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Sleep benefits motor memory consolidation. This mnemonic process is thought to be mediated by thalamo-cortical spindle activity during NREM-stage2 sleep episodes as well as changes in striatal and hippocampal activity. However, direct experimental evidence supporting the contribution of such sleep-dependent physiological mechanisms to motor memory consolidation in humans is lacking. In the present study, we combined EEG and fMRI sleep recordings following practice of a motor sequence learning (MSL) task to determine whether spindle oscillations support sleep-dependent motor memory consolidation by transiently synchronizing and coordinating specialized cortical and subcortical networks. To that end, we conducted EEG source reconstruction on spindle epochs in both cortical and subcortical regions using novel deep-source localization techniques. Coherence-based metrics were adopted to estimate functional connectivity between cortical and subcortical structures over specific frequency bands. Our findings not only confirm the critical and functional role of NREM-stage2 sleep spindles in motor skill consolidation, but provide first-time evidence that spindle oscillations [11–17 Hz] may be involved in sleep-dependent motor memory consolidation by locally reactivating and functionally binding specific task-relevant cortical and subcortical regions within networks including the hippocampus, putamen, thalamus and motor-related cortical regions.

As the world's population ages, a deeper understanding of the relationship between aging and motor learning will become increasingly relevant in basic research and applied settings. In this context, this review aims to address the effects of age on motor sequence learning (MSL) and motor adaptation (MA) with respect to behavioral, neurological, and neuroimaging findings. Previous behavioral research investigating the influence of aging on motor learning has consistently reported the following results. First, the initial acquisition of motor sequences is not altered, except under conditions of increased task complexity. Second, older adults demonstrate deficits in motor sequence memory consolidation. And, third, although older adults demonstrate deficits during the exposure phase of MA paradigms, the aftereffects following removal of the sensorimotor perturbation are similar to young adults, suggesting that the adaptive ability of older adults is relatively intact. This paper will review the potential neural underpinnings of these behavioral results, with a particular emphasis on the influence of age-related dysfunctions in the cortico-striatal system on motor learning.

The transition from wakefulness to sleep is accompanied by widespread changes in brain functioning. Here we investigate the implications of this transition for interregional functional connectivity and their dynamic changes over time. Simultaneous EEG-fMRI was used to measure brain functional activity of 21 healthy participants as they transitioned from wakefulness into sleep. fMRI volumes were independent component analysis (ICA)-decomposed, yielding 42 neurophysiological sources. Static functional connectivity (FC) was estimated from independent component time courses. A sliding window method and k-means clustering (k = 7, L2-norm) were used to estimate dynamic FC. Static FC in Wake and Stage-2 Sleep (NREM2) were largely similar. By contrast, FC dynamics across wake and sleep differed, with transitions between FC states occurring more frequently during wakefulness than during NREM2. Evidence of slower FC dynamics during sleep is discussed in relation to sleep-related reductions in effective connectivity and synaptic strength.

Sleep resting state network (RSN) functional connectivity (FC) is poorly understood, particularly for rapid eye movement (REM), and in non-sleep deprived subjects. REM and non-REM (NREM) sleep involve competing drives; towards hypersynchronous cortical oscillations in NREM; and towards wake-like desynchronized oscillations in REM. This study employed simultaneous electroencephalography-functional magnetic resonance imaging (EEG-fMRI) to explore whether sleep RSN FC reflects these opposing drives. As hypothesized, this was confirmed for the majority of functional connections modulated by sleep. Further, changes were directional: e.g., positive wake correlations trended towards negative correlations in NREM and back towards positive correlations in REM. Moreover, the majority did not merely reduce magnitude, but actually either reversed and strengthened in the opposite direction, or increased in magnitude during NREM. This finding supports the notion that NREM is best expressed as having altered , rather than reduced FC. Further, as many of these functional connections comprised “higher-order” RSNs (which have been previously linked to cognition and consciousness), such as the default mode network, this finding is suggestive of possibly concomitant alterations to cognition and consciousness.

Simultaneous electroencephalography and functional magnetic resonance imaging (EEG-fMRI) studies have revealed brain activations time-locked to spindles. Yet, the functional significance of these spindle-related brain activations is not understood. EEG studies have shown that inter-individual differences in the electrophysiological characteristics of spindles (e.g., density, amplitude, duration) are highly correlated with \"Reasoning\" abilities (i.e., \"fluid intelligence\"; problem solving skills, the ability to employ logic, identify complex patterns), but not short-term memory (STM) or verbal abilities. Spindle-dependent reactivation of brain areas recruited during new learning suggests night-to-night variations reflect offline memory processing. However, the functional significance of stable, trait-like inter-individual differences in brain activations recruited during spindle events is unknown. Using EEG-fMRI sleep recordings, we found that a subset of brain activations time-locked to spindles were specifically related to Reasoning abilities but were unrelated to STM or verbal abilities. Thus, suggesting that individuals with higher fluid intelligence have greater activation of brain regions recruited during spontaneous spindle events. This may serve as a first step to further understand the function of sleep spindles and the brain activity which supports the capacity for Reasoning.

Abstract Study Objectives The behavioral and cognitive consequences of severe sleep deprivation are well understood. Surprisingly, relatively little is known about the neural correlates of mild and acute sleep restriction on tasks that require sustained vigilance for prolonged periods of time during the day. Methods and Results Event-related potential (ERP) paradigms can reveal insight into the neural correlates underlying visual processing and behavioral responding that is impaired with reduced alertness, as a consequence of sleep loss. Here, we investigated the impact of reduced vigilance following at-home mild sleep restriction to better understand the associated behavioral consequences and changes in information processing revealed by ERPs. As expected, vigilance was reduced (e.g. increased lapses and response slowing) that increased over the course of the experiment in the “sleep restricted” (5 hr sleep) compared with the “sleep-extension” (9 hr sleep) condition. Corresponding to these lapses, we found decreased positivity of visually evoked potentials in the Sleep Restriction vs. Sleep Extension condition emerging from 316 to 449 ms, maximal over parietal/occipital cortex. We also investigated electrophysiological signs of motor-related processing by comparing lateralized readiness potentials (LRPs) and found reduced positivity of LRPs in the Sleep Restriction vs. Sleep Extension condition at 70–40 ms before, and 115–158 ms after a response was made. Conclusions These results suggest that even a single night of mild sleep restriction can negatively affect vigilance, reflected by reduced processing capacity for decision making, and dulls motor preparation and execution.

Spindles are often temporally coupled to slow waves (SW). These SW-spindle complexes have been implicated in memory consolidation that involves transfer of information from the hippocampus to the neocortex. However, spindles and SW, which are characteristic of NREM sleep, can occur as part of this complex, or in isolation. It is not clear whether dissociable parts of the brain are recruited when coupled to SW vs. when spindles or SW occur in isolation. Here, we tested differences in cerebral activation time-locked to uncoupled spindles, uncoupled SW and coupled SW-spindle complexes using simultaneous EEG-fMRI. Consistent with the “ active system model ,” we hypothesized that brain activations time-locked to coupled SW-spindles would preferentially occur in brain areas known to be critical for sleep-dependent memory consolidation. Our results show that coupled spindles and uncoupled spindles recruit distinct parts of the brain. Specifically, we found that hippocampal activation during sleep is not uniquely related to spindles. Rather, this process is primarily driven by SWs and SW-spindle coupling. In addition, we show that SW-spindle coupling is critical in the activation of the putamen. Importantly, SW-spindle coupling specifically recruited frontal areas in comparison to uncoupled spindles, which may be critical for the hippocampal-neocortical dialogue that preferentially occurs during sleep.

A spindle detection method was developed that: (1) extracts the signal of interest (i.e., spindle-related phasic changes in sigma) relative to ongoing \"background\" sigma activity using complex demodulation, (2) accounts for variations of spindle characteristics across the night, scalp derivations and between individuals, and (3) employs a minimum number of sometimes arbitrary, user-defined parameters. Complex demodulation was used to extract instantaneous power in the spindle band. To account for intra- and inter-individual differences, the signal was z-score transformed using a 60 s sliding window, per channel, over the course of the recording. Spindle events were detected with a z-score threshold corresponding to a low probability (e.g., 99th percentile). Spindle characteristics, such as amplitude, duration and oscillatory frequency, were derived for each individual spindle following detection, which permits spindles to be subsequently and flexibly categorized as slow or fast spindles from a single detection pass. Spindles were automatically detected in 15 young healthy subjects. Two experts manually identified spindles from C3 during Stage 2 sleep, from each recording; one employing conventional guidelines, and the other, identifying spindles with the aid of a sigma (11-16 Hz) filtered channel. These spindles were then compared between raters and to the automated detection to identify the presence of true positives, true negatives, false positives and false negatives. This method of automated spindle detection resolves or avoids many of the limitations that complicate automated spindle detection, and performs well compared to a group of non-experts, and importantly, has good external validity with respect to the extant literature in terms of the characteristics of automatically detected spindles.

Sleep is essential for the optimal consolidation of newly acquired memories. This study examines the neurophysiological processes underlying memory consolidation during sleep, via reactivation. Here, we investigated the impact of slow wave - spindle (SW-SP) coupling on regionally-task-specific brain reactivations following motor sequence learning. Utilizing simultaneous EEG-fMRI during sleep, our findings revealed that memory reactivation occured time-locked to coupled SW-SP complexes, and specifically in areas critical for motor sequence learning. Notably, these reactivations were confined to the hemisphere actively involved in learning the task. This regional specificity highlights a precise and targeted neural mechanism, underscoring the crucial role of SW-SP coupling. In addition, we observed double-dissociation whereby primary sensory areas were recruited time-locked to uncoupled spindles; suggesting a role for uncoupled spindles in sleep maintenance. These findings advance our understanding the functional significance of SW-SP coupling for enhancing memory in a regionally-specific manner, that is functionally dissociable from uncoupled spindles. Simultaneous EEG-fMRI shows that slow wave-coupled sleep spindles promote region-specific memory reactivation after motor learning, revealing distinct roles for coupled vs. uncoupled spindles in sleep-dependent memory consolidation.

Reconsolidation theory posits that upon retrieval, consolidated memories are destabilized and need to be restabilized in order to persist. It has been suggested that experience with a competitive task immediately after memory retrieval may interrupt these restabilization processes leading to memory loss. Indeed, using a motor sequence learning paradigm, we have recently shown that, in humans, interference training immediately after active task-based retrieval of the consolidated motor sequence knowledge may negatively affect its performance levels. Assessing changes in tapping pattern before and after interference training, we also demonstrated that this performance deficit more likely indicates a genuine memory loss rather than an initial failure of memory retrieval. Here, applying a similar approach, we tested the necessity of the hypothetical retrieval-induced destabilization of motor memory to allow its impairment. The impact of memory retrieval on performance of a new motor sequence knowledge acquired during the interference training was also evaluated. Similar to the immediate post-retrieval interference, interference training alone without the preceding active task-based memory retrieval was also associated with impairment of the pre-established motor sequence memory. Performance levels of the sequence trained during the interference training, on the other hand, were impaired only if this training was given immediately after memory retrieval. Noteworthy, an 8-hour interval between memory retrieval and interference allowed to express intact performance levels for both sequences. The current results suggest that susceptibility of the consolidated motor memory to behavioral interference is independent of its active task-based retrieval. Differential effects of memory retrieval on performance levels of the new motor sequence encoded during the interference training further suggests that memory retrieval may influence the way new information is stored by facilitating its integration within the retrieved memory trace. Thus, impairment of the pre-established motor memory may reflect interference from a competing memory trace rather than involve interruption of reconsolidation.