When practice does not make perfect: well-practiced handwriting interferes with the consolidation phase gains in learning a movement sequence

Results obtained in patients with schizophrenia have shown that antipsychotic drugs may induce motor learning deficits correlated with the striatal type-2 dopamine receptors (D₂R) occupancy. Other findings suggest that the role of the striatum in motor learning could be related to a process of “chunking” discrete movements into motor sequences. We therefore hypothesized that a D₂R blocking substance, such as raclopride, would affect motor learning by specifically disrupting the grouping of movements into sequences. Two monkeys were first trained to perform a baseline-overlearned sequence (Seq. A) drug free. Then, a new sequence was learned (Seq. B) and the overlearned sequence was recalled OFF-drug (Seq. A recall OFF-drug). The effect of raclopride was then assessed on the learning of a third sequence (Seq. C), and on the recall of the overlearned sequence (Seq. A recall ON-drug). Results showed that performance related to the overlearned sequence remained the same in the three experimental conditions (Seq. A, Seq. A recall OFF-drug, Seq. A recall ON-drug), whether the primates received raclopride or not. On the other hand, new sequence learning was significantly affected during raclopride treatment (Seq. C), when compared with new sequence learning without the effect of any drug (Seq. B). Raclopride-induced disturbances consisted in performance fluctuations, which persisted even after many days of trials, and prevented the monkeys from reaching a stable level of performance. Further analyses also showed that these fluctuations appeared to be related to monkeys’ inability to group movements into single flowing motor sequences. The results of our study suggest that dopamine is involved in the stabilization or consolidation of motor performances, and that this function would involve a chunking of movements into well-integrated sequences.     

Aging increases the susceptibility to motor memory interference and reduces off-line gains in motor skill learning

Declines in the ability to learn motor skills in older adults are commonly attributed to deficits in the encoding of sensorimotor information during motor practice. We investigated whether aging also impairs motor memory consolidation by assessing the susceptibility to memory interference and off-line gains in motor skill learning after practice in children, young, and older adults. Subjects performed a ballistic task (A) followed by an accuracy-tracking task (B) designed to disrupt the consolidation of A. Retention tests of A were performed immediately and 24 hours after B. Older adults showed greater susceptibility to memory interference and no off-line gains in motor skill learning. Performing B produced memory interference and reduced off-line gains only in the older group. However, older adults also showed deficits in memory consolidation independent of the interfering effects of B. Age-related declines in motor skill learning are not produced exclusively by deficits in the encoding of sensorimotor information during practice. Aging also increases the susceptibility to memory interference and reduces off-line gains in motor skill learning after practice.     

Contribution of night and day sleep vs. simple passage of time to the consolidation of motor sequence and visuomotor adaptation learning

There is increasing evidence supporting the notion that the contribution of sleep to consolidation of motor skills depends on the nature of the task used in practice. We compared the role of three post-training conditions in the expression of delayed gains on two different motor skill learning tasks: finger tapping sequence learning (FTSL) and visuomotor adaptation (VMA). Subjects in the DaySleep and ImmDaySleep conditions were trained in the morning and at noon, respectively, afforded a 90-min nap early in the afternoon and were re-tested 12 h post-training. In the NightSleep condition, subjects were trained in the evening on either of the two learning paradigms and re-tested 12 h later following sleep, while subjects in the NoSleep condition underwent their training session in the morning and were re-tested 12 h later without any intervening sleep. The results of the FTSL task revealed that post-training sleep (day-time nap or night-time sleep) significantly promoted the expression of delayed gains at 12 h post-training, especially if sleep was afforded immediately after training. In the VMA task, however, there were no significant differences in the gains expressed at 12 h post-training in the three conditions. These findings suggest that “off-line” performance gains reflecting consolidation processes in the FTSL task benefit from sleep, even a short nap, while the simple passage of time is as effective as time in sleep for consolidation of VMA to occur. They also imply that procedural memory consolidation processes differ depending on the nature of task demands. J. Doyon and M. Korman contributed equally.     

The role of motor imagery in learning a totally novel movement

The aim of the present study is to gain more insight into the mechanisms underlying mental practice. The question of whether a totally novel movement may be learned by mental practice was investigated. Healthy young adults had to learn the abduction of the big toe (dominant right foot) without moving the other toes or the foot. The subjects were divided into two groups: subjects who were absolutely unable to abduct their big toe ("absolute zero" group) and subjects who were able to abduct their toe to some extent but showed clear room for improvement ("already doing it" group). Two separate experiments were executed. In the first experiment, 37 absolute-zero subjects had to practice, mentally or physically, the target movement. In the second experiment 40 already-doing-it subjects had to improve their toe-abduction skill. The results showed that absolute-zero subjects could not acquire the toe-abduction movement by means of mental practice. Only subjects who physically practiced the target movement improved significantly. Subjects who had some experience in the task (already-doing-it subjects) improved significantly after mental practice as well as after physical practice. The results seem to indicate that it is more plausible to explain the learning effects of mental practice in terms of a "top-down" mechanism based on the activation of a central representation of the movement than in terms of a peripheral "bottom-up" mechanism based on the activation of muscles.     

Motor sequence learning increases sleep spindles and fast frequencies in post-training sleep

STUDY OBJECTIVES: To investigate polysomnographic (PSG) sleep and NREM sleep characteristics, including sleep spindles and spectral activity involved in offline consolidation of a motor sequence learning task. DESIGN: Counterbalanced within-subject design. SETTING: Three weekly visits to the sleep laboratory. PARTICIPANTS: Fourteen healthy participants aged between 20 and 30 years (8 women). INTERVENTIONS: Motor sequence learning (MSL) task or motor control (CTRL) task before sleep. MEASUREMENTS AND RESULTS: Subjects were trained on either the MSL or CTRL task in the evening and retested 12 hours later the following morning on the same task after a night of PSG sleep recording. Total number and duration of sleep spindles and spectral power between 0.5 and 24 Hz were quantified during NREM sleep. After performing the MSL task, subjects exhibited a large increase in number and duration of sleep spindles compared to after the CTRL task. Higher sigma (sigma; 13 Hz) and beta (beta; 18-20 Hz) spectral power during the post-training night's sleep were also observed after the MSL task. CONCLUSIONS: These results provide evidence that sleep spindles are involved in the offline consolidation of a new sequence of finger movements known to be sleep dependent. Moreover, they expand on prior findings by showing that changes in NREM sleep following motor learning are specific to consolidation (and learning), and not to nonspecific motor activity. Finally, these data demonstrate, for the first time, higher fast rhythms (beta frequencies) during sleep after motor learning.     

Learning and transfer of bimanual multifrequency patterns: effector-independent and effector-specific levels of movement representation

Current behavioural theories consider that during motor learning, an effector-independent memory representation of the acquired skill is built up. Using a transfer paradigm, we addressed the nature of the memory representation for a 2:1 multifrequency co-ordination task, requiring, for example, the left arm to cycle twice as fast as the right. After learning this 2:1 pattern, transfer to its converse pattern (i.e., the right arm cycles twice as fast as the left) revealed powerful evidence for negative transfer. The converse task arrangement revealed similar effects. These observations suggest a reconsideration of current viewpoints on movement representations, which emphasize effector independence. Based on the present findings, we propose a new model of motor memory, consisting of an abstract, effector-independent and an effector-specific layer. The abstract code is hypothesized to represent general spatiotemporal movement features, whereas the specific representation refers to effector-related movement commands. This concept is consistent with recent neuroscientific evidence in animal and human species, and invites a reconsideration of current behavioural theories of motor learning and memory.     

Adaptation to rotated visual feedback: a re-examination of motor interference

We have tested human visuo-motor adaptation in rotated-feedback tasks in which subjects first learn to move a cursor to visual targets with a rotational perturbation between joystick and cursor, and are then challenged with the opposing rotation. We then retest the subjects in the original adaptation task, to measure retention of a short-term memory of its earlier learning. Others have used similar tasks and report retrograde interference between one task and the short-term motor memory of the preceding task, such that later performance is impaired. However, we show that in the short-term conditions tested here, these effects can be considered as anterograde interference effects between the two tasks and we find no evidence of retrograde interference.     

Sleep slow oscillations favour local cortical plasticity underlying the consolidation of reinforced procedural learning in human sleep

We investigated changes of slow‐wave activity and sleep slow oscillations in the night following procedural learning boosted by reinforcement learning, and how these changes correlate with behavioural output. In the Task session, participants had to reach a visual target adapting cursor's movements to compensate an angular deviation introduced experimentally, while in the Control session no deviation was applied. The task was repeated at 13:00 hours, 17:00 hours and 23:00 hours before sleep, and at 08:00 hours after sleep. The deviation angle was set at 15° (13:00 hours and 17:00 hours) and increased to 45° (reinforcement) at 23:00 hours and 08:00 hours. Both for Task and Control nights, high‐density electroencephalogram sleep recordings were carried out (23:30?19:30 hours). The Task night as compared with the Control night showed increases of: (a) slow‐wave activity (absolute power) over the whole scalp; (b) slow‐wave activity (relative power) in left centro‐parietal areas; (c) sleep slow oscillations rate in sensorimotor and premotor areas; (d) amplitude of pre‐down and up states in premotor regions, left sensorimotor and right parietal regions; (e) sigma crowning the up state in right parietal regions. After Task night, we found an improvement of task performance showing correlations with sleep slow oscillations rate in right premotor, sensorimotor and parietal regions. These findings suggest a key role of sleep slow oscillations in procedural memories consolidation. The diverse components of sleep slow oscillations selectively reflect the network activations related to the reinforced learning of a procedural visuomotor task. Indeed, areas specifically involved in the task stand out as those with a significant association between sleep slow oscillations rate and overnight improvement in task performance.     

Posttraining epinephrine and memory consolidation in rats with different basic learning capacities The role of the stria terminalis

Rats received bilateral stria terminalis (ST) lesions or were sham-operated. Five days later, the animals were trained in a two-way active avoidance task (one session, 30 trials) and, immediately after the training session, received 0.01 mg/kg i.p. epinephrine or distilled water. Retention was tested 20 days after the acquisition session. In sham-operated groups, epinephrine improved retention in rats that were poor learners and impaired it in rats that were good learners. In poor learners with posttraining epinephrine, lesions of the ST not only blocked the facilitatory effect of epinephrine but also disrupted performance throughout the retention session. In good learners, ST lesions attenuated the disruptive effect of epinephrine. Lesions per se did not affect either acquisition or retention. We conclude that ST is involved in the modulatory effect of posttraining epinephrine on memory consolidation. In addition and considering the results observed in rats that were poor learners, we suggest that emotional factors and/or other amygdaloid pathways different from the ST could participate in the effects of posttraining epinephrine, along with the ST. Received: 12 June 1997 / Accepted: 19 December 1997     

Retrograde amnesia: prolonging the fixation phase of memory consolidation by paradoxical sleep deprivation.

Mice given one-trial training in a passive avoidance task after 3 days of paradoxical sleep (PS) deprivation, and given electroconvulsive shock (ECS) at one of several intervals after training, display a protracted retrograde amnesia gradient on a retention test given 3 days later. ECS produces only a sharp gradient in comparable groups of animals that are not deprived of PS. The findings suggest that PS plays an important functional role in the processes that underlie the fixation of long-term memory.     

Human adaptation to rotated vision: interplay of a continuous and a discrete process

The mechanisms for adaptation to visual rotation were investigated by exposing subjects to different rotation angles in a stepwise fashion. We found that response direction continuously changed to compensate for the imposed rotation, but this change was limited to 90 deg. Larger changes were accomplished by inverting both spatial axes (which is equivalent to a 180 deg rotation), and then gradually changing response direction "backwards" to the prescribed value. The angle of 0 deg had no such limiting value like 90 deg: Response direction could continuously change through 0 deg and beyond. Our data provided no evidence that adaptation to opposite-directed visual rotations results in interference, due to competition in working memory; instead subjects' performance under such conditions is fully explained by the said continuous changes of response direction. We conclude that adaptation is achieved by a coordinated interplay of continuous (gradual rotation between ±90 deg) and discrete (sign reversal) processes.     

Facilitation of generalization performances in spatial learning problems by posttrial stimulation of the mesencephalic reticular formation

The effects of low posttrial stimulation of the mesenphalic reticular formation (MRF) on spatial learning problems were studied in two consecutive stages. First, the performances of stimulated (S) and no-stimulated (NS) subjects were assessed in a reconvergent three-arm maze. Secondly, the same animals were tested in a generalization paradigm, since they had to solve a similar task in a radial four-arm maze, each group being divided into newly stimulated (S-S, NS-S) or no-stimulated (S-NS, NS-NS) subjects. In the first experiment, no differences were found between the acquisition processes of groups S and NS. Conversely, in the second experiment, previously stimulated animals (S-S and S-NS) showed better generalization of the experimental rule. The results are discussed in terms of perseveration of the neural activity after the early MRF stimulation. From a functional point of view, our data indicate that an enhancement of the neural activity during acquisition facilitates not only a high accessibility of memories concerning the experimental rule in a subsequent similar situation but also the capability to apply a previously elaborated response system in a more complex situation.     

The serial reaction time task revisited: a study on motor sequence learning with an arm-reaching task

With a series of novel arm-reaching tasks, we have shown that visuomotor sequence learning encompasses the acquisition of the order of sequence elements, and the ability to combine them in a single, skilled behavior. The first component, which is mostly declarative, is reflected by changes in movement onset time (OT); the second, which occurs without subject’s awareness, is measured by changes in kinematic variables, including movement time (MT). Key-press-based serial reaction time tasks (SRTT) have been used to investigate sequence learning and results interpreted as indicative of the implicit acquisition of the sequence order. One limitation to SRT studies, however, is that only one measure is used, the response time, the sum of OT and MT: this makes interpretation of which component is learnt difficult and disambiguation of implicit and explicit processes problematic. Here, we used an arm-reaching version of SRTT to propose a novel interpretation of such results. The pattern of response time changes we obtained was similar to the key-press-based tasks. However, there were significant differences between OT and MT, suggesting that both partial learning of the sequence order and skill improvement took place. Further analyses indicated that the learning of the sequence order might not occur without subjects’ awareness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Learning two things at once: differential constraints on the acquisition and consolidation of perceptual learning

Learning is often prevented by events that occur after training, an outcome that is usually attributed to the disruption of consolidation—the transfer of learning to long-term memory. Here, we provide evidence from perceptual learning that improvements in performance can also be blocked by intervening events that occur during the acquisition phase of learning—the period of active practice. Listeners improved on each of two conditions of auditory temporal-interval discrimination (100 and 350 ms) when the two were practiced consecutively, even though that is a classic disruption-of-consolidation regimen. However, when practice on these two conditions was interleaved, there was no learning on either condition. The failure to improve in the interleaved case indicates that, at least in some circumstances, learning can be prevented during acquisition by events that do not disrupt consolidation itself. These results thus suggest that acquisition and consolidation are distinct phases in human learning.     

The process of learning a tool-use movement in monkeys, with special reference to vision

Monkeys learned to use forceps to pick up food. The learning progressed in two stages. After having understood the task to have to use forceps through guidance, they (1) brought forceps toward food without seeing food until it was reached (1st stage), and (2) made forceps reach accurately to food using vision (2nd stage). We suggest that the learning without vision was a process of incorporating grasped-forceps into the body-scheme, thus enabling reaching with the extension (forceps) to a certain place in space. Using vision at the final stage was to precisely reach and to pick up food with the extension.     

On the participation of hippocampal PKC in acquisition, consolidation and reconsolidation of spatial memory

Memory consolidation involves a sequence of temporally defined and highly regulated changes in the activation state of several signaling pathways that leads to the lasting storage of an initially labile trace. Despite appearances, consolidation does not make memories permanent. It is now known that upon retrieval well-consolidated memories can become again vulnerable to the action of amnesic agents and in order to persist must undergo a protein synthesis–dependent process named reconsolidation. Experiments with genetically modified animals suggest that some PKC isoforms are important for spatial memory and earlier studies indicate that several PKC substrates are activated following spatial learning. Nevertheless, none of the reports published so far analyzed pharmacologically the role played by PKC during spatial memory processing. Using the conventional PKC and PKCμ inhibitor 12-(2-cyanoethyl)-6,7,12,13-tetrahydro-13-methyl-5-oxo-5H-indolo[2,3-a]pyrrollo[3,4-c]carbazole (Gö6976) we found that the activity of these kinases is required in the CA1 region of the rat dorsal hippocampus for acquisition and consolidation of spatial memory in the Morris water maze learning task. Our results also show that when infused into dorsal CA1 after non-reinforced retrieval, Gö6976 produces a long-lasting amnesia that is independent of the strength of the memory trace, suggesting that post-retrieval activation of hippocampal PKC is essential for persistence of spatial memory.     

Effects of actinomycin D on brain RNA synthesis and discrimination learning in the goldfish (Carassius auratus)

Intracranial injection of actinomycin D 2 microgram inhibited about 70% of the brain RNA synthesis from 3 hr to 4 days after injection in the goldfish. Under these conditions, fish were given 4-day-training of visual discrimination between a card with vertical stripes and one with horizontal stripes. Fish injected intracranially with actinomycin D showed deficits in between-day retention (long-term memory) but not interruption of within-day acquisition (short-term memory). It is suggested that brain RNA synthesis is necessary only for the formation of long-term memory but not short-term memory.     

Long‐term effects of infant learning on adult conditioned odor aversion are determined by the last preweaning experience

We recently showed that odorizing mother's nipples from birth to weaning attenuated adult conditioned odor aversion (COA). The present study evaluated whether shorter durations of preweaning olfactory experiences could induce similar long‐term effects. We first showed that late preweaning odorization (PN13–PN25) impaired adult COA similarly to odorization from birth to weaning (PN0–PN25) whereas early odorization (PN0–PN12) had no effect on adult COA. As early odorization was followed by an odorless suckling period, we evaluated whether this odorless suckling could have interfered with early associative learning. We therefore weaned the animals either immediately after early odorization or 7 days later. Early odorization (PN0–PN18) followed by late odorless suckling (PN19–PN25) had no effect on adult COA. However, pups with early odorization (PN0–PN18) but without late odorless suckling (weaned at PN18) showed attenuated COA. These results support the hypothesis that interference between early and late preweaning experiences with the mother determines the long‐term impact on adult COA. © 2009 Wiley Periodicals, Inc. Dev Psychobiol 51: 389–398, 2009.     

Dreaming of a learning task is associated with enhanced memory consolidation: Replication in an overnight sleep study

Sleep following learning benefits memory. One model attributes this effect to the iterative “reactivation” of memory traces in the sleeping brain, demonstrated in animal models. Although technical limitations prohibit using the same methods to observe memory reactivation in the human brain, the study of mental activity during sleep provides an alternative method of observing memory activation during sleep. In fact, the content of dream experience may reflect the process of memory reactivation and consolidation in the sleeping brain. In line with this hypothesis, we previously reported that dreaming about a spatial learning task during a nap strongly predicts subsequent performance improvements. Here, we replicate this observation in an overnight sleep study, for the first time demonstrating that pre‐sleep training on a virtual maze navigation task is reflected in dreams reported from all phases of sleep, with unambiguous representation of the task in dream content associated with improved next‐morning performance. These observations are consistent with reactivation‐based models of memory consolidation in sleep, confirming our earlier finding that the cognitive‐level activation of recent experience during sleep is associated with subsequent performance gains.     

Relationship of simultaneously recorded cerebellar nuclear neuron discharge to the acquisition of a complex,operantly conditioned forelimb movement in cats

This study was designed to examine the changes in the modulation of small populations of cerebellar neurons during the acquisition of a complex, operantly conditioned forelimb task in cats. The experiments are based on the general postulate that, during the learning of a complex motor behavior, the cerebellum is important for generating a coordinated movement that meets the task's objectives, and that, as the cerebellum participates in this process, it acts to reinforce the effective motor pattern once it has been established. This specific study examines whether the changes in the modulation of cerebellar nuclear neurons during the learning of this task are consistent with this view. Cats were required to learn to move the manipulandum through a novel pattern of 2–3 consecutive straight grooves connected end to end in different spatial configurations, e.g., the letter L, an inverted L, and the letter C. Throughout the acquisition process, 6–12 single units were recorded simultaneously in the cerebellar nuclei, and the kinematics of the movement were evaluated using an Optotrak system. Cells were recorded from the two interposed nuclei and the dentate nucleus in these initial studies. Trials were sorted off-line based on the level of skill at which the required movement was performed. This was assessed using several objective criteria such as movement times, kinematic characteristics, and smoothness (number of peaks in the velocity profile). Event-related histograms then were constructed from each group of sorted trials. Changes in modulation related to a specific event were measured in successive histograms for each neuron. One of the most consistent findings across the cells in all nuclei was that the magnitude of the task-related modulation reached a peak at the time the task was first performed reasonably well and then progressively decreased (but did not disappear) as the task became well practiced. Both the initial increase and the subsequent decrease in response amplitude were significant statistically. The implications of these observations are discussed in the context of the role the cerebellum may play in the acquisition of complex motor tasks.