Paradoxical Long-term Memory Augmentation following Temporal Pairing between "Limited" and "Extensive" Motor Sequence Training Experiences.

Consecutive training on two movement sequences often leads to retroactive interference-obstructing memory for the initially trained sequence but not for the second. However, in the context of hippocampal-system dependent memories, a poor learning experience, memory for which would soon decay, can be enhanced if temporally paired with a "strong," memory triggering experience. The synaptic tagging and capture hypothesis explains this paradoxical enhancement by suggesting that only strong experiences generate cellular resources necessary for synaptic remodeling. However, synapses engaged in a "weak" learning experience can capture and utilize plasticity-related resources generated for a subsequent strong learning experience. Here, we tested whether such "paradoxical" outcome would result in the context of motor (procedural) memory, if two movement sequences are unequally trained, consecutively. We show, in young adults (n = 100), that limited practice on a novel sequence of finger-to-thumb opposition movements led to different long-term outcomes, depending on whether and when (5 min, 5 hr) it was followed by extensive training on a different sequence. Five-minute pairing, only, resulted in overnight gains for the limited-trained sequence that were well-retained a week later; the overnight gains for the extensively trained sequence were compromised. Thus, consecutive training on different motor tasks can result in mnemonic interactions other than interference. We propose that the newly discovered mnemonic interaction provides the first-tier behavioral evidence in support of the possible applicability of notions stemming from the synaptic tagging and capture hypothesis in relation to human motor memory generation, specifically in relation to the practice-dependent consolidation of novel explicitly instructed movement sequences.

Different delayed consequences of attaining a plateau phase in practicing a simple (finger-tapping sequence learning) and a complex (Tower of Hanoi puzzle) task.

In practicing a new task, the initial performance gains, across consecutive trials, decrease; in the following phase, performance tends to plateau. However, after a long delay additional performance improvements may emerge (delayed/ "offline" gains). It has been suggested that the attainment of the plateau phase is a necessary condition for the triggering of skill consolidation processes that lead to the expression of delayed gains. Here we compared the effect of a long-delay (24-48 h) interval following each of the two within-session phases, on performance in a simple motor task, the finger-tapping sequence learning (FTSL), and in a conceptually complex task, the Tower of Hanoi puzzle (TOHP). In Experiment 1 we determined the amount of practice leading to the plateau phase within a single practice session (long practice), in each task. Experiment 2 consisted of three consecutive sessions with long-delay intervals in between; in the first session, participants underwent a short practice without attaining the plateau phase, but in the next two sessions, participants received long practice, attaining the plateau phase. In the FTSL, short practice resulted in no delayed gains after the long delay, but after 24-48 h following long practice, task performance was further improved. In contrast, no delayed gains evolved in the TOHP during the 24- to 48-h delay following long practice. We propose that the attainment of a plateau phase can indicate either the attainment of a comprehensive task solution routine (achievable for simple tasks) or a preservation of work-in-progress task solution routine (complex tasks); performance after a long post-practice interval can differentiate these two states.

[DISSOCIATION BETWEEN DECLERATIVE AND PROCEDURAL MEMORY IN PATIENTS WITH TRAUMATIC BRAIN INJURY].

INTRODUCTION: Converging evidence from studies of patients suffering focal brain lesions and results from animal models led to the notion of two functionally and structurally distinct memory systems, declarative-explicit-episodic and procedural-implicit-skill. AIMS: Assessment of skill acquisition and procedural memory in patients after blunt traumatic brain injury (TBI) who suffer from deficit of explicit (episodic) memory in comparison to patients without such a deficit. METHODS: Comparison of skill acquisition in the Finger Opposition Sequence task in two patients after TBI presenting with episodic-explicit memory deficit to eight patients without such a deficit. RESULTS: Both subjects demonstrated severe declarative-episodic memory deficits as demonstrated in the Rivermead Behavioural Memory Test (RBMT) but showed robust learning and retention of skill in practicing a finger movement sequence, improving performance speed with no speed-accuracy trade-off. The practice related gains in performance and their retention in a one-month follow-up test were as robust as in patients without explicit memory deficit. CONCLUSIONS: The results coincide with previous case reports demonstrating a dissociation between procedural-implicit and declarative-explicit memory systems. The evaluation of the two memory systems may contribute to patient rehabilitation as a residual functioning of one system can be used to compensate for deficit of the other, in order to improve daily functioning.

Practice schedule and testing per se affect children's transfer abilities in a grapho-motor task.

Children's ability to transfer the gains of a motor experience, such as learning to write a letter, to novel conditions, such as cursive writing of the same letter, are affected by the way in which the learning experience is parsed. Parsing may have limitations because a short session may hamper the engagement of procedural memory consolidation processes. Here, we compared the effects of two practice schedules with the total amount of practice identical training provided in a single-session practice versus multi-session practice, wherein each session on its own was insufficient for generating long-term gains. A total of 40 7- and 8-year-old children practiced the production of a novel letter form by connecting dots, namely, the Invented Letter Task (ILT). Multiple ILT-related transfer tasks were assessed at 24 h post-training and again at 4-5 weeks post-training. Although by the end of training the single-session practice group outperformed the multi-session practice group in speed and accuracy, at 24 h post-training both groups showed comparable gains. However, after multi-session practice, children were as fast or faster and more accurate in the transfer tasks. By 4-5 weeks post-training, the multi-session practice group showed larger gains in the trained condition, a speed advantage in the transfer tasks, and a significant improvement on the transfer tasks. The results suggest that parsing training over several brief sessions may lead to long-term gains in children's grapho-motor skills. Moreover, multi-session practice protocols may contribute to the potential for transfer and to more effective learning from experiences such as transfer tasks.

Better later: evening practice is advantageous for motor skill consolidation in the elderly.

How does the time of day of a practice session affect learning of a new motor sequence in the elderly? Participants practiced a given finger tapping sequence either during morning or evening hours. All participants robustly improved performance speed within the session concurrent with a reorganization of the tapping pattern of the sequence. However, evening-trained participants showed additional gains overnight and at 1 wk posttraining; moreover, evening training led to a further reorganization of the tapping pattern offline. A learning experience preceding nocturnal sleep can lead to a task-specific movement routine as an expression of novel "how to" knowledge in the elderly.

Recitation as a structured intervention to enhance the long-term verbatim retention and gist recall of complex texts in kindergarteners.

Recitation is an effective way for children to become familiar with basic blocks of knowledge. It is not clear, however, whether repeated structured exposure to complex texts via listening or active reciting benefits the ability of kindergarteners to retain verbal material in long-term memory verbatim and as content. Here, we tested the effectiveness of teaching longer texts to kindergarteners by repeated exposure in terms of long-term retention (6 months). A set of 28 rhyming sentences (224 words) were introduced, 3 in each session, and the increasingly longer text was practiced by either voiced recitation or listening. The rhymes were in a literary language, and word meaning in each new rhyme was elaborated when first introduced. Both groups (recitation and listening) showed good long-term retention, but the recitation group outperformed the listening group when assessed at 24 h, 1 month, and 6 months postintervention in terms of the recall rate, error rate, number of prompts required, and sequence fidelity. In the later assessments, the reciting group was the more fluent group in producing the rhymes. Moreover, at 6 months postintervention, the gist (content) of the rhymes and the meaning of vocabulary items from the texts were robustly retained, with an advantage for the recitation group. Thus, practice in affording multiple repetitions, specifically active recitation, resulted in fluent, effortless, and accurate recall of statements and their content. We propose that these results support the notion that repetition-based practice may promote the mastery of complex verbal material by enabling better engagement of procedural memory, that is, by promoting "proceduralization" processes.

Practice Makes Transfer Imperfect: Evidence From Auditory Learning.

BACKGROUND: Evidence from motor and visual studies suggests that the ability to generalize learning gains to untrained conditions decreases as the training progresses. This decrease in generalization was suggested to reflect a shift from higher to lower levels of neuronal representations of the task following prolonged training. In the auditory modality, however, the few studies that tested the influence of prolonging training on generalization ability showed no decrease and sometimes even an increase in generalization. OBJECTIVE: To test the impact of extending training in a basic psychoacoustic task on the ability to generalize the gains attained in training to untrained conditions. DESIGN: Eighty-two young adults participated in two experiments that differed in the specific training regimen. In both experiments, training was conducted using a difference limen for frequency (DLF) task with an adaptive forced-choice procedure, for either a single- or nine-session training. Following training, generalization to the untrained ear and to an untrained frequency was assessed. RESULTS: (a) Training induced significant learning (i.e., smaller DLF thresholds) following a single session of training, and more so following nine training sessions; (b) results from the combined data from both experiments showed that the ability to generalize the learning gains to the untrained ear and frequency was limited after the extended DLF training; (c) larger improvements under the trained condition resulted in smaller generalization to the untrained conditions. CONCLUSIONS: The findings of increased specificity with training in the auditory modality support the notion that gradual changes, both quantitative and qualitative, occur in the neural representations of an auditory task during its acquisition. These findings suggest common underlying mechanisms in basic skill learning across different modalities.

Cerebral Activation During Initial Motor Learning Forecasts Subsequent Sleep-Facilitated Memory Consolidation in Older Adults.

Older adults exhibit deficits in motor memory consolidation; however, little is known about the cerebral correlates of this impairment. We thus employed fMRI to investigate the neural substrates underlying motor sequence memory consolidation, and the modulatory influence of post-learning sleep, in healthy older adults. Participants were trained on a motor sequence and retested following an 8-h interval including wake or diurnal sleep as well as a 22-h interval including a night of sleep. Results demonstrated that a post-learning nap improved offline consolidation across same- and next-day retests. This enhanced consolidation was reflected by increased activity in the putamen and the medial temporal lobe, including the hippocampus, regions that have previously been implicated in sleep-dependent neural plasticity in young adults. Moreover, for the first time in older adults, the neural substrates subserving initial motor learning, including the putamen, cerebellum, and parietal cortex, were shown to forecast subsequent consolidation depending on whether a post-learning nap was afforded. Specifically, sufficient activation in a motor-related network appears to be necessary to trigger sleep-facilitated consolidation in older adults. Our findings not only demonstrate that post-learning sleep can enhance motor memory consolidation in older adults, but also provide the system-level neural correlates of this beneficial effect.

Background matters: Minor vibratory stimulation during motor skill acquisition selectively reduces off-line memory consolidation.

Although a ubiquitous situation, it is not clear how effective is a learning experience when task-irrelevant, sensory noise occurs in the background. Here, young adults were trained on the finger opposition sequence task, in a well-established training and testing protocol affording measures for online as well as off-line learning. During the training session, one group experienced a minor background vibratory stimulation to the trunk by the means of vibrating cushion, while the second group experienced recorded sound vibrations. A control group was trained with no extra sensory stimulation. Sensory stimulation during training had no effect on the online within-session gains, but dampened the expression of the off-line, consolidation phase, gains in the two sensory stimulation groups. These results suggest that background sensory stimulation can selectively modify off-line, procedural memory consolidation processes, despite well-preserved on-line learning. Classical studies have shown that neural plasticity in sensory systems is modulated by motor input. The current results extend this notion and suggest that some types of task-irrelevant sensory stimulation, concurrent with motor training, may constitute a 'gating' factor - modulating the triggering of long-term procedural memory consolidation processes. Thus, vibratory stimulation may be considered as a behavioral counterpart of pharmacological interventions that do not interfere with short term neural plasticity but block long-term plasticity.

Innateness of magnitude perception? Skill can be acquired and mastered at all ages.

We agree with Leibovich et al.'s argument that the number sense theory should be re-evaluated. However, we argue that highly efficient skills (i.e., fluent and highly accurate, "automatic," performance) can be acquired and mastered at all ages. Hence, evidence for primacy or fluency in perceiving continuous magnitudes is insufficient for supporting strong conclusions about the innateness of this aptitude.

Not quite there: skill consolidation in training by doing or observing.

We tested the notion that action observation engages learning processes and mnemonic representations overlapping with those engaged in actual performance. An identical number of training instances, actual performance, or observation, was afforded on a finger opposition sequence task. Both training modes resulted in immediate gains in performance, as well as in robust delayed, "off-line," gains, indicating post-training consolidation. However, the expression of delayed gains could be blocked by the subsequent performance of a second sequence (post-training interference), but not by its observation. The mnemonic representations of "how-to" knowledge acquired from actual or observed movement may not overlap.

Learning from the other limb's experience: sharing the 'trained' M1 representation of the motor sequence knowledge.

KEY POINTS: Participants were scanned during the untrained-hand performance of a motor sequence, intensively trained a day earlier, and also a similarly constructed but novel, untrained sequence. The superior performance levels for the trained, compared to the untrained sequence, were associated with a greater magnitude of activity within the primary motor cortex (M1), bilaterally, for the trained sequence. The differential responses in the 'trained' M1, ipsilateral to the untrained hand, were positively correlated with experience-related differences in the functional connectivity between the 'trained' M1 and (1) its homologue and (2) the dorsal premotor cortex (PMd) within the contralateral hemisphere. No significant correlation was evident between experience-related differences in M1 - M1 and M1 - PMd connectivity measures. These results suggest that the transfer of sequence-specific information between the two primary motor cortices is predominantly mediated by excitatory mechanisms driven by the 'trained' M1 via two independent neural pathways. Following unimanual training on a novel sequence of movements, sequence-specific performance may improve overnight not only in the trained hand, but also in the hand afforded no actual physical experience. It is not clear, however, how transfer to the untrained hand is achieved. In the present study, we examined whether and how interaction between the two primary motor cortices contributes to the performance of a sequence of movements, extensively trained the day before, by the untrained hand. Accordingly, we studied participants during the untrained-hand performance of a finger-to-thumb opposition sequence (FOS), intensively trained a day earlier (T-FOS), and a similarly constructed, but novel, untrained FOS (U-FOS). Changes in neural signals driven by task performance were assessed using functional magnetic resonance imaging. To minimize potential differences as a result of the rate of sequence execution per se, participants performed both sequences at an identical paced rate. The analyses showed that the superior fluency in executing the T-FOS compared to the U-FOS was associated with higher activity within the primary motor cortex (M1), bilaterally, for the T-FOS. The differential responses in the 'trained' M1 were positively correlated with experience-related differences in the functional connectivity between the 'trained' M1 and (1) its left homologue and (2) the left dorsal premotor cortex. However, no significant correlation was evident between the changes in connectivity in these two routes. These results suggest that the transfer of sequence-specific information between the two primary motor cortices is predominantly mediated by excitatory mechanisms driven by the 'trained' M1 via at least two independent neural pathways.

Effective learning and retention of braille letter tactile discrimination skills in children with developmental dyslexia.

Children with developmental dyslexia (DD) may differ from typical readers in aspects other than reading. The notion of a general deficit in the ability to acquire and retain procedural ('how to') knowledge as long-term procedural memory has been proposed. Here, we compared the ability of elementary school children, with and without reading difficulties (DD, typical readers), to improve their tactile discrimination with practice and tested the children's ability to retain the gains. Forty 10-11-year-olds practiced the tactile discrimination of four braille letters, presented as pairs, while blindfolded. In a trial, participants were asked to report whether the target stimuli were identical or different from each other. The structured training session consisted of six blocks of 16 trials each. Performance was re-tested at 24 hours and two weeks post-training. Both groups improved in speed and in accuracy. In session 1, children with DD started as significantly less accurate and were slower than the typical readers but showed rapid learning and successfully closed the gap. Only two children with DD failed to benefit from training and were not included in subsequent data analyses. At 24 hours post-training both groups showed effective retention of the gains in speed and accuracy. Importantly, children with DD were able to retain the gains in speed and accuracy, over a two-week interval as effectively as typical readers. Thus, children with DD were as effective in the acquisition and retention of tactile discrimination of braille letters as typical readers of the same age. The results do not support the notion of a general procedural learning disability in DD.

Patterns of modulation in the activity and connectivity of motor cortex during the repeated generation of movement sequences.

It is not clear how the engagement of motor mnemonic processes is expressed in online brain activity. We scanned participants, using fMRI, during the paced performance of a finger-to-thumb opposition sequence (FOS), intensively trained a day earlier (T-FOS), and a similarly constructed, but novel, untrained FOS (U-FOS). Both movement sequences were performed in pairs of blocks separated by a brief rest interval (30 sec). We have recently shown that in the primary motor cortex (M1) motor memory was not expressed in the average signal intensity but rather in the across-block signal modulations, that is, when comparing the first to the second performance block across the brief rest interval. Here, using an M1 seed, we show that for the T-FOS, the M1-striatum functional connectivity decreased across blocks; however, for the U-FOS, connectivity within the M1 and between M1 and striatum increased. In addition, in M1, the pattern of within-block signal change, but not signal variability per se, reliably differentiated the two sequences. Only for the U-FOS and only within the first blocks in each pair, the signal significantly decreased. No such modulation was found within the second corresponding blocks following the brief rest interval in either FOS. We propose that a network including M1 and striatum underlies online motor working memory. This network may promote a transient integrated representation of a new movement sequence and readily retrieves a previously established movement sequence representation. Averaging over single events or blocks may not capture the dynamics of motor representations that occur over multiple timescales.

Not all declarative memories are created equal: Fast Mapping as a direct route to cortical declarative representations.

Memory formation for newly acquired associations typically depends on hippocampal-neocortical interactions. Through the process of system-consolidation, the mnemonic binding role of the hippocampus is subsequently replaced by cortical hubs, such as the ventromedial prefrontal cortex (vmPFC) or the anterior temporal lobe (ATL). Here, using BOLD-fMRI, we compared retrieval of semantic associations acquired through Fast Mapping (FM), an incidental, exclusion-based learning procedure, to retrieval of similar associations that were intentionally acquired through Explicit Encoding (EE). Despite an identical retrieval task, the encoding histories of the retrieved semantic associations (FM vs. EE) induced distinct neural substrates and disparate related neural dynamics in time. Retrieval of associations acquired through EE engaged the expected hippocampal and vmPFC related networks. Furthermore, retrieval intentionally encoded associations gave rise to a typical overnight increase in engagement of the vmPFC and increased vmPFC-hippocampal-neocortical functional connectivity. On the other hand, retrieval of associations acquired through FM immediately engaged an ATL related network that typically supports well-established semantic knowledge, a network that did not engage the hippocampus and the vmPFC. Moreover, FM learning was associated with minimal overnight changes in the BOLD responses and in the functional connectivity. Our findings indicate that FM may induce a direct, ATL-mediated acquisition and retention of novel arbitrary associations, bypassing the initial hippocampal-cortical representation phase. A direct, ATL-mediated vocabulary acquisition through FM could support the learning and retention of new associations in young children with presumably an immature hippocampal system, and possibly even in amnesic adults with hippocampal lesions.

Maintaining vs. enhancing motor sequence memories: respective roles of striatal and hippocampal systems.

It is now accepted that hippocampal- and striatal-dependent memory systems do not act independently, but rather interact during both memory acquisition and consolidation. However, the respective functional roles of the hippocampus and the striatum in these processes remain unknown. Here, functional magnetic resonance imaging (fMRI) was used in a daytime sleep/wake protocol to investigate this knowledge gap. Using a protocol developed earlier in our lab (Albouy et al., 2013a), the manipulation of an explicit sequential finger-tapping task, allowed us to isolate allocentric (spatial) and egocentric (motor) representations of the sequence, which were supported by distinct hippocampo- and striato-cortical networks, respectively. Importantly, a sleep-dependent performance enhancement emerged for the hippocampal-dependent memory trace, whereas performance was maintained for the striatal-dependent memory trace, irrespective of the sleep condition. Regression analyses indicated that the interaction between these two systems influenced subsequent performance improvements. While striatal activity was negatively correlated with performance enhancement after both sleep and wakefulness in the allocentric representation, hippocampal activity was positively related to performance improvement for the egocentric representation, but only if sleep was allowed after training. Our results provide the first direct evidence of a functional dissociation in consolidation processes whereby memory stabilization seems supported by the striatum in a time-dependent manner whereas memory enhancement seems linked to hippocampal activity and sleep-dependent processes.

Limits on movement integration in children: The concatenation of trained subsequences into composite sequences as a specific experience-triggered skill.

Complex movement sequences may be easier to acquire in sub-segments. Nevertheless, the neuro-behavioral constraints on assembling short multi-element movement segments, acquired piecemeal and serially, into larger, composite units of action, are not clear. Here we examined the ability of children to combine movement subsequences into longer, composite, sequences. Eleven-year-olds were trained in the performance of two, 3-elements, finger-to-thumb opposition movement sequences and were tested, overnight, in the performance of composite, 6-elements, sequences. Two experiments were compared, differing only in whether or not a brief test for integration into a composite sequence was afforded immediately post-training. This composite sequence (Full) was a direct forward integration of the two subsequences, maintaining the order in which the two subsequences were trained. In both experiments, overnight performance of movement elements within the composite sequences was better than naive performance, but slower and less accurate compared to the performance of the identical movement elements in the context of the trained subsequences. Integration was as effective in the Full sequence as when the order between subsequences was switched (Reversed). However, the early test for subsequence integration was critical in inducing clear between-session ('offline') gains, as expressed in overnight performance, in both the Full and Reversed sequences. Without this brief experience in integration, no overnight gains were expressed in any of the 6-elements sequences. Moreover, the immediate post-training test resulted in a relative advantage of the Full and Reversed sequences over a 6-element sequence in which the order of the elements was mirror-reversed within each subsequence. Thus, training on subsequences may not spontaneously lead to an advantage in the performance of composite sequences, in children. However, an early brief experience with a composite sequence can suffice to trigger the establishment and consolidation of an integration routine. This routine is specific for the order of movement within the trained subsequences, but not for the order in which the subsequences were practiced.

Asymmetric interaural generalization of learning gains in a speech-in-noise identification task.

The pattern of generalization of learning gains to untrained conditions in adult human perceptual skill learning has been used as an effective behavioral probe for studying the functional organization of the learning system. Learning gains were previously reported to generalize symmetrically between the ears for tonal stimuli. However, given the open question concerning the specialization of the hemispheres in the processing of speech sounds, it is not clear whether symmetrical interaural generalization will follow training on such stimuli. Here the effect of monaural single-session training on the identification of consonant-vowel stimuli in noise was examined. Participants showed similar robust gains in performance at 24 h post-training in both trained ears. There was, however, an asymmetrical generalization of the learning gains from the trained to the untrained ear, with more transfer from the right-trained to the left-untrained ear than vice versa. Training and transfer gains were retained for both ears over an interval of several months, although for the untrained ear a brief exposure was necessary to relearn the task. These results provide first-time evidence for an asymmetry in interaural generalization for speech sounds following training and provide further support to the lateralization of speech sounds along the auditory system.

Done that: short-term repetition related modulations of motor cortex activity as a stable signature for overnight motor memory consolidation.

An almost universally accepted tacit expectation is that learning and memory consolidation processes must be reflected in the average brain activity in brain areas relevant to task performance. Motor cortex (M1) plasticity has been implicated in motor skill acquisition and its consolidation. Nevertheless, no consistent pattern of changes in the average signal, related to motor learning or motor memory consolidation following a single session of training, has emerged from imaging studies. Here we show that the pattern and magnitude of short-term brain activity modulations in response to task repetition, in M1, may provide a robust signature for effective motor memory consolidation processes. We studied participants during the paced performance of a finger-to-thumb opposition sequence (FOS), intensively trained a day earlier, and a similarly constructed untrained FOS. In addition to within-session "on-line" gains, most participants expressed delayed, consolidation-phase gains in the performance of the trained FOS. The execution of the trained FOS induced repetition enhancements in the contralateral M1 and bilaterally in the medial-temporal lobes, offsetting novelty-related repetition suppression effects. Moreover, the M1 modulations were positively correlated with the magnitude of each participant's overnight delayed gains but not with absolute performance levels. Our results suggest that short-term enhancements of brain signals upon task repetition reflect the effectiveness of overnight motor memory consolidation. We propose that procedural memory consolidation processes may affect the excitation-inhibition balance within cortical representations of the trained movements; this new balance is better reflected in repetition effects than in the average level of evoked neural activity.

Off-line consolidation of motor sequence learning results in greater integration within a cortico-striatal functional network.

The consolidation of motor sequence learning is known to depend on sleep. Work in our laboratory and others have shown that the striatum is associated with this off-line consolidation process. In this study, we aimed to quantify the sleep-dependent dynamic changes occurring at the network level using a measure of functional integration. We directly compared changes in connectivity before and after sleep or the simple passage of daytime. As predicted, the results revealed greater integration within the cortico-striatal network after sleep, but not an equivalent daytime period. Importantly, a similar pattern of results was also observed using a data-driven approach; the increase in integration being specific to a cortico-striatal network, but not to other known functional networks. These findings reveal, for the first time, a new signature of motor sequence consolidation: a greater between-regions interaction within the cortico-striatal system.