular canals, into an eye movement command delivered to the extraocular muscles. If the viewed target remains on the fovea of the retina, the reflex is compensatory, and its gain, eye velocity/head velocity, is one. When the image of the viewed object slips across the retina, visual acuity decreases, and the gain of the reflex, which is no longer one, is plastically adapted or adjusted until retinal stability is restored. The anatomic substrate for this plasticity thus involves brain structures in which visual-vestibular interaction can potentially occur, as well as vestibular and visual sensory and oculomotor motor structures. Further, it has been known for many years that removal of the flocculus of the cerebellum permanently precludes further vestibulo-ocular reflex adaptation, demonstrating the involvement of the cerebellum in this behavior. Maekawa and Simpson (J Neurophysiol 1973;36: 649-66) discovered that one visual input to the flocculus involved the accessory optic system and the inferior olive. Ensuing work has demonstrated that the visual signals used to adapt the vestibulo-ocular reflex are transmitted by this accessory optic system to the flocculus and subsequently to brain stem structures involved in vestibulo-ocular reflex plasticity. Presently the inclusive list of anatomic sites involved in vestibulo-ocular reflex circuitry and its adaptive plasticity is small. Our laboratory continues to believe that this behavior should be caused by interactions within this small class of neurons. By studying each class of identified neuron and its interactions with others within the list, we hope to ultimately understand the mechanisms used by the brain in the expression of this behavior.

Adaptation, Physiological↗

A novel model of motor learning capable of developing an optimal movement control law online from scratch.

A computational model of a learning system (LS) is described that acquires knowledge and skill necessary for optimal control of a multisegmental limb dynamics (controlled object or CO), starting from "knowing" only the dimensionality of the object's state space. It is based on an optimal control problem setup different from that of reinforcement learning. The LS solves the optimal control problem online while practicing the manipulation of CO. The system's functional architecture comprises several adaptive components, each of which incorporates a number of mapping functions approximated based on artificial neural nets. Besides the internal model of the CO's dynamics and adaptive controller that computes the control law, the LS includes a new type of internal model, the minimal cost (IM(mc)) of moving the controlled object between a pair of states. That internal model appears critical for the LS's capacity to develop an optimal movement trajectory. The IM(mc) interacts with the adaptive controller in a cooperative manner. The controller provides an initial approximation of an optimal control action, which is further optimized in real time based on the IM(mc). The IM(mc) in turn provides information for updating the controller. The LS's performance was tested on the task of center-out reaching to eight randomly selected targets with a 2DOF limb model. The LS reached an optimal level of performance in a few tens of trials. It also quickly adapted to movement perturbations produced by two different types of external force field. The results suggest that the proposed design of a self-optimized control system can serve as a basis for the modeling of motor learning that includes the formation and adaptive modification of the plan of a goal-directed movement.

Adaptation, Physiological↗

Associative and motor learning in 12-month-old transgenic APP+PS1 mice.

Doubly transgenic 12-month-old amyloid precursor protein and presenilins 1 (APP+PS1) mice (n=14) and littermate control mice (n=17) were tested on eyeblink classical conditioning-a task impaired in humans with Alzheimer's disease (AD). Mice were also tested on a motor learning task (rotorod) and on sensory tasks (prepulse inhibition [PPI] and acoustic startle). Transgenic mice had impaired motor performance on rotorod. Overall, APP+PS1 mice performed similarly to controls on both 500ms delay and 500ms trace eyeblink conditioning as well as on prepulse inhibition (PPI) and acoustic startle. However, within the transgenic group, cortical amyloid burden correlated significantly with decreased trace eyeblink conditioning. Moreover, cortical amyloid burden and hippocampal microglia activation correlated significantly with decreased PPI. These data suggest that only those transgenic mice with the most severe amyloid pathology exhibited deficits in hippocampus-dependent tasks. Transgenic mouse models of amyloid deposition differ from Alzheimer patients not only by the absence of major neuronal loss, but also by the general absence of severe impairments in eyeblink conditioning, except for mice with the greatest amyloid pathology.

Alzheimer Disease↗

A model system for motor learning: adaptive gain control of the blink reflex.

An important aspect of the control of movement is how the nervous system produces adaptive gain modification. To investigate this problem in a simple motor system, we studied lid movement and orbicularis oculis muscle activity in human and rabbit subjects during adaptation of reflex eye blinks. The gain of the reflex could be increased or decreased, depending upon the nature of the adaptive stimulus. Since these gain changes could persist upon removal of the adapting stimulus, adaptation appears to result from a modification of the neural program subserving the blink reflex. The orbicularis oculis electromyogram revealed that the neural modifications producing adaptive gain changes predominantly altered the longer latency components of the reflex, while the short latency components remained unchanged. Moreover, in two other paradigms that modulate the gain of reflexes, habituation and reflex modification, similar changes also occurred primarily in the longer latency components of the blink reflex. This result suggests that modification of neurons in longer latency, indirect pathways, may underlie different forms of motor learning.

Adaptation, Physiological↗

Differential role for the striatum and cerebellum in response to novel movements using a motor learning paradigm.

The aim of this pilot study was to examine the role of the striatum and cerebellum in the adaptation to a novel movement within a sequence of practiced movements using a motor learning paradigm. The performance of patients in the early or advanced stages of Parkinson's disease (PD) and of patients with damage to the cerebellum (CE) was compared, respectively to a group of aged and young matched controls on an adapted version of the Mirror-Tracing Test. In this task, subjects were required to trace a series of complex figures in two conditions: (1) a Practiced condition, in which the figures were composed of the juxtaposition of three simple designs that were extensively practiced before; and (2) a Mixed condition in which triads were created by replacing the last simple figure of the triads in the Practiced condition by a new simple figure that had never been traced individually before. Results showed that all clinical groups were slower than controls at tracing the Practiced triads. Most interestingly, however, only patients in the advanced stages of PD showed increased completion time to trace the triads in the Mixed condition. This suggests that a bilateral striatal dysfunction affects the ability to adapt to a novel motion within a sequence of practiced movements. Although exploratory, these results support a functional dissociation between the striatum and cerebellum in acquiring visuomotor skilled behaviors.

Adult↗

The hyperpolarization-activated HCN1 channel is important for motor learning and neuronal integration by cerebellar Purkinje cells.

In contrast to our increasingly detailed understanding of how synaptic plasticity provides a cellular substrate for learning and memory, it is less clear how a neuron's voltage-gated ion channels interact with plastic changes in synaptic strength to influence behavior. We find, using generalized and regional knockout mice, that deletion of the HCN1 channel causes profound motor learning and memory deficits in swimming and rotarod tasks. In cerebellar Purkinje cells, which are a key component of the cerebellar circuit for learning of correctly timed movements, HCN1 mediates an inward current that stabilizes the integrative properties of Purkinje cells and ensures that their input-output function is independent of the previous history of their activity. We suggest that this nonsynaptic integrative function of HCN1 is required for accurate decoding of input patterns and thereby enables synaptic plasticity to appropriately influence the performance of motor activity.

Action Potentials↗

Deficits in long-term retention of learned motor skills in patients with cortical or subcortical degeneration.

We investigated the acquisition and long-term retention of new skills in patients with cortical (Alzheimer's disease, AD) and subcortical (progressive supranuclear palsy, PSP; Parkinson's disease, PD) degeneration. The motor skill task performance of the PD and PSP patients improved with training, but the improvement disappeared within a few months, whereas AD patients retained learned skills for 3-18 months. The results of our experiments show that subcortical dysfunction induces a retention deficit for newly learned motor skills. Our present study suggests that a normal striatum is necessary for the formation of long-lasting motor skills, and that the striatum plays an important role as a motor skill consolidation system.

Alzheimer Disease↗

Providing explicit information disrupts implicit motor learning after basal ganglia stroke.

Despite their purported neuroanatomic and functional isolation, empirical evidence suggests that sometimes conscious explicit processes can influence implicit motor skill learning. Our goal was to determine if the provision of explicit information affected implicit motor-sequence learning after damage to the basal ganglia. Individuals with stroke affecting the basal ganglia (BG) and healthy controls (HC) practiced a continuous implicit motor-sequencing task; half were provided with explicit information (EI) and half were not (No-EI). The focus of brain damage for both BG groups was in the putamen. All of the EI participants were at least explicitly aware of the repeating sequence. Across three days of practice, explicit information had a differential effect on the groups. Explicit information disrupted acquisition performance in participants with basal ganglia stroke but not healthy controls. By retention (day 4), a dissociation was apparent--explicit information hindered implicit learning in participants with basal ganglia lesions but aided healthy controls. It appears that after basal ganglia stroke explicit information is less helpful in the development of the motor plan than is discovering a motor solution using the implicit system alone. This may be due to the increased demand placed on working memory by explicit information. Thus, basal ganglia integrity may be a crucial factor in determining the efficacy of explicit information for implicit motor-sequence learning.

Adult↗

Motor learning in man: a review of functional and clinical studies.

This chapter reviews results of clinical and functional imaging studies which investigated the time-course of cortical and subcortical activation during the acquisition of motor a skill. During the early phases of learning by trial and error, activation in prefrontal areas, especially in the dorsolateral prefrontal cortex, is has been reported. The role of these areas is presumably related to explicit working memory and the establishment of a novel association between visual cues and motor commands. Furthermore, motor associated areas of the right hemisphere and distributed cerebellar areas reveal strong activation during the early motor learning. Activation in superior-posterior parietal cortex presumably arises from visuospatial processes, while sensory feedback is coded in the anterior-inferior parietal cortex and the neocerebellar structures. With practice, motor associated areas of the left-hemisphere reveal increased activity. This shift to the left hemisphere has been observed regardless of the hand used during training, indicating a left-hemispheric dominance in the storage of visuomotor skills. Concerning frontal areas, learned actions of sequential character are represented in the caudal part of the supplementary motor area (SMA proper), whereas the lateral premotor cortex appears to be responsible for the coding of the association between visuo-spatial information and motor commands. Functional imaging studies which investigated the activation patterns of motor learning under implicit conditions identified for the first, a motor circuit which includes lateral premotor cortex and SMA proper of the left hemisphere and primary motor cortex, for the second, a cognitive loop which consists of basal ganglia structures of the right hemisphere. Finally, activity patterns of intermanual transfer are discussed. After right-handed training, activity in motor associated areas maintains during performance of the mirror version, but is increased during the performance of the original-oriented version with the left hand. In contrary, increased activity during the mirror reversed action, but not during the original-oriented performance of the untrained right hand is observed after left-handed training. These results indicate the transfer of acquired right-handed information which reflects the mirror symmetry of the body, whereas spatial information is mainly transferred after left-handed training. Taken together, a combined approach of clinical lesion studies and functional imaging is a promising tool for identifying the cerebral regions involved in the process of motor learning and provides insight into the mechanisms underlying the generalisation of actions.

Brain↗

On discontinuities in motor learning: a longitudinal study of complex skill acquisition on a ski-simulator.

The qualitative behavioral reorganizations that occurred during the acquisition of a complex motor skill were examined. Five novice participants practiced for 39 sessions of ten 1-min trials on a modified version of the ski-simulator. Analyses focused on the motion of the apparatus platform, modeled as a self-sustained oscillator. At the beginning of the experiment, all participants adopted a behavior that could be modeled with a highly nonlinear stiffness function and a Rayleigh damping function. The behavior in the final part of the experiment was captured by a qualitatively different model, with a linear stiffness function and a van der Pol damping behavior. The transition from the initial to the final model was gradual and was marked in most cases by an abrupt increase of oscillation frequency. During the transition stage, the 2 damping behaviors seemed alternately exploited within each trial. The results are discussed in the framework of the dynamical systems approach to motor coordination and learning, considering motor skill acquisition as a phase transition.

Adult↗

Goal setting in acquisition of a volleyball skill late in motor learning.

To examine the effects of different types of goal setting on motor skill acquisition during advanced stages of learning. 44 female volleyball players were tested in four experimental training groups with generic goals, specific long-term goals, specific short-term goals, and as a control group. This study's pretest, training, and retention test phases used performance of a volleyball dig/forearm pass oriented to a target. Analyses yielded no significant differences among groups, although performance increased from pre- to retention test.

Adolescent↗

Changes of cortical activity when executing learned motor sequences.

Fifteen right-handed subjects performed a learned sequence of four movements (flex index finger, extend hand, extend index finger, flex hand) either with their left or their right hand. The sequence of movements had to be continuously repeated for 20 s (period of execution). In the beginning of each period of execution large negative DC potentials were recorded in positions located above the mesial fronto-central cortex (Cz) and the sensorimotor hand areas of either hemisphere (C3 and C4). In contrast, DC potentials were absent in Cz at the end of the period of execution. In recordings from a position above the sensorimotor hand area contralateral to the performing side, negative DC potentials declined to some extent during task execution but were still present at the end of the period. Variations of both the amplitude and topography of negative cortical DC potentials during task-execution indicate changes of both the size and pattern of cortical activity. These findings were consistently found at both the beginning and end of the experiment. Motor performance as quantified by movement times and inter-onset latencies of movements showed no change, either during the periods of execution or when comparing the beginning of the experiment with the end. Conclusions are: (1) the execution of a learned motor sequence task cannot be associated with a particular size and pattern of cortical activity. (2) A pronounced decline of neural activity in the mesial, fronto-central area constitutes the predominant feature of the changes of cortical activity during the period of execution.(ABSTRACT TRUNCATED AT 250 WORDS)

Adult↗