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Anatomy of motor learning. II. Subcortical structures and learning by trial and error.

We used positron emission tomography to study motor learning by trial and error. Subjects learned sequences of eight finger movements. Tones generated by a computer told the subjects whether any particular move was correct or incorrect. A control condition was used in which the subjects generated moves, but there was no feedback to indicate success or failure, and so on learning occurred. In this condition (free selection) the subjects were required to make a finger movement on each trial and to vary the movements randomly over trials. The subjects had a free choice of which finger to move on any one trial. On this task there was no systematic change in responses over trials and no change in the response times. Two other conditions were included. In one the subjects repetitively moved the same finger on all trials and in a baseline condition the subjects heard the pacing tones and auditory feedback but made no movements. Comparing new learning with the free selection task, there was a small activation in the right prefrontal cortex. This may reflect the fact that in new learning, but not free selection, the subject rehearse past moves and adapt their responses accordingly. The caudate nucleus was strongly activated during new learning. It is suggested that this activity may be related either to mental rehearsal or to reinforcement of the movements as a consequence of the outcomes. The putamen was activated anteriorly on the free selection task and more posteriorly when the subjects repetitively made the same movement. It is suggested that the differences in the location of the peak activation in the striatum may represent the operation of different corticostriatal loops. The cerebellar nuclei (bilaterally) and vermis were more active in the new learning condition than during the performance of the free selection task. There was no difference in the activation of the cerebellum when the free selection task was compared with repetitive performance of the same movement. We tentatively suggest that the basal ganglia may be involved in the specification of movement on the basis of memory of either the movements or the outcomes, but that the cerebellum may be more directly involved in changes in the parameters of movement execution.

Acoustic Stimulation↗

Reversal of motor learning in the vestibulo-ocular reflex in the absence of visual input.

Motor learning in the vestibulo-ocular reflex (VOR) and eyeblink conditioning use similar neural circuitry, and they may use similar cellular plasticity mechanisms. Classically conditioned eyeblink responses undergo extinction after prolonged exposure to the conditioned stimulus in the absence of the unconditioned stimulus. We investigated the possibility that a process similar to extinction may reverse learned changes in the VOR. We induced a learned alteration of the VOR response in rhesus monkeys using magnifying or miniaturizing goggles, which caused head movements to be accompanied by visual image motion. After learning, head movements in the absence of visual stimulation caused a loss of the learned eye movement response. When the learned gain was low, this reversal of learning occurred only when head movements were delivered, and not when the head was held stationary in the absence of visual input, suggesting that this reversal is mediated by an active, extinction-like process.

Animals↗

Human muscle spindle response in a motor learning task.

1. Impulse discharge of single muscle spindle afferents from the finger extensor muscles was recorded in the radial nerve of conscious human subjects, during a motor learning task engaging the metacarpo-phalangeal joint of a single finger, using the microneurography technique. 2. Subjects were requested first to pay attention to a complex sequence of imposed single joint movements, and immediately afterwards to reproduce actively the same sequence. No external load was added to the finger and visual control was denied altogether so that subjects relied on mechanoreceptor input exclusively for the sampling and reproduction of movement. In addition, sequences of imposed movements were delivered while subjects were not attending in order to allow analysis of the attention effect. 3. The response of the individual unit was uniform in repeated tests. There were clear differences between spindle firing rate in imposed and actively reproduced movements with most units. However, the difference was complex during the individual sequence, in that firing rate was usually higher during periods of reproduced movements when the muscle was relatively short whereas it was identical when the muscle was relatively long. 4. The hypothesis that reproduction and verification of an imposed movement may be based on simple matching between identical spindle firing in imposed and active movements, was difficult to reject altogether because identical spindle input was present during considerable sections of the movement sequence. It may be speculated that agonists and antagonists cover different ranges of joint excursion, with identical spindle firing rates in imposed and reproduced movements. 5. Attention to imposed movements was associated with a minute and inconsistent increase of spindle firing rate in some afferents and then usually with a slight increase of EMG activity of the parent muscle as well. 6. It was concluded that focusing attention on the kinaesthetic input during imposed movement was not associated with a consistent increase of fusimotor drive.

Action Potentials↗

Motor learning by observation: evidence from a serial reaction time task.

This study sought evidence of observational motor learning, a type of learning in which observation of the skilled performance of another person not only facilitates motor skill acquisition but does so by contributing to the formation of effector-specific motor representations. Previous research has indicated that observation of skilled performance engages cognitive processes similar to those occurring during action execution or physical practice, but has not demonstrated that these include processes involved in effector-specific representation. In two experiments, observer subjects watched the experimenter performing a serial reaction time (SRT) task with a six-item unique sequence before sequence knowledge was assessed by response time and/or free generation measures. The results suggest that: (1) subjects can acquire sequence information by watching another person performing the task (Experiments 1-2); (2) observation results in as much sequence learning as task practice when learning is measured by reaction times (RTs) and more than task practice when sequence learning is measured by free generation performance (Experiment 2, Part 1); and (3) sequence knowledge acquired by model observation can be encoded motorically--that is, in an effector-specific fashion (Experiment 2, Part 2).

Adult↗

Conjugate limb coordination after experience with an interlimb yoke: evidence for motor learning in the rat fetus.

This study investigated the capacity of the E20 rat fetus to adaptively alter patterns of interlimb coordination in a prenatal model of motor learning. Fetal limb movement was manipulated with an interlimb yoke, consisting of a fine thread attached at the ankles, which created a physical linkage between two limbs. Exposure to the yoke resulted in a gradual increase in conjugate movements of the yoked limbs during a 30-min training period, which persisted after removal of the yoke. Training effects were evident when the yoke was applied to two hindlimbs, two forelimbs, or a homolateral forelimb-hindlimb pair. A savings in the rate of acquisition also was observed when fetuses experienced yoke training in a second session. These data argue that the rat fetus can respond to kinesthetic feedback resulting from variation in motor performance, which suggests that experience contributes to the development of coordinated motor behavior before birth.

Analysis of Variance↗

[Motor learning with the minimal involvement of visual afferentation].

Amongst motor control and learning models, "A Cerebellar Model of Timing and Prediction" of A. Barto and J. Houk is the most interesting and physiologically well-grounded. Developing D. Marr's "The Theory of Cerebellar Cortex", this model proposed the important role in motor learning of the ability of Purkinje cells to change their activity level by the dendritic bistability mechanism. The aim of this investigation was to verify this idea in experiments with human learning of precise elbow flexion. The unsupervisual method of learning was used in order to guarantee the principal role of proprioception in training. The experiments were carried out in darkness to exclude the vision control. Subjects were asked to perform a precise horizontal elbow flexion as fast as possible and repeat this action from 30 to 50 times up to the point of complete movement acquisition (stable movement with the error in the range of 5% of a given flexion amplitude). The target point (a given angle of the horizontal elbow flexion) was not presented to the subjects in advance. Reaching the target point was indicated by a short light flash. During training, subjects learned to hit target point with the given precision. Kinematic characteristics of the movement (time change of elbow flexion angle, velocity, and acceleration) together with EMG of the flexor and extensor were recorded. The obtained results were in good agreement with J. Houk and A. Barto's hypothesis. Analysis of changes in the kinematic characteristics in the course of training revealed an asymmetric velocity profile and a fragmentary shape of acceleration profile at the beginning of learning. In the course of training, the acceleration profile transformed into biphasic curve with a single change in polarity. Thus, it acquired a characteristic shape of a plateau. Correspondingly, to the end of training, the character of the asymmetry of the velocity profile changed. No correlation was observed between the velocity parameters and movement precision. These features essentially distinguish the motor reactions under study from the common visuomotor coordinations. It is suggested that the amplitude and duration of the acceleration plateau reflect the intensity and time of inhibition of the descending activity of Purkinje cells as a result of bistability (in accordance with Houk and Barto's hypothesis).

Adolescent↗

A mental route to motor learning: improving trajectorial kinematics through imagery training.

There are contrasting reports upon the level of effectiveness of motor imagery in learning new motor skills, but there is general consensus that motor imagery can lead to improvements in performance, especially in combination with physical practice. In the present study we examined the effectiveness of motor imagery in the acquisition of movement invariants in two grapho-motor trajectorial learning tasks with differing visuospatial components: 'Ideogram drawing' and 'connecting circles'. Two subject groups were studied: An imagery group, which underwent 10 min of motor imagery training and a control group, which practised a control visuomotor task over the same period of time. The results showed that imagery training alone enabled the subjects to achieve a significant approach to movement isochrony as well as a significant shifting of peak velocity toward the target. After a practice phase, both groups improved their performance, but the imagery group was still significantly faster than the control group. Furthermore, a series of tests measuring visual imagery abilities was administered to the subjects. There were however no significant relationships between the motor performance and the visual imagery ability levels of the subjects. It is concluded that motor imagery can improve the acquisition of the spatio-temporal patterns of grapho-motor trajectories and that there are different processes involved in visual and motor imagery.

Adult↗

A neo-Piagetian investigation of the serial position effect in children's motor learning.

Children's serial motor skill acquisition was studied within a neo-Piagetian framework. High and low M-processors performed on a curvilinear repositioning task. A primacy-recency effect was evidenced for both groups on the age-related task, while a recency effect occurred for only the high M-processors on the task one stage beyond the developmental processing capacity of the subjects. High M-processors were more accurate and less variable than low M-processors. Although low M-processors performed better on the more complex task than on the simpler one, their performance never exceeded that of the high M-processors. Implications of these results for future research were discussed.

Journal Article↗

Motor learning in rats: modification of the pattern of reaching and licking by operant conditioning.

Motor learning was studied in computer controlled experiments in which the prolongation of a definite phase of a discrete movement was reinforced by intracranial selfstimulation or by the offer of water. In Experiment 1, rats slowed down the retraction phase of the lateralized reaching reaction from 300 ms to 512 ms. In Experiment 2, rats learned to follow computer generated spout movement by increasing the interlick interval or by alternating long and short licks.

Animals↗

Drifting towards a diffuse control model of exploratory motor learning: A comparison of global and within-trial performance measures.

Accurate measurement is crucial for understanding the processes that underlie exploratory patterns in motor learning. Accordingly, measures of learning should be sensitive to the changes that take place during skill acquisition. Most studies, however, use trial-based global measures that assess performance but do not actually measure gradual changes taking place within trials. The present study attempted to remedy this shortcoming by analysing a visual adaptation task, and comparing traditional global measures of learning with new, within-trial measures. Movement time was the only global measure sensitive to changes in the movement trajectory during learning. Three new measures were expected to reveal changes to the movement trajectory that are associated with learning: (i) the length of runs, (ii) change of trajectory angle in relation to the target, and (iii) drift (change in distance from the target). All three measures were sensitive to learning and indicated a gradual straightening of the movement trajectories over trials. Furthermore, three different methods to partition trajectories into segments were examined. The new within-trial measures, irrespective of partitioning method, prove promising for the development of a diffuse control model of exploratory learning.

Exploratory Behavior↗

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↗

Report on a workshop concerning the cerebellum and motor learning, held in St Louis October 2004.

A one-day meeting on the cerebellum and motor learning was held in St Louis (October 2004), to address issues arising from a previous larger meeting (Tuebingen, June 2004). The learning tasks considered were VOR adaptation, saccadic adaptation and eyeblink conditioning. A theoretical development was reported that indicated how the cerebellum could use sensory error signals for adaptive control, by decorrelating them from an efferent copy of motor commands. The main topics for discussion were the nature of the error signals actually used by the cerebellum, and the evidence for multiple sites of synaptic plasticity. Reports of studies on VOR adaptation confirmed the presence of error signals in addition to retinal slip, in particular the eye-movement related simple-spike firing of floccular PCs. This firing appears to drive synaptic plasticity in the vestibular nuclei. From a theoretical perspective, a second site of plasticity in the brainstem has two advantages: it improves the high-frequency performance of the VOR given a delayed slip signal, and it allows VOR adaptation when smooth pursuit effectively removes the retinal slip signal. In contrast, some of the physiological data reported on saccadic adaptation seemed incompatible with current theoretical ideas about error signals. However, since other reported data were broadly consistent with those ideas, an important area of experimental disagreement was identified. Furthermore, behavioural studies indicated the presence of multiple sites of plasticity, consistent with earlier lesion studies that suggested one such site within cerebellar cortex and another outside it. Data from eyeblink conditioning suggested that the predictability of the error signal was important. Related ideas have previously emerged from studies of skeletal movement, but their theoretical implications for the cerebellar algorithm have yet to be fully explored. Finally, the long-standing controversy concerning sites of plasticity in eyeblink conditioning illustrated the technical difficulties involved in tracking down such sites.

Adaptation, Physiological↗

Motor learning of compatible and incompatible visuomotor maps.

Brain imaging studies demonstrate increasing activity in limb motor areas during early motor skill learning, consistent with functional reorganization occurring at the motor output level. Nevertheless, behavioral studies reveal that visually guided skills can also be learned with respect to target location or possibly eye movements. The current experiments examined motor learning under compatible and incompatible perceptual/motor conditions to identify brain areas involved in different perceptual-motor transformations. Subjects tracked a continuously moving target with a joystick-controlled cursor. The target moved in a repeating sequence embedded within random movements to block sequence awareness. Psychophysical studies of behavioral transfer from incompatible (joystick and cursor moving in opposite directions) to compatible tracking established that incompatible learning was occurring with respect to target location. Positron emission tomography (PET) functional imaging of compatible learning identified increasing activity throughout the precentral gyrus, maximal in the arm area. Incompatible learning also led to increasing activity in the precentral gyrus, maximal in the putative frontal eye fields. When the incompatible task was switched to a compatible response and the previously learned sequence was reintroduced, there was an increase in arm motor cortex. The results show that learning-related increases of brain activity are dynamic, with recruitment of multiple motor output areas, contingent on task demands. Visually guided motor sequences can be linked to either oculomotor or arm motor areas. Rather than identifying changes of motor output maps, the data from imaging experiments may better reflect modulation of inputs to multiple motor areas.

Adult↗

Purkinje cell activity during motor learning.

Monkeys were trained to grasp a handle and move it in a horizontal arc to a central position by flexing or extending the wrist. A torque motor applied forces to the handle that switched at random intervals to alternately load flexor and extensor muscles. At each load switch, the handle was displaced transiently from the central position, and then moved back by the monkeys and held there steadily again. Recordings were made from cerebellar Purkinje cells (P-cells) whose simple spike (SS) activity was related to the task. The magnitude of one of the oppositely directed loads was then altered and the monkeys took about 12-100 trials with the novel load before performing as regularly as previously. During this period with one known and one novel load, some P-cells underwent increases in complex spike (CS) frequency at specific times after the load switch. This increased CS frequency would last for a similar number of trials as that taken by the monkey to adapt to the novel load before decreasing to near its previous level. Associated with the increased CS frequency ther were decreases in SS frequency that persisted after the CS frequency had decreased to near its previous level. These results are consistent with theoretical proposals that motor learning takes place in the cerebellum through changes in the strength of transmission of parallel fiber synapses on P-cells caused by the climbing fiber input. These results further suggest that climbing fiber firing causes a decrease in the strength of parallel fiber synapses.

Action Potentials↗

Motor learning after recovery from hemiparesis.

Twenty patients who had almost completely recovered from hemiparesis following unilateral cerebrovascular accident and 16 control subjects had to perform motor learning tasks including a three-dimensional motor problem and two standard precision tests. The ability of hemiparetic patients to solve simple spatial-motor problems and to gain by training was preserved with limitations concerning high precision control. However, hemiparetic patients had a higher demand for time and corrections, as well as a reduced consistency of performance. Thus recovery from hemiparesis was accompanied by reduced skillfulness and automaticity of motor control.

Adult↗

Motor learning and ultradian sleep cycle: an electroencephalographic study of trampoliners.

Evidence from both animal experiments and human studies suggests that sleep might be involved in neuronal and biochemical mechanisms of learning. In the present study distinct changes in the temporal organization of sleep stages were observed in 8 volunteers participating in a training course in trampolining. Since trampolining requires the acquisition of unaccustomed motor skills, it can be regarded as a special case of motor learning. Subjects who were able to acquire new motor skills during distinct training units in trampolining showed an increase in sleep-cycle period and mean duration of REM and slow-wave sleep. These results are discussed with respect to biochemical mechanisms which may be involved in both learning and organization of sleep stages.

Activity Cycles↗

Functional connectivity of cortical networks involved in bimanual motor sequence learning.

Motor skill learning requires the involvement and integration of several cortical and subcortical regions. In this study, we focus on how the functional connectivity of cortical networks changes with the acquisition of a novel motor skill. Using functional magnetic resonance imaging, we measured the localized blood oxygenation level-dependent (BOLD) signal in cortical regions while subjects performed a bimanual serial reaction time task under 2 conditions: 1) explicitly learning a novel sequence (NOVEL) and 2) playing a previously learned sequence (LEARNED). To investigate stages of learning, each condition was further divided into nonoverlapping early and late conditions. Functional connectivity was measured using a task-specific low-frequency coherence analysis of the data. We show that within the cortical motor network, the sensorimotor cortex, premotor cortex, and supplementary motor area have significantly greater inter- and intrahemispheric coupling during the early NOVEL condition compared with the late NOVEL condition. Additionally, we observed greater connectivity between frontal regions and cortical motor regions in the early versus late NOVEL contrast. No changes in functional connectivity were observed in the LEARNED condition. These results demonstrate that the functional connectivity of the cortical motor network is modulated with practice and suggest that early skill learning is mediated by enhanced interregional coupling.

Adult↗

Task goals and change in dynamical degrees of freedom with motor learning.

In this article, the authors examined the hypothesis that the direction of the change (increase or decrease) in the dynamical degrees of freedom (dimension) regulated as a function of motor learning is task-dependent. Adult participants learned 1 of 2 isometric force-production tasks (Experiment 1: constant force output; Experiment 2: sinusoidal force output) over 5 days of practice and a 6th day with augmented information withdrawal. The results showed that over practice, the task goal induced either an increase (Experiment 1) or a decrease (Experiment 2) in the dimension of force output as performance error was reduced. These findings support the proposition that the observed increase or decrease in dimension with learning is dependent on both the intrinsic dynamics of the system and the short-term change required to realize the task goal.

Adaptation, Physiological↗