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The role of working memory in motor learning and performance.

Three experiments explore the role of working memory in motor skill acquisition and performance. Traditional theories postulate that skill acquisition proceeds through stages of knowing, which are initially declarative but later procedural. The reported experiments challenge that view and support an independent, parallel processing model, which predicts that procedural and declarative knowledge can be acquired separately and that the former does not depend on the availability of working memory, whereas, the latter does. The behaviour of these two processes was manipulated by providing or withholding visual (and auditory) appraisal of outcome feedback. Withholding feedback was predicted to inhibit the use of working memory to appraise success and, thus, prevent the formation of declarative knowledge without affecting the accumulation of procedural knowledge. While the first experiment failed to support these predictions, the second and third experiments demonstrated that procedural and declarative knowledge can be acquired independently. It is suggested that the availability of working memory is crucial to motor performance only when the learner has come to rely on its use.

Adult↗

Predicting sensory events. The role of the cerebellum in motor learning.

There is growing evidence that the cerebellum is involved in the implicit learning of movement sequences. On the serial reaction time (RT) task patients with cerebellar lesions fail to demonstrate normal decreases in RT and we have shown a similar effect in monkeys with bilateral cerebellar lesions. However, it is not clear if this impairment is unique to sequence learning or whether the cerebellum is also involved in the learning of discrete responses to predictable visual targets. We investigated this possibility in another group of monkeys with bilateral lesions of the cerebellum centred on the lateral nuclei. Three animals were pre-operatively trained to make rapid manual responses to a single target appearing on a touch-sensitive VDU screen. In one condition, a target could appear at any of three possible locations (spatially unpredictable). In a second condition the target always appeared in the same place (spatially predictable). A third condition was similar to the second except that the onset of the target was temporally predictable whereas in the previous conditions this parameter was randomized. Following the lesions, the RT savings earned on the conditions in which the cues were predictable were abolished. This was despite a lack of significant increase in movement times. The results imply that the animals were either failing to predict the spatial location or time of presentation of the target, or that they were unable to use their prediction to improve their reaction times. The function of the cerebellum in motor sequence learning may therefore be part of a more general operation in learning to prepare responses to predictable sensory events.

Animals↗

Conditional visuo-motor learning in primates: a key role for the basal ganglia.

Sensory guidance of behavior often involves standard visuo-motor mapping of body movements onto objects and spatial locations. For example, looking at and reaching to grasp a glass of wine requires the mapping of the eyes and hand to the location of the glass in space, as well as the formation of a hand configuration appropriate to the shape of the glass. But our brain is far more than just a standard sensorimotor mapping machine. Through evolution, the brain of advanced mammals, in particular human and non-human primates, has acquired a formidable capacity to construct non-standard, arbitrary mapping using associations between external events and behavioral responses that bear no direct relationship. For example, we have all learned to stop at a red traffic light and to go at a green one, or to wait for a specific tone before dialing a phone number and to hang up when hearing a busy signal. These arbitrary associations are acquired through experience, thereby providing primates with a rich and flexible sensorimotor repertoire. Understanding how they are learned, and how they are recalled and used when the context requires them, has been one of the challenging issues for cognitive neuroscience. Valuable insights have been gained over the last two decades through the convergence of multiple complementary approaches. Human neuropsychology and experimental lesions in monkeys have identified a network of brain structures important for conditional sensorimotor associations, whereas imaging studies in healthy human subjects and electrophysiological recordings in awake monkeys have sought to identify the different functional processes underlying the overall function. The present review focuses on the contribution of a network linking the prefrontal cortex, basal ganglia, and dorsal premotor cortex, with special emphasis on results from recording experiments in monkeys. We will first review data pointing to a specific contribution of each component of the network to the performance of well-learned arbitrary visuo-motor associations, as well as data suggesting how novel associations are formed. Then we will propose a model positing that each component of the fronto-striatal network makes a specific contribution to the formation and/or execution of sensorimotor associations. In this model, the basal ganglia are thought to play a key role in linking the sensory, motor, and reward information necessary for arbitrary mapping.

Animals↗

Short- and long-term changes in joint co-contraction associated with motor learning as revealed from surface EMG.

In the field of motor control, two hypotheses have been controversial: whether the brain acquires internal models that generate accurate motor commands, or whether the brain avoids this by using the viscoelasticity of musculoskeletal system. Recent observations on relatively low stiffness during trained movements support the existence of internal models. However, no study has revealed the decrease in viscoelasticity associated with learning that would imply improvement of internal models as well as synergy between the two hypothetical mechanisms. Previously observed decreases in electromyogram (EMG) might have other explanations, such as trajectory modifications that reduce joint torques. To circumvent such complications, we required strict trajectory control and examined only successful trials having identical trajectory and torque profiles. Subjects were asked to perform a hand movement in unison with a target moving along a specified and unusual trajectory, with shoulder and elbow in the horizontal plane at the shoulder level. To evaluate joint viscoelasticity during the learning of this movement, we proposed an index of muscle co-contraction around the joint (IMCJ). The IMCJ was defined as the summation of the absolute values of antagonistic muscle torques around the joint and computed from the linear relation between surface EMG and joint torque. The IMCJ during isometric contraction, as well as during movements, was confirmed to correlate well with joint stiffness estimated using the conventional method, i.e., applying mechanical perturbations. Accordingly, the IMCJ during the learning of the movement was computed for each joint of each trial using estimated EMG-torque relationship. At the same time, the performance error for each trial was specified as the root mean square of the distance between the target and hand at each time step over the entire trajectory. The time-series data of IMCJ and performance error were decomposed into long-term components that showed decreases in IMCJ in accordance with learning with little change in the trajectory and short-term interactions between the IMCJ and performance error. A cross-correlation analysis and impulse responses both suggested that higher IMCJs follow poor performances, and lower IMCJs follow good performances within a few successive trials. Our results support the hypothesis that viscoelasticity contributes more when internal models are inaccurate, while internal models contribute more after the completion of learning. It is demonstrated that the CNS regulates viscoelasticity on a short- and long-term basis depending on performance error and finally acquires smooth and accurate movements while maintaining stability during the entire learning process.

Adult↗

Glutamate-mediated plasticity in corticostriatal networks: role in adaptive motor learning.

Little is known about how memories of new voluntary motor actions, also known as procedural memory, are formed at the molecular level. Our work examining acquisition of lever-pressing for food in rats has shown that activation of glutamate NMDA receptors, within broadly distributed but interconnected regions (e.g., nucleus accumbens core, prefrontal cortex, basolateral amygdala), is critical for such learning to occur. This receptor stimulation triggers intracellular cascades that involve protein phosphorylation and new protein synthesis. In support of this idea, we have found that posttrial inhibition of protein synthesis in the ventral striatum impairs learning, whereas posttrial NMDA receptor blockade does not. More recent data show extension of this network to the central amygdala, where infusions of NMDA antagonists also impair learning. We hypothesize that activity in this distributed network (including dopaminergic activity and perhaps muscarinic cholinergic activity) computes coincident events and thus enhances the probability that temporally related actions and events (e.g., lever pressing and delivery of reward) become associated. Such basic mechanisms of plasticity within this reinforcement learning network also appear to be profoundly affected in addiction.

Adaptation, Psychological↗

Motor learning in children with spina bifida: intact learning and performance on a ballistic task.

Learning and performance on a ballistic task were investigated in children with spina bifida meningomyelocele (SBM), with either upper level spinal lesions (n = 21) or lower level spinal lesions (n = 81), and in typically developing controls (n = 35). Participants completed three phases (20 trials each) of an elbow goniometer task that required a ballistic arm movement to move a cursor to one of two target positions on a screen, including (1) an initial learning phase, (2) an adaptation phase with a gain change such that recalibration of the ballistic arm movement was required, and (3) a learning reactivation phase under the original gain condition. Initial error rate, asymptotic error rate, and learning rate did not differ significantly between the SBM and control groups. Relative to controls, the SBM group had reduced volumes in the cerebellar hemispheres and pericallosal gray matter (the region including the basal ganglia), although only the pericallosal gray matter was significantly correlated with motor adaptation. Congenital cerebellar dysmorphology is associated with preserved motor skill learning on voluntary, nonreflexive tasks in children with SBM, in whom the relative roles of the cerebellum and basal ganglia may differ from those in the adult brain.

Adaptation, Physiological↗

Impaired motor learning in children with hydrocephalus.

Hydrocephalic (n = 19) and normal (n = 20) children in two age groups (averaged at 10 and 14 years old) were asked to learn 5 predetermined timing rhythm interval tasks (including timing duration and relative timing pattern) by pressing keys on a computer keyboard. In the acquisition phase, visual and auditory goal timing intervals, as well as visualized feedback were presented to all participants before and after their key presses, respectively. A retention test without the auditory information and visualized feedback was administered 1 day later. By using the computerized timing test, we demonstrated in this study that the hydrocephalic group had significantly (ANOVA analysis) increased relative timing errors; this function depends on the formation of an internal model or a motor program related to long-term memory disorders. These findings could lead to the formulation of training procedures with simplified movements that may help hydrocephalic children improve their motor skill learning.

Adolescent↗

Motor learning enhances perceptual judgment: a case for action-perception transfer.

Transfer from perception to action is well documented, for instance in the form of observational learning. Transfer from action to perception, on the other hand, has not been researched. Such action-perception transfer (APT) is compatible with several learning theories and has been predicted within the framework of common coding of perceptual and motor events (Prinz, 1992, 1997). Our first experiment aimed at an empirical evaluation of APT and involved motor practice of timed two-cycle arm movements on verbal command without visual feedback. In a transfer test, visual judgments of similar patterns had to be made. In addition, transfer from the visual to the motor task was studied. In Experiment 2 we separated kinesthetic aspects of motor practice from preparatory and efferent contributions to APT. The experiments provide evidence that transfer between perception and action is bi-directional. Transfer from perception to action and, more importantly, from action to perception was found. Furthermore, APT was equally pronounced for participants who had actively practiced movements during training and for passive participants who had received merely kinesthetic feedback about the movement. This kinesthetic-visual transfer is likely to be achieved via visuomotor-kinesthetic matching or via timekeeping mechanisms that are involved in both motor and visual performance.

Adult↗

Frontal and parietal networks for conditional motor learning: a positron emission tomography study.

Studies on nonhuman primates show that the premotor (PM) and prefrontal (PF) areas are necessary for the arbitrary mapping of a set of stimuli onto a set of responses. However, positron emission tomography (PET) measurements of regional cerebral blood flow (rCBF) in human subjects have failed to reveal the predicted rCBF changes during such behavior. We therefore studied rCBF while subjects learned two arbitrary mapping tasks. In the conditional motor task, visual stimuli instructed which of four directions to move a joystick (with the right, dominant hand). In the evaluation task, subjects moved the joystick in a predetermined direction to report whether an arrow pointed in the direction associated with a given stimulus. For both tasks there were three rules: for the nonspatial rule, the pattern within each stimulus determined the correct direction; for the spatial rule, the location of the stimulus did so; and for the fixed-response rule, movement direction was constant regardless of the pattern or its location. For the nonspatial rule, performance of the evaluation task led to a learning-related increase in rCBF in a caudal and ventral part of the premotor cortex (PMvc, area 6), bilaterally, as well as in the putamen and a cingulate motor area (CM, area 24) of the left hemisphere. Decreases in rCBF were observed in several areas: the left ventro-orbital prefrontal cortex (PFv, area 47/12), the left lateral cerebellar hemisphere, and, in the right hemisphere, a dorsal and rostral aspect of PM (PMdr, area 6), dorsal PF (PFd, area 9), and the posterior parietal cortex (area 39/40). During performance of the conditional motor task, there was only a decrease in the parietal area. For the spatial rule, no rCBF change reached significance for the evaluation task, but in the conditional motor task, a ventral and rostral premotor region (PMvr, area 6), the dorsolateral prefrontal cortex (PFdl, area 46), and the posterior parietal cortex (area 39/40) showed decreasing rCBF during learning, all in the right hemisphere. These data confirm the predicted rCBF changes in premotor and prefrontal areas during arbitrary mapping tasks and suggest that a broad frontoparietal network may show decreased synaptic activity as arbitrary rules become more familiar.

Adult↗

Motor learning as a function of KR schedule and characteristics of task-intrinsic feedback.

Forty participants (age range = 18-35 years) practiced 1 of 2 versions of an aiming task (with or without spring resistance). Knowledge of results (KR) was provided to them either immediately or after a delay of 2 trials. Immediate KR led to significantly more accurate performance during the 80 trials in acquisition but significantly less accurate performance on a 40-trial retention test given 24 hr after practice. In addition, the spring version of the task was performed significantly less accurately than the no-spring version on the 24-hr retention test. Most important, a significant interaction on the 24-hr retention test revealed that performance of the no-spring version of the task, when KR had been given after a 2-trial delay, was significantly more accurate than performance of the other 3 combinations of task version and KR schedule. The results suggest that KR dependency in motor skill learning is related to familiarity with task-intrinsic feedback in addition to the schedule on which KR is presented.

Adolescent↗

Learning motor synergies makes use of information on muscular load.

Prism adaptation, a form of procedural learning, requires the integration of visual and motor information for its proper acquisition. Although the role of the visual feedback has begun to be understood, the nature of the motor information necessary for the development of the adaptation remains unknown. In this work we have tested the idea that modifying the arm load at different stages of the adaptation process, and the ensuing change of motor information perceived by the subjects, would modify the final properties of the adaptation. We trained a set of subjects to throw balls to a target while wearing prism glasses and varied the weight of their arms at different time points during the task. We observed that the acquisition of the adaptation was not affected by the change in load. However, its persistence (i.e., the aftereffect) was reduced when tested under a weight condition different from the training trials. Furthermore, when the training weight conditions were restored later during testing, a second, late aftereffect was unmasked, suggesting that the missing aftereffect did not disappear but had remained latent. Our results show that the internal representation of a motor memory incorporates information about load conditions and that the memory stored under a specific weight condition can be fully retrieved only when the original training condition is restored.

Adolescent↗

Qualitative and quantitative knowledge of results: effects on motor learning.

OBJECTIVE: This study investigated the effects of qualitative and quantitative knowledge of results (KR) on the acquisition of a motor skill. It was hypothesized that there would be differences in performance during skill acquisition and retention, depending on the type of feedback given. Qualitative KR was in the form of verbal encouragement and quantitative KR was in the form of an algebraic number representing an error score. METHODS: Seventy-seven adults were randomly assigned to one of four feedback conditions, Quantitative, Qualitative, Quantitative and Qualitative, and no feedback (Control). Participants learned an isometric force production skill. Data were collected during skill acquisition and retention phases. Computer hardware and custom software were used to collect data and administer the feedback conditions of the independent variable. RESULTS: There was a statistically significant difference in the Acquisition Phase for the main effect of Condition F(3,73) = 6.35, p < .05, and for Block F(9,657) = 2.07, p < .05, but there was no statistically significant Condition X Block interaction F(27,657) = 1.02, p > .05. Pair-wise comparisons revealed statistically significant differences between conditions containing qualitative feedback and conditions containing no qualitative feedback (p < .05). The main effect of condition was significant F(3,73) = 3.00, p < .05 in the retention phase, however there were no significant pair-wise comparisons (p > .05). CONCLUSION: The results of this study suggest that in a healthy adult population, qualitative feedback, by itself and when combined with quantitative feedback, resulted in superior skill acquisition, but not in the retention of that skill. The artificiality of the task along with differing modes of feedback (audible versus visual) are two potentially limiting factors to this study. Future research that controls for these factors may yield more definitive findings about the role that qualitative feedback has in improving motor performance and learning.

Adolescent↗

Distinct contribution of the striatum and cerebellum to motor learning.

The striatum and cerebellum have been shown to be key structures of a distributed system for the control of skilled movements. However, the mechanisms under which they operate remain unclear. This study compared the performance of patients with Parkinson's disease (PD) or with cerebellar damage (CE) to that of age-matched controls. Each group performed two visuomotor paradigms: a random variant of the serial reaction time (SRT) task that tested the subject's ability to make efficient stimulus-response associations and an adapted version of the mirror-tracing task that measured their capacity to combine simple movements into complex ones. PD patients with bilateral striatal damage showed an impaired learning profile on the SRT task and a normal facilitation effect in the tracing task, while CE patients showed the reverse pattern. Although further research is needed, the present findings suggest that the striatum and cerebellum are involved in distinct learning mechanisms.

Cerebellum↗

Motor learning processes in a movement-scaling task in olivopontocerebellar atrophy and Parkinson's disease.

Nine Parkinson's disease (PD), seven olivopontocerebellar atrophy (OPCA) patients and two age-matched control groups learned a linear arm movement-scaling task over 2 days, requiring movements proportional in length to visually presented target-bars. Scaling was acquired through knowledge of results (KR concerning the direction and magnitude of errors) following every second acquisition trial. Initial acquisition of both groups was significantly worse than their respective controls (poorer movement scaling), but rapidly improved to nearly identical levels. Retention for the PD group's movement scaling was as good as controls initially, but markedly poorer after 24 h. The OPCA group did not show this deficit. Both patient groups extrapolated accurately to longer, previously unpracticed target distances (no KR provided), suggesting an unimpaired capacity to generate and use an internal representation of the movement scaling. They also rapidly learned a new scaling relationship when the gain was changed. Overall, the learning of this movement-scaling task was not adversely affected in OPCA, and the impairment was restricted primarily to longer-term retention in PD. The study suggests that: (1) the ability to acquire movement scaling in a task that requires conscious use of error feedback and no new coordination may depend little on the cerebellum, and (2) the basal ganglia may participate in longer-term storage of scaling information.

Adult↗

A multimuscle state analysis of adult motor learning.

We introduce a new EMG state analysis to test two competing hypotheses about the role of muscle coactivity in learning a complex, multijoint reaching movement. Following Bernstein, one hypothesis is that as a task is learned, coactivity should decrease as degrees of freedom are released and limb stiffness is reduced. An alternative hypothesis is that as movement speed increases with learning, muscle coactivity should increase, possibly to stabilize joints against high inertial forces. Three participants performed a vertical reaching movement identical to that used by Schneider et al. We monitored the activity of four arm and shoulder muscles as participants completed 100 practice trials. Each frame of EMG activity was assigned to one of 16 possible combinations of the four monitored muscles based on an on-off activation threshold. This analysis yielded a time-based summary of muscle coactivity during the movement and across practice trials. Results of the state analysis supported the second hypothesis. As participants decreased their movement times over practice, coactivity increased - participants used more three- and four-muscle coactivity states. Changes were especially dramatic during the braking phase of the Up and Down portion of the vertical movement. When participants performed deliberately slow movements after speeded practice, three- and four-muscle coactivity was suppressed. We suggest that increased use of muscle coactivity may serve to counteract unwanted rotational forces generated during fast movements.

Adult↗

Cognitive-motor learning in Parkinson's disease.

Procedural learning deficits are common in Parkinson's disease (PD), but contradictory results have been reported in rotary pursuit learning. This article compared rotary pursuit learning in 2 nondemented PD groups and 2 normal control (NC) groups, using a between-subjects group design in which 3 rotation speeds were presented either randomly or in blocks. The pattern of learning differed between the randomized and the blocked conditions in the NC, but not in the PD groups. Learning was impaired in the PD group in the random condition only. Memory, visuospatial, or executive skills were not associated with the PD group's poorer learning in the randomized context. Results show that procedural learning deficits are not universal with basal ganglia abnormalities but rather depend on the specific cognitive requirements of the learning context.

Aged↗