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A study of cerebellar cortical involvement in motor learning using a new avoidance conditioning paradigm involving limb movement.

These experiments were performed to examine the relationship between the simple and complex spike responses of 3-5 simultaneously recorded Purkinje cells during the acquisition, performance and extinction of a conditioned forelimb movement in decerebrate, unanesthetized ferrets. The data demonstrate parallel, correlated changes in simple and complex spike responses throughout the experimental period. Since the evaluated Purkinje cells were examined in the cerebellar cortical region that contains neurons highly modulated by the intermittent application of the conditioning stimulus, these findings argue against an induction of a long-lasting modification in simple spike responses by the climbing fiber input as the basis for this type of motor learning.

Animals↗

Schema theory: critical review and implications for the role of cognition in a new theory of motor learning.

This paper is based on a symposium celebrating the 26th anniversary of the publication of "A Schema Theory of Discrete Motor Skill Learning" (Schmidt, 1975) held at the annual conference of the North American Society for the Psychology of Sport and Physical Activity in June 2001. We provide a brief historical context for schema theory and a review of the development of the mechanistic approach to motor learning in general. We explore recent findings in mental practice, observational learning, augmented feedback presentation, and the variability of practice that are inconsistent with schema theory and provide a rationale for the importance of cognitive activity in motor learning.

Child↗

Sensitive period for sensorimotor integration during vocal motor learning.

Sensory experience during sensitive periods in development may direct the organization of neural substrates, thereby permanently influencing subsequent adult behavior. We report a sensitive period during the imitative motor learning phase of sensorimotor integration in birdsong development. By temporarily and reversibly blocking efference to the vocal muscles, we disrupted vocal motor practice during selected stages of song development. Motor disruption during prolonged periods early in development, which allows recovery of vocal control prior to the onset of adult song, has no effect on adult song production. However, song disruption late in development, during the emergence of adult song, results in permanent motor defects in adult song production. These results reveal a decreased ability to compensate for interference with motor function when disturbances occur during the terminal stage of vocal motor development. Temporary disruption of syringeal motor control in adults does not produce permanent changes in song production. Permanent vocal aberrations in juveniles are evident exclusively in learned song elements rather than nonlearned calls, suggesting that the sensitive period is associated with motor learning.

Acoustic Stimulation↗

Simulations of cerebellar motor learning: computational analysis of plasticity at the mossy fiber to deep nucleus synapse.

We question the widely accepted assumption that a molecular mechanism for long-term expression of synaptic plasticity is sufficient to explain the persistence of memories. Instead, we show that learning and memory require that these cellular mechanisms be correctly integrated within the architecture of the neural circuit. To illustrate this general conclusion, our studies are based on the well characterized synaptic organization of the cerebellum and its relationship to a simple form of motor learning. Using computer simulations of cerebellar-mediated eyelid conditioning, we examine the ability of three forms of plasticity at mossy fiber synapses in the cerebellar nucleus to contribute to learning and memory storage. Results suggest that when the simulation is exposed to reasonable patterns of "background" cerebellar activity, only one of these three rules allows for the retention of memories. When plasticity at the mossy fiber synapse is controlled by nucleus or climbing fiber activity, the circuit is unable to retain memories because of interactions within the network that produce spontaneous drift of synaptic strength. In contrast, a plasticity rule controlled by the activity of the Purkinje cell allows for a memory trace that is resistant to ongoing activity in the circuit. These results suggest specific constraints for theories of cerebellar motor learning and have general implications regarding the mechanisms that may contribute to the persistence of memories.

Cerebellar Cortex↗

Cerebellar signatures of vestibulo-ocular reflex motor learning.

The vestibulo-ocular reflex (VOR) comprises an outstanding system to perform studies that probe possible cerebellar roles in motor learning. Novel VOR gains can be induced (learned) by the wearing of minifying or magnifying lenses, and learning requires the presence of the cerebellum. Previously, it was shown that Purkinje cells change their head velocity sensitivities with learning and that this change was thought to be inappropriate to be causal for the changed behavior. We now demonstrate that Purkinje cells also change their eye position, eye velocity, and head velocity sensitivities after learning. These combined changes at the Purkinje cell level contribute to a net modulation that is appropriate to support the new VOR gains. Importantly, the changes in the eye position parameter, reported for the first time, suggest the involvement of the neuronal integrator pathways in VOR learning. We provide evidence that all of these changes are necessary for VOR behavior and can explain learning deficits after cerebellar removal.

Animals↗

Neural averaging in motor learning.

The capacity for skill development over multiple training episodes is fundamental to human motor function. We have studied the process by which skills evolve with training by progressively modifying a series of motor learning tasks that subjects performed over a 1-mo period. In a series of empirical and modeling studies, we show that performance undergoes repeated modification with new learning. Each in a series of prior training episodes contributes such that present performance reflects a weighted average of previous learning. Moreover, we have observed that the relative weighting of skills learned wholly in the past changes with time. This suggests that the neural substrate of skill undergoes modification after consolidation.

Arm↗

Interacting adaptive processes with different timescales underlie short-term motor learning.

Multiple processes may contribute to motor skill acquisition, but it is thought that many of these processes require sleep or the passage of long periods of time ranging from several hours to many days or weeks. Here we demonstrate that within a timescale of minutes, two distinct fast-acting processes drive motor adaptation. One process responds weakly to error but retains information well, whereas the other responds strongly but has poor retention. This two-state learning system makes the surprising prediction of spontaneous recovery (or adaptation rebound) if error feedback is clamped at zero following an adaptation-extinction training episode. We used a novel paradigm to experimentally confirm this prediction in human motor learning of reaching, and we show that the interaction between the learning processes in this simple two-state system provides a unifying explanation for several different, apparently unrelated, phenomena in motor adaptation including savings, anterograde interference, spontaneous recovery, and rapid unlearning. Our results suggest that motor adaptation depends on at least two distinct neural systems that have different sensitivity to error and retain information at different rates.

Adaptation, Physiological↗

Motor learning concepts applied to activity-based intervention with adults with hemiplegia.

This paper presents a framework for the integration of motor learning research findings with a neurodevelopmental treatment perspective. The importance of activity-based intervention is emphasized, and a strategy for activity synthesis is presented. Clinical problems seen in persons with hemiplegia are used to clarify concepts and illustrate therapeutic interventions.

Hemiplegia↗

Conscious and effortful or effortless and automatic: a practice/performance paradox in motor learning.

High cognitive effort has been frequently related to better indices of motor learning through the study of many different paradigms. However, automaticity presumably invokes minimal cognitive processing but has often been related to high-level motor performance, which suggests a paradox. The objective of this study was to approach this paradox by examining the viability of the use of different cognitive strategies during practice and performance which promote the benefits of high cognitive effort and automaticity. Members of the university community (14 men and 15 women) divided into 3 groups practiced a discrete precision task. All participants completed four sessions totaling 320 trials and were tested on retention and transfer seven days later. Findings suggest that it is indeed possible to benefit from both effortful and minimal cognitive processing strategies and that they should be used complementarily.

Adult↗

Possible role of intramembrane receptor-receptor interactions in memory and learning via formation of long-lived heteromeric complexes: focus on motor learning in the basal ganglia.

Learning in neuronal networks occurs by instructions to the neurons to change their synaptic weights (i.e., efficacies). According to the present model a molecular mechanism that can contribute to change synaptic weights may be represented by multiple interactions between membrane receptors forming aggregates (receptor mosaics) via oligomerization at both pre- and post-synaptic level. These assemblies of receptors together with inter alia single receptors, adapter proteins, G-proteins and ion channels form the membrane bound part of a complex three-dimensional (3D) molecular circuit, the cytoplasmic part of which consists especially of protein kinases, protein phosphatases and phosphoproteins. It is suggested that this molecular circuit has the capability to learn and store information. Thus, engram formation will depend on the resetting of 3D molecular circuits via the formation of new receptor mosaics capable of addressing the transduction of the chemical messages impinging on the cell membrane to certain sets of G-proteins. Short-term memory occurs by a transient stabilization of the receptor mosaics producing the appropriate change in the synaptic weight. Engram consolidation (long-term memory) may involve intracellular signals that translocate to the nucleus to cause the activation of immediate early genes and subsequent formation of postulated adapter proteins which stabilize the receptor mosaics with the formation of long-lived heteromeric receptor complexes. The receptor mosaic hypothesis of the engram formation has been formulated in agreement with the Hebbian rule and gives a novel molecular basis for it by postulating that the pre-synaptic activity change in transmitter and modulator release reorganizes the receptor mosaics at post-synaptic level and subsequently at pre-synaptic level with the formation of novel 3D molecular circuits leading to a different integration of chemical signals impinging on pre- and post-synaptic membranes hence leading to a new value of the synaptic weight. Engram retrieval is brought about by the scanning of the target networks by the highly divergent arousal systems. Hence, a continuous reverberating process occurs both at the level of the neural networks as well as at the level of the 3D molecular circuits within each neuron of the network until the appropriate tuning of the synaptic weights is obtained and, subsequently, the reappearance of the engram occurs. Learning and memory in the basal ganglia is discussed in the frame of the present hypothesis. It is proposed that formation of long-term memories (consolidated receptor mosaics) in the plasma membranes of the striosomal GABA neurons may play a major role in the motivational learning of motor skills of relevance for survival. In conclusion, long-lived heteromeric receptor complexes of high order may be crucial for learning, memory and retrieval processes, where extensive reciprocal feedback loops give rise to coherent synchronized neural activity (binding) essential for a sophisticated information handling by the central nervous system.

Animals↗

Effects of physical guidance and knowledge of results on motor learning: support for the guidance hypothesis.

The guidance hypothesis (Schmidt, 1991) predicts that the guiding properties of augmented feedback are beneficial for motor learning when used to reduce error, but detrimental when relied upon. Therefore, a heavily guiding form of feedback might be detrimental for learning. In addition, the guidance hypothesis predicts that practice with a high relative frequency of augmented feedback would be detrimental for learning. An experiment is described that crossed two forms of feedback with two levels of relative frequency. Subjects practiced movements to a target with either physical guidance or knowledge of results, and with either a high or faded relative frequency. The high frequency physical guidance condition resulted in the poorest retention, and both high frequency feedback conditions resulted in the least accuracy in transfer. These results provide support for the guidance hypothesis and suggest consideration of the combined effects on learning of the type and relative frequency of augmented feedback and acquisition-test conditions.

Adult↗

Motor learning in children with spina bifida: dissociation between performance level and acquisition rate.

The cerebellum is part of a neural circuit involved in procedural motor learning. We examined how congenital cerebellar malformations affect mirror drawing performance, a procedural learning task that involves learning to trace the outline of a star while looking at the reflection of the star in a mirror. Participants were 88 children with spina bifida myelomeningocele, a neural tube defect that results in lesions of the spinal cord, dysmorphology of the cerebellum, and requires shunt treatment for hydrocephalus, and 35 typically developing controls. Participants completed 10 trials in the morning and 10 trials following a 3-hr delay. Although children with spina bifida myelomeningocele were initially slower at tracing and made more errors than controls, all participants improved their performance of the task, as demonstrated by increased speed and accuracy across trials. Moreover, degree of cerebellar dysmorphology was not correlated with level of performance, rate of acquisition, or retention of mirror drawing. The results suggest that congenital cerebellar dysmorphology in spina bifida does not impair motor skill learning as measured by acquisition and retention of the mirror drawing task.

Adolescent↗

Motor learning by imagery is differentially affected in Parkinson's and Huntington's diseases.

Studies of motor imagery and motor learning have thus far been concerned only with its effects on healthy subjects. Therefore, in order to investigate the possible involvement of the basal ganglia, the effectiveness of motor imagery in the acquisition of motor constants in a graphomotor trajectorial learning task was examined in 11 non-demented mildly affected Huntington's disease (HD) patients and 12 non-demented Parkinson's disease (PD) patients. The patients received, after baseline, 10 min of motor imagery training, followed by a motor practice phase. Additionally, a test battery for visual imagery abilities was administered in order to investigate possible relations between visual and motor imagery. The results showed that imagery training alone enabled the HD patients to achieve a significant approach to movement isochrony, whereas the PD patients showed no marked improvements, either with motor imagery or with motor practice. Furthermore, the PD patients had more difficulties than the HD patients in solving the visual imagery tasks. Subsequent correlational analysis revealed significant relationships between the degree of caudate atrophy in the HD patients and their performance in the visual imagery tasks. However, there were no substantial correlations between the performance on the visual imagery tasks and the improvement of motor performance through motor imagery, which indicates that visual and motor imagery are independent processes. It is suggested that the dopaminergic input to the basal ganglia plays an important role in the translation of motor representations into motor performance, whereas the caudate nucleus atrophy of the HD patients does not seem to affect motor imagery, but only the visual imagery process. Furthermore, the deficits found in PD patients might also be related to their limited attentional resources and difficulties in employing predictive motor strategies.

Adult↗

Temporal and amplitude generalization in motor learning.

A fundamental feature of human motor control is the ability to vary effortlessly over a substantial range, both the duration and amplitude of our movements. We used a three-dimensional robotic interface, which generated novel velocity dependent forces on the hand, to investigate how adaptation to these altered dynamics experienced only for movements at one temporal rate and amplitude generalizes to movements made at a different rate or amplitude. After subjects had learned to make a single point-to-point movement in a novel velocity-dependent force field, we examined the generalization of this learning to movements of both half the duration or twice the amplitude. Such movements explore a state-space not experienced during learning-any changes in behavior are due to generalization of the learning, the form of which was used to probe the intrinsic constraints on the motor control process. The generalization was assessed by determining the force field in which subjects produced kinematically normal movements. We found substantial generalization of the motor learning to the new movements supporting a nonlocal representation of the control process. Of the fields tested, the form of the generalization was best characterized by linear extrapolation in a state-space representation of the controller. Such an intrinsic constraint on the motor control process can facilitate the scaling of natural movements.

Adult↗

Motor learning: nonspecific subcortical mechanisms in rats.

Adult rats with bilateral lesions in the globus pallidus, substantia nigra, median raphe, midbrain central gray, or pontine reticular formation were tested for novel motor skill learning (sliding a barrel bolt to the right in order to open a door leading to a reward). Significantly impaired learning was found in animals with lesions to globus pallidus, substantia nigra, median raphe, or pontine reticular formation. These results combined with earlier findings suggest that the foregoing subcortical structures along with the regions of the ventrolateral and parafascicular nuclei of the thalamus constitute a nonspecific mechanism involved not only in motor learning but in discrimination and maze learning as well. This mechanism is contrasted with the more fashionable specific mechanisms which are involved in particular classes of learning; the sensorimotor cortex, for example, would be a component of the specific mechanism underlying motor learning. A subcortical nonspecific learning mechanism may also inhabit the human brain, as suggested by the clinical condition of "subcortical dementia."

Animals↗

Robotics, motor learning, and neurologic recovery.

Robotic devices are helping shed light on human motor control in health and injury. By using robots to apply novel force fields to the arm, investigators are gaining insight into how the nervous system models its external dynamic environment. The nervous system builds internal models gradually by experience and uses them in combination with impedance and feedback control strategies. Internal models are robust to environmental and neural noise, generalized across space, implemented in multiple brain regions, and developed in childhood. Robots are also being used to assist in repetitive movement practice following neurologic injury, providing insight into movement recovery. Robots can haptically assess sensorimotor performance, administer training, quantify amount of training, and improve motor recovery. In addition to providing insight into motor control, robotic paradigms may eventually enhance motor learning and rehabilitation beyond the levels possible with conventional training techniques.

Algorithms↗

Frontal lesions impair the attentional control of movements during motor learning.

This study examined the effects of frontal lobe lesions on the control of movements during motor learning. We compared the performance of patients with unilateral frontal or temporal excisions and controls in two-dimensional aiming movements during adaptation to a transformed visuomotor mapping. Subjects tried to reach a fixed target on a graphics tablet using indirect visual control from a monitor in either: (1) the standard visuomotor mapping, (2) a full inversion of motor space preserving the axis of movement, or (3) a mirror-like inversion of one axis of motor space. In the standard mapping, all groups showed precise and rapid aiming movements. In the full inversion condition, frontal lobe patients showed a stronger tendency than others to initiate movements in the natural direction (capture errors) during adaptation. In the mirror-like inversion, frontal patients showed deficits in both movement initiation and movement corrections. These control deficits disappeared with practice. These data provide evidence for a critical role of frontal cortex in the attentional control of unpracticed movements in man.

Adult↗

The independence of recall and recognition in motor learning.

A basic tenet of both current closed-loop theories of motor learning (Adams, 1971; Schmidt, 1975) is that the generation of response specifications during learning is required for the development of recall memory. Two experiments were performed to test this tenet by attempting to demonstrate the development of recall memory in the absence of response specification production. The task in both experiments required blindfolded subjects to learn to produce a rapid, novel criterion movement on a linear positioning device. Control subjects in both experiments actively produced movements during learning with knowledge of results (KR) while experimental subjects in Experiment 1 experienced only the endpoint locations and in Experiment 2 were passively moved to the endpoint locations. Following initial KR trials, both experimental and control groups attempted to actively produce the criterion movement in the absence of KR. The results of both experiments support closed-loop theory that active practice is required to develop recall memory. There was some suggestion, however, that passive experience with sensory feedback may also aid recall memory development, contrary to the two closed-loop theories.

Journal Article↗