Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding.
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ABSTRACT:
SUBMITTER: Kirov R
PROVIDER: S-EPMC2730962 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5-1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5-16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9-12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO-fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO-SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories.
| S-EPMC6374430 | biostudies-literature
Project description:Synchronization of neural activity within local networks and between brain regions is a major contributor to rhythmic field potentials such as the EEG. On the other hand, dynamic changes in microstructure and activity are reflected in the EEG, for instance slow oscillation (SO) slope can reflect synaptic strength. SO-spindle coupling is a measure for neural communication. It was previously associated with memory consolidation, but also shown to reveal strong interindividual differences. In studies, weak electric current stimulation has modulated brain rhythms and memory retention. Here, we investigate whether SO-spindle coupling and SO slope during baseline sleep are associated with (predictive of) stimulation efficacy on retention performance. Twenty-five healthy subjects participated in three experimental sessions. Sleep-associated memory consolidation was measured in two sessions, in one anodal transcranial direct current stimulation oscillating at subjects individual SO frequency (so-tDCS) was applied during nocturnal sleep. The third session was without a learning task (baseline sleep). The dependence on SO-spindle coupling and SO-slope during baseline sleep of so-tDCS efficacy on retention performance were investigated. Stimulation efficacy on overnight retention of declarative memories was associated with nesting of slow spindles to SO trough in deep nonrapid eye movement baseline sleep. Steepness and direction of SO slope in baseline sleep were features indicative for stimulation efficacy. Findings underscore a functional relevance of activity during the SO up-to-down state transition for memory consolidation and provide support for distinct consolidation mechanisms for types of declarative memories.
| S-EPMC8503833 | biostudies-literature
Project description:Sleep constitutes a privileged state for new memories to reactivate and consolidate. Previous work has demonstrated that consolidation can be bolstered experimentally either via delivery of reminder cues (targeted memory reactivation [TMR]) or via noninvasive brain stimulation geared toward enhancing endogenous sleep rhythms. Here, we combined both approaches, controlling the timing of TMR cues with respect to ongoing slow-oscillation (SO) phases. Prior to sleep, participants learned associations between unique words and a set of repeating images (e.g., car) while hearing a prototypical image sound (e.g., engine starting). Memory performance on an immediate test vs. a test the next morning quantified overnight memory consolidation. Importantly, two image sounds were designated as TMR cues, with one cue delivered at SO UP states and the other delivered at SO DOWN states. A novel sound was used as a TMR control condition. Behavioral results revealed a significant reduction of overnight forgetting for words associated with UP-state TMR compared with words associated with DOWN-state TMR. Electrophysiological results showed that UP-state cueing led to enhancement of the ongoing UP state and was followed by greater spindle power than DOWN-state cueing. Moreover, UP-state (and not DOWN-state) cueing led to reinstatement of target image representations. Together, these results unveil the behavioral and mechanistic effects of delivering reminder cues at specific phases of endogenous sleep rhythms and mark an important step for the endeavor to experimentally modulate memories during sleep.
| S-EPMC9636934 | biostudies-literature
Project description:Intermittent theta burst stimulation (iTBS) is a noninvasive brain stimulation technique capable of increasing cortical excitability beyond the stimulation period. Due to the rapid induction of modulatory effects, prefrontal application of iTBS is gaining popularity as a therapeutic tool for psychiatric disorders such as depression. In an attempt to increase efficacy, higher than conventional intensities are currently being applied. The assumption that this increases neuromodulatory may be mechanistically false for iTBS. This study examined the influence of intensity on the neurophysiological and behavioural effects of iTBS in the prefrontal cortex. Sixteen healthy participants received iTBS over prefrontal cortex at either 50, 75 or 100% resting motor threshold in separate sessions. Single-pulse TMS and concurrent electroencephalography (EEG) was used to assess changes in cortical reactivity measured as TMS-evoked potentials and oscillations. The n-back task was used to assess changes in working memory performance. The data can be summarised as an inverse U-shape relationship between intensity and iTBS plastic effects, where 75% iTBS yielded the largest neurophysiological changes. Improvement in reaction time in the 3-back task was supported by the change in alpha power, however, comparison between conditions revealed no significant differences. The assumption that higher intensity results in greater neuromodulatory effects may be false, at least in healthy individuals, and should be carefully considered for clinical populations. Neurophysiological changes associated with working memory following iTBS suggest functional relevance. However, the effects of different intensities on behavioural performance remain elusive in the present healthy sample.
| S-EPMC6866298 | biostudies-literature
Project description:A dysfunction in the excitatory-inhibitory (E/I) coordination in neuronal assembly has been proposed as a possible neurobiological mechanism of Autistic Spectrum Disorder (ASD). However, the potential impact of this mechanism in cognitive performance is not fully explored. Since the main consequence of E/I dysfunction is an impairment in oscillatory activity and its underlying cognitive computations, we assessed the electroencephalographic activity of ASD and typically developing (TD) subjects during a working-memory task. We found that ASD subjects committed more errors than TD subjects. Moreover, TD subjects demonstrated a parametric modulation in the power of alpha and theta band while ASD subjects did not demonstrate significant modulations. The preceding leads to significant differences between the groups in both the alpha power placed on the occipital cortex and the theta power placed on the left premotor and the right prefrontal cortex. The impaired theta modulation correlated with autistic symptoms. The results indicated that ASD may present an alteration in the recruitment of the oscillatory activity during working-memory, and this alteration could be related to the physiopathology of the disorder.
| S-EPMC5662653 | biostudies-literature
Project description:The implications of the substantial individual differences in infant sleep for early brain development remain unclear. Here, we examined whether night sleep quality relates to daytime brain activity, operationalized through measures of EEG theta power and its dynamic modulation, which have been previously linked to later cognitive development. For this longitudinal study, 76 typically developing infants were studied (age: 4-14 months, 166 individual study visits) over the course of 6 months with one, two, three, or four lab visits. Habitual sleep was measured with a 7-day sleep diary and actigraphy, and the Brief Infant Sleep Questionnaire. Twenty-channel EEG was recorded while infants watched multiple rounds of videos of women singing nursery rhymes; oscillatory power in the theta band was extracted. Key metrics were average theta across stimuli and the slope of change in theta within the first novel movie. Both objective and subjective sleep assessment methods showed a relationship between more night waking and higher overall theta power and reduced dynamic modulation of theta over the course of the novel video stimuli. These results may indicate altered learning and consolidation in infants with more disrupted night sleep, which may have implications for cognitive development.
| S-EPMC9828365 | biostudies-literature
Project description:Precise temporal coordination of slow oscillations (SO) and sleep spindles is a fundamental mechanism of sleep-dependent memory consolidation. SO and spindle morphology changes considerably throughout development. Critically, it remains unknown how the precise temporal coordination of these two sleep oscillations develops during brain maturation and whether their synchronization indexes the development of memory networks. Here, we use a longitudinal study design spanning from childhood to adolescence, where participants underwent polysomnography and performed a declarative word-pair learning task. Performance on the memory task was better during adolescence. After disentangling oscillatory components from 1/f activity, we found frequency shifts within SO and spindle frequency bands. Consequently, we devised an individualized cross-frequency coupling approach, which demonstrates that SO-spindle coupling strength increases during maturation. Critically, this increase indicated enhanced memory formation from childhood to adolescence. Our results provide evidence that improved coordination between SOs and spindles indexes the development of sleep-dependent memory networks.
| S-EPMC7314542 | biostudies-literature
Project description:BackgroundTheta-band neuronal oscillations in the prefrontal cortex are associated with several cognitive functions. Oscillatory phase is an important correlate of excitability and phase synchrony mediates information transfer between neuronal populations oscillating at that frequency. The ability to extract and exploit the prefrontal theta rhythm in real time in humans would facilitate insight into neurophysiological mechanisms of cognitive processes involving the prefrontal cortex, and development of brain-state-dependent stimulation for therapeutic applications.ObjectivesWe investigate individual source-space beamforming-based estimation of the prefrontal theta oscillation as a method to target specific phases of the ongoing theta oscillations in the human dorsomedial prefrontal cortex (DMPFC) with real-time EEG-triggered transcranial magnetic stimulation (TMS). Different spatial filters for extracting the prefrontal theta oscillation from EEG signals are compared and additional signal quality criteria are assessed to take into account the dynamics of this cortical oscillation.MethodsTwenty two healthy participants were recruited for anatomical MRI scans and EEG recordings with 18 composing the final analysis. We calculated individual spatial filters based on EEG beamforming in source space. The extracted EEG signal was then used to simulate real-time phase-detection and quantify the accuracy as compared to post-hoc phase estimates. Different spatial filters and triggering parameters were compared. Finally, we validated the feasibility of this approach by actual real-time triggering of TMS pulses at different phases of the prefrontal theta oscillation.ResultsHigher phase-detection accuracy was achieved using individualized source-based spatial filters, as compared to an average or standard Laplacian filter, and also by detecting and avoiding periods of low theta amplitude and periods containing a phase reset. Using optimized parameters, prefrontal theta-phase synchronized TMS of DMPFC was achieved with an accuracy of ±55°.ConclusionThis study demonstrates the feasibility of triggering TMS pulses during different phases of the ongoing prefrontal theta oscillation in real time. This method is relevant for brain state-dependent stimulation in human studies of cognition. It will also enable new personalized therapeutic repetitive TMS protocols for more effective treatment of neuropsychiatric disorders.
| S-EPMC8255809 | biostudies-literature
Project description:STUDY OBJECTIVES: Thalamo-cortical spindles driven by the up-state of neocortical slow (< 1 Hz) oscillations (SOs) represent a candidate mechanism of memory consolidation during sleep. We examined interactions between SOs and spindles in human slow wave sleep, focusing on the presumed existence of 2 kinds of spindles, i.e., slow frontocortical and fast centro-parietal spindles. DESIGN: Two experiments were performed in healthy humans (24.5 ± 0.9 y) investigating undisturbed sleep (Experiment I) and the effects of prior learning (word paired associates) vs. non-learning (Experiment II) on multichannel EEG recordings during sleep. MEASUREMENTS AND RESULTS: Only fast spindles (12-15 Hz) were synchronized to the depolarizing SO up-state. Slow spindles (9-12 Hz) occurred preferentially at the transition into the SO down-state, i.e., during waning depolarization. Slow spindles also revealed a higher probability to follow rather than precede fast spindles. For sequences of individual SOs, fast spindle activity was largest for "initial" SOs, whereas SO amplitude and slow spindle activity were largest for succeeding SOs. Prior learning enhanced this pattern. CONCLUSIONS: The finding that fast and slow spindles occur at different times of the SO cycle points to disparate generating mechanisms for the 2 kinds of spindles. The reported temporal relationships during SO sequences suggest that fast spindles, driven by the SO up-state feed back to enhance the likelihood of succeeding SOs together with slow spindles. By enforcing such SO-spindle cycles, particularly after prior learning, fast spindles possibly play a key role in sleep-dependent memory processing.
| S-EPMC3174843 | biostudies-other
Project description:The coupling of gamma oscillation (~ 40+ Hz) amplitude to the phase of ongoing theta (~ 6 Hz) oscillations has been proposed to be directly relevant for memory performance. Current theories suggest that memory capacity scales with number of gamma cycles that can be fitted into the preferred phase of a theta cycle. Following this logic, transcranial alternating current stimulation (tACS) may be used to adjust theta cycles (increasing/decreasing theta frequency) to decrease or increase memory performance during stimulation. Here, we used individualized EEG-informed theta tACS to (1) experimentally “slow down” individual theta frequency (ITF), (2) evaluate cognitive after effects on a battery of memory and learning tasks, and (3) link the cognitive performance changes to tACS-induced effects on theta-band oscillations as measured by post EEG. We found frequency- and task-specific tACS after effects demonstrating a specific enhancement in memory capacity. This tACS-induced cognitive enhancement was specific to the visual memory task performed immediately after tACS offset, and specific to the ITF-1 Hz (slowing) stimulation condition and thus following a protocol specifically designed to slow down theta frequency to enhance memory capacity. Follow-up correlation analyses in this group linked the enhanced memory performance to increased left frontal-parietal theta-band connectivity. Interestingly, resting-state theta power immediately after tACS offset revealed a theta power increase not for the ITF-1 Hz group, but only for the ITF group where the tACS frequency was ‘optimal’ for entrainment. These results suggest that while individually calibrated tACS at peak frequency maximally modulates resting-state oscillatory power, tACS stimulation slightly below this optimal peak theta frequency is better suited to enhance memory capacity performance. Importantly, our results further suggest that such cognitive enhancement effects can last beyond the period of stimulation and are linked to increased network connectivity, opening the door towards more clinical and applied relevance of using tACS in cognitive rehabilitation and/or neurocognitive enhancement.
| S-EPMC9392784 | biostudies-literature