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Albouy, G.

Publications and source records attributed to Albouy, G..

At least 19 recordsLinked to original sources

Sleep Spindle-Locked Targeted Memory Reactivation Enhances Declarative Memory Consolidation

Study ObjectivesSleep spindles are implicated in memory consolidation. Yet direct evidence linking spindle dynamics to declarative memory outcomes remains limited. We thus tested whether targeted memory reactivation (TMR) time-locked to sleep spindles enhances declarative memory, and whether the temporal organization of stimulated spindles-trains versus isolated events-is selectively associated with distinct memory outcomes. MethodsTwenty-eight healthy young adults learned image locations from two categories (animals, clothing) in a grid, each paired with a distinct auditory cue. During overnight NREM sleep, one cue was replayed time-locked to spindles detected in real-time using a closed-loop system (TMR condition); the other served as the non-reactivated control (No-TMR condition). Category-cue assignment was counterbalanced. Post-sleep recall, recognition accuracy, and movement time were assessed. ResultsRecall accuracy was significantly higher in the TMR than the No-TMR condition (93.96% vs. 90.61%, p = .024), whereas recognition accuracy (p = .139) and movement time (p = .651) did not differ. Stimulation intensity within spindle trains correlated with the TMR effect on recall (Spearman {rho} = .531, p = .004), whereas the proportion of isolated spindle stimulations correlated with the TMR effect on recognition ({rho} = .563, p = .002). Cross-associations were not significant. ConclusionsSpindle-locked TMR enhances recall-based declarative memory retention. The selective association between spindle temporal clustering and memory outcomes suggests that train-embedded and isolated spindles support different aspects of memory consolidation, highlighting spindle temporal context as a functionally relevant dimension of sleep-dependent memory processing.

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Children exhibit greater persistence of motor learning-related patterns of hippocampal activity into post-task wake epochs

Previous research has demonstrated that children exhibit superior - as compared to adults - consolidation of newly acquired motor sequences across post-learning periods of wakefulness. Given that consolidation is thought to be supported by the reactivation of learning-related patterns of brain activity during the rest periods following active task practice, we hypothesized that the childhood advantage in offline consolidation may be linked to greater reactivation during post-learning wakefulness. Twenty-two children (7-11 years) and 23 adults (18-30 years) completed two sessions of a motor sequence learning task, separated by a 5-hour wake interval. Multivoxel analyses of task-related and resting-state functional magnetic resonance imaging data were employed to assess the persistence of learning-related patterns of neural activity into post-task rest epochs, reflective of reactivation processes. Behavioral results demonstrated the previously reported childhood advantage in offline consolidation over a post-learning wake interval. Imaging results revealed that children exhibited greater persistence of task-related hippocampal - but not putaminal - activity into post-learning rest as compared to adults. These findings suggest that the childhood advantage in awake motor memory consolidation may be supported, at least partially, by enhanced reactivation of task-dependent hippocampal activity patterns during offline epochs.

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No evidence for an effect of M1 cTBS on schema-mediated motor sequence learning

The availability of a pre-existing cognitive-motor schema accelerates the learning of novel motor information. The encoding of a novel schema-compatible, compared to-incompatible, motor sequence was recently shown to be supported by the left primary motor cortex (M1). However, causal evidence for the role of M1 in schema-mediated motor learning is currently lacking. In the current study, we aimed to address this knowledge gap by transiently disrupting M1 using inhibitory continuous theta burst stimulation (cTBS). Forty-eight young healthy participants learned a bimanual motor sequence task (cognitive-motor schema). Twenty-four hours later, they learned a novel sequence whose ordinal schematic structure was compatible with that learned on the previous day. To provide causal evidence for a role of M1 on such schema-mediated motor learning, we applied either cTBS or sham stimulation to the left M1 immediately prior to encoding the schema-compatible novel sequence. Electromyography results showed no evidence for an effect of left M1 cTBS on corticospinal excitability as measured with motor-evoked potentials. Similarly, behavioral results indicated no significant effect of cTBS on subsequent schema-mediated motor sequence learning. Altogether, the present data do not provide evidence for a causal role of the left M1 in schema-mediated motor sequence learning.

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The order, but not the structure, of cross-domain learning influences memory consolidation

Everyday activities often require learning sequences that necessitate the involvement of both the declarative and the procedural memory domains. Previous research has shown that a learning structure that is common across tasks from different domains can improve learning and resistance to interference. However, it remains unknown whether such shared learning structure can enhance longer-term memory retention. To address this question, forty-eight healthy adults participated in a pre-registered study in which they learned both an object sequence task (declarative learning) and a motor sequence task (procedural learning) in two separate sessions separated by 4h. Participants were assigned to either an associated group, where the two tasks shared a common learning structure - that consisted of a specific mapping between finger movements and object categories across learning sessions - or an unassociated group with no such cross-domain shared structure. Memory retention was assessed with a 24h retest session on both tasks. Contrary to our predictions, a shared higher-order structure between tasks from different domains did not enhance memory retention. Exploratory follow-up analyses revealed that the order the tasks were learned (i.e., object or motor first), rather than their structural overlap, influenced performance. Specifically, learning the motor task before the object task impaired the consolidation of the object task irrespective of whether the tasks shared a common learning structure or not. This effect was unidirectional as learning the object task before the motor task had no effect on the consolidation of the motor task. Altogether, the current findings suggest that the order of cross-domain learning experiences rather than their structure influences memory consolidation.

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Sleep after Motor Sequence Learning Enhances Post-Movement Parietal Beta Synchronization

The neural substrates supporting the beneficial effect of sleep on motor memory consolidation are well described. However, less is known about the brain oscillatory dynamics underlying these processes. We characterized the oscillatory dynamics associated with motor sequence learning and their modulation by post-learning sleep using magnetoencephalography (MEG) in young healthy adults. After learning a motor sequence task while their brain activity was recorded with MEG, participants were distributed in two groups according to whether they slept or were totally sleep deprived during the first post-training night. Consolidation was assessed with a retest in the MEG three days after training. Behaviorally, performance improved over the consolidation interval irrespective of whether sleep was afforded during the first night. MEG results showed that initial motor sequence learning was characterized by a progressive decrease in beta Event Related Desynchronization (ERD, 18-25Hz) over bilateral motor areas. Interestingly, while these practice-related modulations of beta ERD were not influenced by the sleep status, post-learned-movement beta Event Related Synchronization (ERS) over bilateral parietal areas increased over the consolidation interval in the sleep, compared to the sleep deprived, group. These results extend current models of motor memory consolidation by identifying ERS as an oscillatory marker of sleep-dependent consolidation.

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Neural correlates of motor sequence learning and enhanced offline consolidation in 7- to 11-year-old children

IntroMany daily activities involve series of interrelated movements and thus the capacity to learn new motor sequences is vital for everyday functioning. Although learning new skills is especially prominent throughout childhood, remarkably few studies have examined the neural underpinnings of motor sequence learning (MSL) and memory consolidation in children. MethodsTwenty-two children (7-11 years) and 23 adults (18-30 years) underwent functional magnetic resonance imaging while completing two sessions of a MSL task, separated by a 5-hour offline period of wakefulness. ResultsAnalyses of the behavioral data revealed comparable initial learning in children and adults. However, and consistent with previous research, children exhibited superior motor memory consolidation over the 5-hour offline epoch. Neuroimaging analyses revealed that children exhibited smaller modulations in brain activity between task and rest epochs in a widespread network, including the sensorimotor cortex, supplementary motor area, cerebellum, putamen and regions associated with the default mode network. Similar levels of activity during task and rest epochs in the hippocampus, dorsolateral prefrontal cortex and somatosensory cortex were associated with better motor memory consolidation in children. ConclusionResults potentially suggest that the continued engagement of the developing brain during interleaved rest contributes to the childhood advantage in motor memory consolidation.

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Motor cortical areas facilitate schema-mediated integration of new motor information into memory

New information is rapidly learned when it is compatible with pre-existing knowledge, i.e. with a previously acquired schematic representation of the learned information. The influence of pre-established schema on learning has been extensively studied in the declarative memory domain, where it was shown that schema-compatible information could be rapidly assimilated into neocortical storage, bypassing the slow hippocampo-neocortical memory transfer process. Schema-mediated learning was recently examined in the motor memory domain; however, its neural substrates remain unknown. The goal of this study was to address this knowledge gap using both univariate and multivariate analyses of functional Magnetic Resonance Imaging (fMRI) data acquired in 60 young healthy participants during the practice of a motor sequence that was either compatible or incompatible with a previously acquired cognitive-motor schema. Consistent with previous literature, our behavioural results suggest that performance of sequential movements was enhanced when practice occurred in a context that was compatible with the previously acquired schema. Brain imaging results show that practice in a schema-compatible context specifically recruited the left primary motor cortex and resulted in a decrease in connectivity between the bilateral motor cortex and a set of task-relevant brain regions including the hippocampus, striatum, and cerebellum. Temporally fine-grained MRI analyses revealed that multivoxel activation patterns in the primary motor and the premotor cortices were modulated by schema-compatibility, with greater pattern similarity detected for sequence elements corresponding to and surrounding novel sequential movements under schema-compatible compared with -incompatible conditions. Altogether, these results suggest that motor cortical regions facilitate schema-mediated integration of novel movements into memory.

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Impaired online and enhanced offline motor sequence learning in individuals with Parkinson's disease

Whereas memory consolidation research has traditionally focused on longer temporal windows (i.e., hours to days) following an initial learning episode, recent research has also examined the functional significance of the shorter rest epochs commonly interspersed with blocks of task practice (i.e., "micro-offline" intervals on the timescale of seconds to minutes). In the motor sequence learning domain, evidence from young, healthy individuals suggests that micro-offline epochs afford a rapid consolidation process that is supported by the hippocampus. Consistent with these findings, amnesic patients with hippocampal damage were recently found to exhibit degraded micro-offline performance improvements. Interestingly, these offline losses were compensated for by larger performance gains during online practice. Given the known role of the striatum in online motor sequence learning, we hypothesized that individuals with dysfunction of the striatal system would exhibit impaired online, yet enhanced micro-offline, learning (i.e., a pattern of results opposite to those observed in patients with hippocampal lesions). We tested this hypothesis using Parkinsons disease (PD) as a model of striatal dysfunction. Forty-two drug-naive individuals (men and women) with a clinical diagnosis of unilateral PD and 30 healthy control subjects completed a motor sequence learning paradigm. Individuals with PD exhibited deficits during online task practice that were paralleled by greater improvements over micro-offline intervals. This pattern of results could not be explained by disease-related deficits in movement execution. These data suggest that striatal dysfunction disrupts online learning, yet total learning remains unchanged because of greater micro-offline performance improvements that potentially reflect hippocampal-mediated compensatory processes. Significance StatementThe short rest intervals commonly interspersed between periods of active task engagement have traditionally been employed to minimize the build-up of fatigue. There is recent evidence, however, suggesting that these rest epochs may play an active role in motor learning and memory processes and the hippocampus appears to be a critical brain region supporting this rapid "offline" learning. Here, we show that individuals with Parkinsons disease, a movement disorder characterized by dysfunction in the basal ganglia including the striatum, exhibit deficits during active task practice but greater learning over the interspersed offline intervals. Results potentially suggest that the relatively intact hippocampus may help compensate for motor sequence learning deficits linked to a disrupted striatal system in Parkinsons disease.

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The capacity of the medial temporal lobe to represent memory items in their ordinal position in a sequence is domain-general

Memory systems in humans are less segregated than initially thought as learning tasks from different memory domains (e.g., declarative vs. procedural) can recruit similar brain areas. However, it remains unclear whether the functional role of these overlapping brain regions - and the hippocampus in particular - is domain-general. Here, we test the hypothesis that the hippocampus encodes and preserves the temporal order of sequential information irrespective of the nature of that information. We used multivariate pattern analyses (MVPA) of functional magnetic resonance imaging (fMRI) data acquired in young healthy individuals during the execution of learned sequences of movements and objects to test whether the hippocampus represents information about the temporal order of items in a learned sequence irrespective of their nature. We also examined such coding in brain regions involved in both motor (primary and premotor cortices) and object (perirhinal cortex and parahippocampus) sequence learning. Our results suggest that hippocampal and perirhinal multivoxel activation patterns do not carry information about specific items or temporal position in a random series of objects or movements. Rather, these regions code for the representation of items in their learned temporal position in sequences irrespective of their nature (i.e., item-position coding). In contrast, although all other ROIs showed evidence of item-position coding, this representation could - at least partially - be attributed to the coding of other information such as position information. Altogether, our findings indicate that the capacity of regions in the medial temporal lobe to represent the temporal order of sequential information is domain-general. Our data suggest that these regions contribute to the development of item-position maps that might provide a cognitive framework to order sequential behaviors irrespective of their nature.

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Effect of interhemispheric zero-phase entrainment of the intrinsic mu-rhythm on behavioral and neural markers of predictive coding

Goal-directed behavior requires the integration of information from the outside world and internal (somatosensory) sources about our own actions. Expectations (or internal models) are generated from prior knowledge and constantly updated based on sensory feedback. This optimized information integration (predictive coding) results in a global behavioral advantage of anticipated action in the presence of uncertainty. Our goal was to probe the effect of phase entrainment of the sensorimotor mu-rhythm on visuomotor integration. Participants received transcranial alternating current stimulation over bilateral motor cortices (M1) while performing a visually-guided force adjustment task during functional magnetic resonance imaging. Inter-hemispheric zero-phase entrainment resulted in effector-specific modulation of performance precision and effector-generic minimization of force signal complexity paralleled by BOLD activation changes in bilateral caudate and increased functional connectivity between the right M1 and contralateral putamen, inferior parietal, and medial temporal regions. While effector-specific changes in performance precision were associated with contralateral caudate and hippocampal activation decreases, only the global reduction in force signal complexity was associated with increased functional M1 connectivity with bilateral striatal regions. We propose that zero-phase synchronization represents a neural mode of optimized information integration related to internal model updating within the recursive perception-action continuum associated with predictive coding.

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Neurophysiological Correlates of Phase-Specific Enhancement of Motor Memory Consolidation via Slow-Wave Closed-Loop Targeted Memory Reactivation

Memory consolidation can be enhanced during sleep using targeted memory reactivation (TMR) and closed-loop (CL) acoustic stimulation on the up-phase of slow oscillations (SOs). Here, we tested whether applying TMR at specific phases of the SOs (up vs. down vs. no reactivation) could influence the behavioral and neural correlates of motor memory consolidation in healthy young adults. Results showed that up- (as compared to down-) state cueing resulted in greater performance improvement. Sleep electrophysiological data indicated that up-stimulated SOs exhibited higher amplitude and greater peak-nested sigma power. Task-related functional magnetic resonance images revealed that up-state cueing strengthened activity in - and segregation of - striato-motor and hippocampal networks; and that these modulations were related to the beneficial effect of TMR on sleep features and performance. Overall, these findings highlight the potential of CL-TMR to induce phase-specific modulations of motor performance, sleep oscillations and brain responses during motor memory consolidation.

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Children exhibit a developmental advantage in the offline processing of a learned motor sequence

Research that examines changes in a specific behavior across the lifespan frequently reports an inverted-U trajectory. That is, young adults exhibit optimal performance, children are conceptualized as developing systems progressing towards this ideal state, and older adulthood is characterized by performance decrements. However, not all behaviors follow this trajectory, as there are instances in which children outperform young adults. This study aimed to reveal instances of childhood advantage in the domain of motor learning and memory consolidation. Using a visually cued serial reaction time task, data were acquired from 7-35 and >55-year-old participants (n=238 datasets) across two experiments that assessed initial encoding as well as memory consolidation over 5-hour and 24-hour offline periods. Results revealed comparable initial learning dynamics among age groups, but 7- to 12-year-old children exhibited smaller sequence-specific learning relative to adolescents (13-17 year-olds), young adults (18-35 year-olds) and older adults (> 55 years). Interestingly, children demonstrated the greatest performance gains in the 5-hour and 24-hour delayed retests, reflecting enhanced motor memory consolidation. These results suggest that children exhibit an advantage in the offline processing of recently learned motor sequences.

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The hippocampus binds movements to their temporal position in a motor sequence

A plethora of daily motor tasks consist of sequences of movements or steps that need to be performed in a specific order. Yet, it remains unclear how the brain represents sequential motor actions in a way that preserves their temporal order. Here, we used multivoxel pattern similarity analysis of functional Magnetic Resonance Imaging (fMRI) data acquired during motor sequence practice to investigate whether the hippocampus, a brain region known to support temporal order in the non-motor memory domain, represents information about the temporal order of sequential motor actions. We also examined such representation in other regions of the motor network (i.e., the premotor cortex (PMC), supplementary motor area (SMA), anterior superior parietal lobule (aSPL) and striatum) known for their critical role in motor sequence learning. Our results show that hippocampal activation patterns carried information about movements in their learned temporal position in the sequence (i.e., movement-position binding), but not about movements or positions in random movement patterns. In contrast, other ROIs showed evidence of binding in the sequence as well as movement (M1, SMA, PMC, putamen and aSPL) and position (aSPL and PMC) coding in random movement patterns. Importantly, movement coding contributed to sequence learning patterns in M1, SMA and PMC but not in the putamen and aSPL, suggesting a specific involvement of these regions in movement-position binding. Altogether, our findings provide novel insight into the role of the hippocampus in the motor memory domain and point to its capacity to bind movements to their temporal position in a motor sequence. Our results also deepen our understanding of how striatal and cortical regions contribute to motor sequence learning via movement coding or movement-position binding. Significance StatementConsistent evidence collected over the last two decades indicates that the hippocampus - a brain structure traditionally associated to declarative memory - is critically involved in motor memory. Yet, the functional role and representational contribution of the hippocampus during motor learning remains to be elucidated. Using a multivariate functional MRI approach, we show here that the hippocampus binds movements to their temporal position in a learned sequence of actions. These results point towards the involvement of the hippocampus in preserving information about temporal order in motor memory - a process well described for declarative memories. We suggest that the ability of the hippocampus to encode temporal order during sequence learning is common across declarative and non-declarative memory systems.

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Prefrontal stimulation disrupts motor memory consolidation at the micro timescale

Functional brain responses in hippocampo- and striato-cortical networks during initial motor sequence learning (MSL) are critical for memory consolidation. We have recently shown that prefrontal stimulation applied prior to initial MSL can alter these learning-related responses. In the present study, we investigated whether such stimulation-induced modulations of brain responses can influence motor memory consolidation at different timescales. Specifically, we examined the effect of prefrontal stimulation on the behavioral and neural responses associated to (i) fast consolidation processes occurring during short rest episodes interspersed with practice during initial learning (i.e., micro timescale) and (ii) slow consolidation process taking place across practice sessions separated by 24h (i.e., macro timescale). To do so, we applied active (inhibitory or facilitatory) or control theta-burst stimulation to the prefrontal cortex of young healthy participants before they were trained on an MSL task while their brain activity was recorded using functional magnetic resonance imaging (fMRI). Motor performance was retested, in the MRI scanner, after a night of sleep. Both our behavioral and brain imaging results indicate that while stimulation did not modulate consolidation at the macro timescale, it disrupted the micro-offline consolidation process. Specifically, our behavioral data indicate that active - as compared to control - stimulation resulted in a decrease in micro-offline gains in performance over the short rest intervals. At the brain level, stimulation disrupted activity in the caudate nucleus and the hippocampus during the micro-offline intervals. Additionally, multivariate pattern persistence from task into inter-practice rest episodes - which is thought to reflect the reactivation of learning-related patterns - was hindered by active prefrontal stimulation in the hippocampus and caudate nucleus. Importantly, stimulation also altered the link between the brain and the behavioral markers of the micro-offline consolidation process. These results collectively suggest that active prefrontal stimulation prior to MSL disrupted both the behavioral and neural correlates of motor memory consolidation at the micro timescale.

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Electrophysiological signatures of targeted memory reactivation during sleep are not accompanied by motor performance improvements in older adults

Targeted memory reactivation (TMR) during sleep enhances memory consolidation in young adults by modulating electrophysiological markers of neuroplasticity. Interestingly, older adults exhibit deficits in motor memory consolidation, an impairment that has been linked to age-related degradations in the same sleep features sensitive to TMR. We hypothesized that TMR would enhance consolidation in older adults via the modulation of these markers. Seventeen older participants were trained on a motor task involving two auditory-cued sequences. During a post-learning nap, two auditory cues were played: one associated to a learned (i.e., reactivated) sequence and one control. Performance during two delayed retests did not differ between reactivated and non-reactivated sequences. Moreover, both associated and control sounds modulated brain responses, yet there were no consistent differences between the auditory cue types. Our results collectively demonstrate that older adults do not benefit from specific reactivation of a motor memory trace by an associated auditory cue during post-learning sleep. It is possible, however, that auditory stimulation during post-learning sleep boosts motor memory consolidation in a non-specific manner.

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Sleep does not influence schema-facilitated motor memory consolidation

Study ObjectivesNovel information is rapidly learned when it is compatible with previous knowledge. This "schema" effect, initially described for declarative memories, was recently extended to the motor memory domain. Importantly, this beneficial effect was only observed 24 hours - but not immediately - following motor schema acquisition. Given the established role of sleep in memory consolidation, we hypothesized that sleep following the initial learning of a schema is necessary for the subsequent rapid integration of novel motor information. MethodsTwo experiments were conducted to investigate the effect of diurnal and nocturnal sleep on schema-mediated motor sequence memory consolidation. In Experiment 1, participants first learned an 8-element motor sequence through repeated practice (Session 1). They were then afforded a 90-minute nap opportunity (N=25) or remained awake (N=25) before learning a second motor sequence (Session 2) which was highly compatible with that learned prior to the sleep/wake interval. Experiment 2 was similar; however, Sessions 1 and 2 were separated by a 12-hour interval that included nocturnal sleep (N=28) or only wakefulness (N=29). ResultsFor both experiments, we found no group differences in motor sequence performance (reaction time and accuracy) following the sleep/wake interval. Furthermore, in Experiment 1, we found no correlation between sleep features (non-REM sleep duration, spindle and slow wave activity) and post-sleep behavioral performance. ConclusionsThe results of this research suggest that integration of novel motor information into a cognitive-motor schema does not specifically benefit from post-learning sleep.

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Connectivity in Large-Scale Resting State Brain Networks is Related to Motor Learning: a High-Density EEG Study

Previous research has shown that resting-state functional connectivity (rsFC) between different brain regions (seeds) is related to motor learning and motor memory consolidation. Using high-density electroencephalography (hdEEG) we addressed this question from a brain network perspective. Specifically, we examined frequency-dependent functional connectivity in resting-state networks from twenty-nine young healthy participants before and after they were trained on a motor sequence learning task. Consolidation was assessed with an overnight retest on the motor task. We showed training-related decreases in gamma band connectivity within the motor network, and between the motor and functionally distinct resting-state networks including the attentional network. Brain-behavior correlation analyses revealed that baseline beta, delta and theta rsFC was related to subsequent motor learning and memory consolidation such that lower connectivity within the motor network and between the motor and several distinct resting-state networks was correlated with better learning and overnight consolidation. Last, training-related increases in beta-band connectivity between the motor and the visual networks were related to greater consolidation. Altogether our results indicate that connectivity in large-scale resting-state brain networks is related to - and modulated by - motor learning and memory consolidation processes. These finding corroborate previous seed-based connectivity research and provide evidence that frequency-dependent functional connectivity in resting state networks is critically linked to motor learning and memory consolidation.

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Sigma Oscillations Protect or Reinstate Motor Memory Depending on their Temporal Coordination with Slow Waves

Targeted memory reactivation (TMR) during post-learning sleep is known to enhance motor memory consolidation but the underlying neurophysiological processes remain unclear. Here, we confirm the beneficial effect of auditory TMR on motor performance. At the neural level, TMR enhanced slow wave (SW) characteristics. Additionally, greater TMR-related phase-amplitude coupling between slow (0.5-2 Hz) and sigma (12-16 Hz) oscillations after the SW peak was related to higher TMR effect on performance. Importantly, sounds that were not associated to learning strengthened SW-sigma coupling at the SW trough and the increase in sigma power nested in the trough of the potential evoked by these unassociated sounds was related to the TMR benefit. Altogether, our data suggest that, depending on their precise temporal coordination during post learning sleep, slow and sigma oscillations play a crucial role in either memory reinstatement or protection against irrelevant information; two processes that critically contribute to motor memory consolidation.

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