Motor sequence consolidation: constrained by critical time windows or competing components

Skill improvements may develop between practice sessions during memory consolidation. Skill enhancement within an egocentric coordinate frame develops over wake, whereas skill enhancement in an allocentric coordinate frame develops over a night of sleep. We tested whether both types of improvement could develop over two different 24-h intervals: 8 am to 8 am or from 8 pm to 8 pm. We found that for each 24 h interval, only one type of skill improvement was seen. Despite passing through wake and a night of sleep participants only showed skill improvements commensurate with either a night of sleep or a day awake. The nature of the off-line skill enhancement was determined by when consolidation occurred within the normal sleep–wake cycle. We conclude that motor sequence consolidation is constrained either by having critical time windows or by a competitive interaction in which improvements within one co-ordinate frame actively block improvements from developing in the alternative co-ordinate frame.     

Motor sequence learning with the nondominant left hand

Whereas the human right hemisphere is active during execution of contralateral hand movements, the left hemisphere is engaged for both contra- and ipsilateral movements, at least for right-handed subjects. Whether this asymmetry is also found during motor learning remains unknown. Implicit sequence learning by the nondominant left hand was examined with the serial reaction time (SRT) task during functional brain imaging. As learning progressed, increases in brain activity were observed in left lateral premotor cortex (PMC) and bilaterally in supplementary motor areas (SMA), with the increase significantly greater in the left hemisphere. The left SMA site was similar to one previously identified with right-hand learning, suggesting that this region is critical for representing a sequence independent of effector. Learning with the left hand also recruited a widespread set of temporal and frontal regions, suggesting that motor skill learning with the nondominant hand develops within both cognitive and motor-related functional networks. After skill acquisition, subjects performed the SRT task with their right hands, and sequence transfer was tested with the original and a mirror-ordered sequence. With the original sequence, the stimulus sequence and series of response locations remained unchanged, but the finger movements were different. With the mirror-ordered sequence, the response sequence involved finger movements homologous to those used during training. Performance of the original and mirror sequence by the right hand was significantly better than with random stimuli. Mirror transformation of the sequence by the right hand was associated with a marked increase in regional activity in the left motor cortex, consistent with a role for sequential transformation at this level of the motor output pathway.     

Coordinate processing during the left-to-right hand transfer investigated by EEG

Information about visuomotor tasks is coded in extrinsic, object-centered and intrinsic, body-related coordinates. For the reproduction of a trained task in mirror orientation with the opposite untrained hand, acquired extrinsic coordinates must be transformed. In contrast, intrinsic coordinates have to be modified during the execution of the originally oriented task. As shown recently, processes of coordinate transformations during the right-to-left hand transfer are associated with movement preparation and occur preferentially in the left hemisphere. Here, movement-related potentials, EEG power, and EEG coherence were recorded during the repetition of a drawing task previously trained by the nondominant left hand (Learned-task) and its execution in original and mirror orientation by the right hand (Normal- and Mirror-task). To identify EEG correlates of coordinate processing during intermanual transfer rather than effects due to the use of the right versus left hand, only those EEG data were analyzed which differed between the Normal- and Mirror-tasks. Whereas the Normal-task did not differ from the Learned-task in any of these predefined EEG parameters, beta coherence increased in the Mirror-task in the period ranging from 1 to 2 s after movement onset. These increases were especially prominent between hemispheres but were also observed symmetrically in the parieto-frontal electrode pairs of both hemispheres. Behavioral data revealed that the performance in the Learned- and both transfer tasks improved after left-hand training. Results of the present study indicate that coordinate transformation during the left-to-right hand transfer occurs in the phase of movement execution and affects predominantly extrinsic coordinates. Intrinsic coordinates are presumably mainly used in their original form. The modification of extrinsic coordinates is accompanied by increased information flow between both hemispheres; thereby inter-hemispheric connections—as mediated via the corpus callosum—seem to play a central role.     

Transient disruption of M1 during response planning impairs subsequent offline consolidation

Transcranial magnetic stimulation (TMS) was used to probe the involvement of the left primary motor cortex (M1) in the consolidation of a sequencing skill. In particular we asked: (1) if M1 is involved in consolidation of planning processes prior to response execution (2) whether movement preparation and movement execution can undergo consolidation independently and (3) whether sequence consolidation can occur in a stimulus specific manner. TMS was applied to left M1 while subjects prepared left hand sequential finger responses for three different movement sequences, presented in an interleaved fashion. Subjects also trained on three control sequences, where no TMS was applied. Disruption of subsequent consolidation was observed, but only for sequences where subjects had been exposed to TMS during training. Further, reduced consolidation was only observed for movement preparation, not movement execution. We conclude that left M1 is causally involved in the consolidation of effective response planning for left hand movements prior to response execution, and mediates consolidation in a sequence specific manner. These results provide important new insights into the role of M1 in sequential memory consolidation and sequence response planning.     

Action observation supports effector-dependent learning of finger movement sequences

Practising a motor skill can result in effector-dependent learning (learning that does not transfer from the set of muscles used in training to a new set of muscles). Proceeding from neurophysiological evidence of motor activation during action observation, this study asked whether observational learning, learning through observation of skilled performance, can also be effector-dependent. Adult human participants observed a models right hand as the model responded to an eight-item sequence in a serial reaction time (SRT) task. Their sequence learning was then compared in two tests with that of controls who had observed the models right hand responding to random targets during training. All participants performed the SRT task with their right hand in the first test and with their left hand in the second. Evidence of observational learning was obtained in the right hand test but not in the left hand test. This implies that sequence learning based on observation of right hand performance did not transfer to the left hand, and therefore that observational learning can support effector-dependent learning of finger movement sequences. A second experiment used the same procedure to assess learning by a group of participants who observed a sequence of response locations only. This group did not observe the models responses. Results suggested that action observation was necessary for the effector-dependent observational learning demonstrated in Experiment 1.     

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.     

Theta EEG neurofeedback benefits early consolidation of motor sequence learning

Procedural learning is subject to consolidation processes believed to depend on the modulation of functional connections involved in representing the acquired skill. While sleep provides the most commonly studied framework for such consolidation processes, posttraining modulation of oscillatory brain activity may also impact on plasticity processes. Under the hypothesis that consolidation of motor learning is associated with theta band activity, we used EEG neurofeedback (NFB) to enable participants to selectively increase either theta or beta power in their EEG spectra following the acquisition phase of motor sequence learning. We tested performance on a motor task before and after training, right after the NFB session to assess immediate NFB effects, 1 day after NFB to assess interaction between NFB effects and overnight sleep‐dependent stabilization, and 1 week after the initial session, to assess the effects of NFB on long‐term stabilization of motor training. We also explored the extent of the influence of single‐electrode NFB on EEG recorded across the scalp. Results revealed a significantly greater improvement in performance immediately after NFB in the theta group than in the beta group. This effect continued for testing up to 1 week following training. Across participants, post‐NFB improvement correlated positively with theta/beta ratio change achieved during NFB. Additionally, NFB was found to cause widespread band‐power modulation beyond the electrode used for feedback. Thus, upregulating postlearning theta power may yield contributions to the immediate performance and subsequent consolidation of an acquired motor skill.     

Motor-learning-related changes in piano players and non-musicians revealed by functional magnetic-resonance signals

 In this study, we investigated blood-flow-related magnetic-resonance (MR) signal changes and the time course underlying short-term motor learning of the dominant right hand in ten piano players (PPs) and 23 non-musicians (NMs), using a complex finger-tapping task. The activation patterns were analyzed for selected regions of interest (ROIs) within the two examined groups and were related to the subjects’ performance. A functional learning profile, based on the regional blood-oxygenation-level-dependent (BOLD) signal changes, was assessed in both groups. All subjects achieved significant increases in tapping frequency during the training session of 35 min in the scanner. PPs, however, performed significantly better than NMs and showed increasing activation in the contralateral primary motor cortex throughout motor learning in the scanner. At the same time, involvement of secondary motor areas, such as bilateral supplementary motor area, premotor, and cerebellar areas, diminished relative to the NMs throughout the training session. Extended activation of primary and secondary motor areas in the initial training stage (7–14 min) and rapid attenuation were the main functional patterns underlying short-term learning in the NM group; attenuation was particularly marked in the primary motor cortices as compared with the PPs. When tapping of the rehearsed sequence was performed with the left hand, transfer effects of motor learning were evident in both groups. Involvement of all relevant motor components was smaller than after initial training with the right hand. Ipsilateral premotor and primary motor contributions, however, showed slight increases of activation, indicating that dominant cortices influence complex sequence learning of the non-dominant hand. In summary, the involvement of primary and secondary motor cortices in motor learning is dependent on experience. Interhemispheric transfer effects are present. Received: 11 August 1998 / Accepted: 23 November 1998     

Distinguishable brain activation networks for short- and long-term motor skill learning

The acquisition of a new motor skill is characterized first by a short-term, fast learning stage in which performance improves rapidly, and subsequently by a long-term, slower learning stage in which additional performance gains are incremental. Previous functional imaging studies have suggested that distinct brain networks mediate these two stages of learning, but direct comparisons using the same task have not been performed. Here we used a task in which subjects learn to track a continuous 8-s sequence demanding variable isometric force development between the fingers and thumb of the dominant, right hand. Learning-associated changes in brain activation were characterized using functional MRI (fMRI) during short-term learning of a novel sequence, during short-term learning after prior, brief exposure to the sequence, and over long-term (3 wk) training in the task. Short-term learning was associated with decreases in activity in the dorsolateral prefrontal, anterior cingulate, posterior parietal, primary motor, and cerebellar cortex, and with increased activation in the right cerebellar dentate nucleus, the left putamen, and left thalamus. Prefrontal, parietal, and cerebellar cortical changes were not apparent with short-term learning after prior exposure to the sequence. With long-term learning, increases in activity were found in the left primary somatosensory and motor cortex and in the right putamen. Our observations extend previous work suggesting that distinguishable networks are recruited during the different phases of motor learning. While short-term motor skill learning seems associated primarily with activation in a cortical network specific for the learned movements, long-term learning involves increased activation of a bihemispheric cortical-subcortical network in a pattern suggesting "plastic" development of new representations for both motor output and somatosensory afferent information.     

Sleep modulates word-pair learning but not motor sequence learning in healthy older adults

Sleep benefits memory across a range of tasks for young adults. However, remarkably little is known of the role of sleep on memory for healthy older adults. We used 2 tasks, 1 assaying motor skill learning and the other assaying nonmotor/declarative learning, to examine off-line changes in performance in young (20-34 years), middle-aged (35-50 years), and older (51-70 years) adults without disordered sleep. During an initial session, conducted either in the morning or evening, participants learned a motor sequence and a list of word pairs. Memory tests were given twice, 12 and 24 hours after training, allowing us to analyze off-line consolidation after a break that included sleep or normal wake. Sleep-dependent performance changes were reduced in older adults on the motor sequence learning task. In contrast, sleep-dependent performance changes were similar for all 3 age groups on the word pair learning task. Age-related changes in sleep or networks activated during encoding or during sleep may contribute to age-related declines in motor sequence consolidation. Interestingly, these changes do not affect declarative memory.     

rTMS联合运动训练对静息态脑网络影响的研究

重复经颅磁刺激(rTMS)联合运动训练可以提高肢体运动能力,在脑卒中后的运动康复中有重要的应用价值。探讨rTMS联合运动训练对静息态脑网络的影响。招募10名健康受试者,使用1 Hz rTMS刺激优势半球,结束后非利手立即执行运动训练,以提高非利手的运动能力,rTMS联合运动训练共持续14天。采集rTMS联合运动训练前后闭目静息态的脑电(EEG)信号,使用相位延迟指数(PLI)进行功能连接性分析,并以PLI值为边的权重计算依据来建立有权无向脑网络,计算网络节点的最短路径长度和节点效率,使用非参数符号秩和检验进行统计学分析。结果发现,rTMS联合运动训练使EEG低频段(theta和alpha)脑功能区间的连接显著增加、高频段(beta、gamma₁和gamma₂)显著降低,对脑功能区内的连接影响较小。特别地,采取rTMS联合运动训练,使alpha频段非优势侧中央区与优势侧额叶区(训练前0.141 4±0.102 5,训练后0.217 2±0.134 7,P<0.05)、非优势侧额叶区(训练前0.141 0±0.109 9,训练后0.205 9±0.136 1,P <0.05)的功能连接性显著增加。网络特征结果显示,节点效率在低频段增加、高频段降低,而节点最短路径长度表现出相反的结果,其中gamma₂频段在双侧中央区的节点效率(左中央区,实验前0.060 0±0.000 3,实验后0.042 9±0.001 3,P <0.05;右中央区,实验前0.060 7±0.002 3,实验后0.041 9±0.002 4,P <0.05)和最短路径长度(左中央区,实验前18.539 0±0.457 1,实验后28.585 8±1.001 4,P<0.05;右中央区,实验前18.650 8±0.438 6,实验后28.853 0±1.652 6,P <0.05)发生显著性的改变。通过该项研究,加深对rTMS联合运动训练促进运动能力神经机制的理解,为未来探究其对脑卒中、脑损伤患者脑活动的影响提供帮助。     

EEG correlates of coordinate processing during intermanual transfer

Goal-directed movements require mapping of target information to patterns of muscular activation. While visually acquired information about targets is initially encoded in extrinsic, object-centered coordinates, muscular activation patterns are encoded in intrinsic, body-related coordinates. Intermanual transfer of movements previously learned with one hand is accomplished by the recall of unmodified extrinsic coordinates if the task is performed in original orientation. Intrinsic coordinates are retrieved in case of mirror-reversed orientation. In contrast, learned extrinsic coordinates are modified during the mirror movement and intrinsic coordinates during the originally oriented task. To investigate the neural processes of recall and modification, electroencephalogram (EEG) recording was employed during the performance of a figure drawing task previously trained with the right hand in humans. The figure was reproduced with the right hand (Learned-task) and with the left hand in original (Normal-task) and mirror orientations (Mirror-task). Prior to movement onset, beta-power and alpha- and beta-coherence decreased during the Normal-task as compared with the Learned-task. Negative amplitudes over fronto-central sites during the Normal-task exceeded amplitudes manifested during the Learned-task. In comparison to the Learned-task, coherences between fronto-parietal sites increased during the Mirror-task. Results indicate that intrinsic coordinates are processed during the pre-movement period. During the Normal-task, modification of intrinsic coordinates was revealed by cerebral activation. Decreased coherences appeared to reflect suppressed inter-regional information flow associated with utilization of intrinsic coordinates. During the Mirror-task, modification of extrinsic coordinates induced activation of cortical networks.     

Effect of unimanual training on contralateral motor overflow in children and adults

Young children and adults performed a rapid unimanual finger‐lifting task. Active hand performance and ipsilateral and contralateral motor overflow were examined using a cross‐hand transfer‐of‐training paradigm. Lateral asymmetries in both the performing hands and overflow hands were investigated. An expected developmental trend was evidenced with children exhibiting more motor overflow than adults. There was also greater overflow evidenced when performing with the left hand than with the right hand in both children and adults. Children evidenced a similar asymmetry in transfer of training, that is, greater transfer of training from the left hand to the right hand than vice versa. The relationship between asymmetries in motor overflow and transfer of training is discussed in terms of cerebral specialization for movement control. Finally, training does seem to influence ipsilateral overflow, suggesting that task efficiency may play a role in the occurrence of motor overflow and that caution be exercised in the use of motor overflow as a diagnostic tool.     

Intermanual transfer of procedural learning after extended practice of probabilistic sequences

Previous studies using simple, repeating patterns have suggested that the knowledge gained in early sequence learning is not effector-specific in that it transfers to muscle groups other than those used during training. The current experiments extended these findings to transfer after extensive practice with probabilistic sequences using a task on which people fail to gain declarative knowledge of the regularity. Specifically, an alternating serial reaction time (ASRT) task was used in which predictable and unpredictable trials alternated. Participants responded for the first five sessions using their right hand, then switched to the left hand for the sixth session. Stimuli were spatial in the first experiment and nonspatial in the second. Significant near-perfect transfer of pattern knowledge was seen in both experiments, suggesting that muscle-specific information for either the fingers or the eyes cannot explain the observed learning. Electronic Publication     

Aberrant brain activation following motor skill learning in schizophrenic patients as shown by functional magnetic resonance imaging

BACKGROUND: Motor skill learning may be impaired in schizophrenia. While functional brain imaging studies have shown reduced activation during motor task performance in schizophrenic patients, brain activity changes with motor skill learning in these patients have not been studied by functional imaging. METHODS: A sequential complex motor task involving the right hand was performed by nine medicated schizophrenic patients and 10 age-matched healthy controls. Functional magnetic resonance images were obtained using a gradient echo, echoplanar imaging (EPI) pulse sequence before and after 1 week of training in performing the task. RESULTS: Bilaterally, patients showed significantly less blood oxygenation level-dependent (BOLD) signal response in the premotor area (PMA) before beginning motor training than controls. BOLD signal response increased in the left PMA of schizophrenic patients after 1 week of motor training; in contrast, the signal decreased in the left PMA of control subjects. Training effects concerning the number of finger movement sequences achieved did not differ between groups. Daily neuroleptic dose did not significantly affect changes with training in BOLD signal response in the PMA. CONCLUSIONS: These preliminary results suggest that schizophrenic patients have dysfunction of neural networks in areas including the PMA that are involved in executing a complex motor task. In terms of brain activity, motor learning may be less efficient or slower in the patients than in healthy subjects.     

Degree of handedness affects intermanual transfer of skill learning

Intermanual transfer of skill learning has often been used as a paradigm to study functional specialization and hemispheric interactions in relation to handedness. This literature has not evaluated whether degree of handedness impacts learning and intermanual transfer. Because handedness scores are related to factors that might influence intermanual transfer, such as engagement of the ipsilateral hemisphere during movement (Dassonville et al. in Proc Natl Acad Sci USA 94:14015–14018, 1997) and corpus callosum volume (Witelson in Science 229:665–668, 1985; Brain 112:799–835, 1989), we tested whether degree of handedness is correlated with transfer magnitude. We had groups of left and right handed participants perform a sensorimotor adaptation task and a sequence learning task. Following learning with either the dominant or nondominant hand, participants transferred to task performance with the other hand. We evaluated whether the magnitude of learning and intermanual transfer were influenced by either direction and/or degree of handedness. Participants exhibited faster sensorimotor adaptation with the right hand, regardless of whether they were right or left handed. In addition, less strongly left handed individuals exhibited better intermanual transfer of sensorimotor adaptation, while less strongly right handed individuals exhibited better intermanual transfer of sequence learning. The findings suggest that involvement of the ipsilateral hemisphere during learning may influence intermanual transfer magnitude.     

Improvement and generalization of arm motor performance through motor imagery practice

This study compares the improvement and generalization of arm motor performance after physical or mental training in a motor task requiring a speed-accuracy tradeoff. During the pre- and post-training sessions, 40 subjects pointed with their right arm as accurately and as fast as possible toward targets placed in the frontal plane. Arm movements were performed in two different workspaces called right and left paths. During the training sessions, which included only the right path, subjects were divided into four training groups (n = 10): (i) the physical group, subjects overtly performed the task; (ii) the mental group, subjects imagined themselves performing the task; (iii) the active control group, subjects performed eye movements through the targets, (iv) the passive control group, subjects did not receive any specific training. We recorded movement duration, peak acceleration and electromyographic signals from arm muscles. Our findings showed that after both physical and mental training on the right path (training path), hand movement duration and peak acceleration respectively decreased and increased for this path. However, motor performance improvement was greater after physical compared with mental practice. Interestingly, we also observed a partial learning generalization, namely an enhancement of motor performance for the left path (non-training path). The amount of this generalization was roughly similar for the physical and mental groups. Furthermore, while arm muscle activity progressively increased during the training period for the physical group, the activity of the same muscles for the mental group was unchanged and comparable with that of the rest condition. Control groups did not exhibit any improvement. These findings put forward the idea that mental training facilitates motor learning and allows its partial transfer to nearby workspaces. They further suggest that motor prediction, a common process during both actual and imagined movements, is a fundamental operation for both sensorimotor control and learning.     

Probing for hemispheric specialization for motor skill learning: a transcranial direct current stimulation study

Convergent findings point to a left-sided specialization for the representation of learned actions in right-handed humans, but it is unknown whether analogous hemispheric specialization exists for motor skill learning. In the present study, we explored this question by comparing the effects of anodal transcranial direct current stimulation (tDCS) over either left or right motor cortex (M1) on motor skill learning in either hand, using a tDCS montage to better isolate stimulation to one hemisphere. Results were compared with those previously found with a montage more commonly used in the field. Six groups trained for three sessions on a visually guided sequential pinch force modulation task with their right or left hand and received right M1, left M1, or sham tDCS. A linear mixed-model analysis for motor skill showed a significant main effect for stimulation group (left M1, right M1, sham) but not for hand (right, left) or their interaction. Left M1 tDCS induced significantly greater skill learning than sham when hand data were combined, a result consistent not only with the hypothesized left hemisphere specialization for motor skill learning but also with possible increased left M1 responsiveness to tDCS. The unihemispheric montage effect size was one-half that of the more common montage, and subsequent power analysis indicated that 75 subjects per group would be needed to detect differences seen with only 12 subjects with the customary bihemispheric montage.     

Changes in motor cortex excitability following training of a novel goal-directed motor task

Training of skilled movements leads to typical changes in motor evoked potentials (MEPs). To explore how such changes are related to motor performance and hand preference, a goal-directed movement task was implemented on a haptic interface. Right and left hands of right-handed subjects were trained in two sessions separated by a pause of 10 min. Transcranial magnetic stimulation (TMS) was applied contralaterally to the trained hand before and after each session. Effects of right hand training: after session #1 MEP-facilitation was +60%, intracortical inhibition (ICI) was reduced and task improvement was +37%. Following session #2 all variables remained unchanged. Left hand training: after session #1 MEP-facilitation was +59%, ICI remained unchanged and task improvement was +30%. Following session #2 all variables remained unchanged. It is concluded that mainly the early phase of skill acquisition induces neuroplastic changes. The asymmetry in ICI obviously reflects functional side differences in hand motor control.