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Hassan, U.

Publications and source records attributed to Hassan, U..

15 recordsLinked to original sources

SafeLens: A Statistically Controlled Nonlinear Machine Learning Framework for Characterizing Hidden Dynamics in Event-Locked Neural Activity

Machine learning has advanced rapidly over the past decade, yet event-locked neural activity is still analyzed predominantly with traditional statistics and linear models. While traditional linear methods provide computationally tractable statistical control for pre-selected features or trial-averaged waveforms, they miss subtle nonlinear and trial-varying neural dynamics. Nonlinear models can capture these complex patterns, but their feature reliance is opaque and notoriously difficult to threshold statistically. We introduce SafeLens (Searchlight Analysis of Fluctuation Events, Leveraging Extensive Null Sampling) to combine the power of nonlinear machine learning with the rigorous false-positive control of traditional statistical inference. At each position of a sliding window, a random forest learns to discriminate event-locked activity from interleaved resting-state neural activity using multiscale temporal derivatives. Randomized feature ablation inverts slope polarity in held-out trials to map the random forest models' reliance on specific rising versus falling excursions across the time-frequency space. SafeLens then establishes an empirical null by running the same pipeline on separate resting-state recordings, training forests to discriminate rest from rest. This empirical null translates each channel's complex nonlinear resting dynamics into a model-matched noise floor on the map's linear reliance scale, allowing a single threshold to control the family-wise error rate against the channel's own background structure rather than a summary statistic of its baseline. When we injected simulated cortico-cortical evoked potentials (CCEPs) into resting intracranial EEG recordings, SafeLens recovered ~2.5 times as many polarity-resolved deflections as trial-average thresholding and the closest data-driven method, maintaining its advantage under trial-to-trial variability while yielding ~5-11 times fewer false components, ~2-5 times lower mean boundary error, and superior single-trial latency tracking as a timing prior. In eight patients, CCEPs remained detectable above chance until 1,040 ms after stimulation, compared with 570 and 455 ms for those benchmarks. Together, these findings establish SafeLens as a novel solution for enabling nonlinear models to uncover subtle, trial-varying neural dynamics under strict statistical control.

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Suppression of corticospinal excitability by sleep spindles without increase in GABAergic inhibition

Thalamocortical sleep spindles are hypothesised to support memory consolidation during sleep by creating transient windows of enhanced hippocampal-neocortical communication and synaptic plasticity. A recent real-time electroencephalography (EEG)-triggered transcranial magnetic stimulation (TMS) study found a pulsed suppression of corticospinal excitability during spindles relative to spindle-free non-rapid eye movement (NREM) sleep, driven by the spindle falling phase. We hypothesised that this phasic suppression may reflect local inhibitory network dynamics, measurable as GABA-A receptor-mediated short-interval intracortical inhibition (SICI) using paired-pulse TMS. We applied real-time EEG-triggered single- and paired-pulse TMS over the primary motor cortex during pre-sleep wakefulness, spindle-free N2/N3 sleep, and at four sleep spindle phases (peak, falling, trough, and rising). Corticospinal excitability was strongly reduced from wakefulness to spindle-free N2/N3 sleep, and further suppressed during sleep spindles. Numerically, excitability was lowest during the falling phase and trough, although we found no significant modulation across spindle phases. Contrary to our hypothesis, neither spindle presence nor phase significantly modulated SICI. Secondary analyses provided preliminary evidence that slow oscillations present at stimulation increased excitability and reduced SICI, irrespective of spindle presence. Together, these findings indicate distinct contributions of sleep/wake vigilance states, sleep spindles, and slow oscillations to cortical network dynamics, and provide new insight into the transient modulation of corticospinal excitability and GABA-A-receptor mediated SICI during human NREM sleep.

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Cognitive load modulates cortical excitability in the human prefrontal cortex

The prefrontal cortex dynamically adjusts its excitability to meet changing cognitive demands, yet our understanding of how these rapid state changes unfold in real time remains limited. Existing evidence relies predominantly on correlational neuroimaging and invasive electrophysiology in clinical populations, neither of which affords causal measurement in healthy humans. Here, using concurrent single-pulse TMS-EEG during a parametric cognitive multi-source interference task (MSIT) in 27 healthy participants, we causally probed left prefrontal excitability across conditions spanning a range of cognitive interference levels. Prefrontal excitability scaled systematically with cognitive load, peaking at intermediate incongruency levels where trial-type uncertainty was greatest, and differentiating high-from low-conflict trials at the single-subject level. Critically, prefrontal excitability and midfrontal theta power showed parallel state dependency patterns, linking causal perturbation of prefrontal circuit responsiveness to an established oscillatory marker of cognitive control. The observed excitability modulation was selective to the left prefrontal cortex: stimulation of right dlPFC, pre-SMA, and vertex in a separate control cohort (N=5) produced no load-dependent effects. These results position prefrontal excitability as a real-time, regionally selective physiological readout of how the human prefrontal cortex adapts to cognitive demand. HighlightsO_LIWe evaluated the links between cognitive interference, prefrontal excitability, and intrinsic theta activity during a multi-source interference task C_LIO_LICognitive load, estimated based on behavioral performance, was greatest at at intermediate interference levels (33% congruent), where trial-type uncertainty was maximal C_LIO_LIPrefrontal excitability, measured via single-pulse TMS-evoked potentials, scaled with cognitive load C_LIO_LIEffects were observed at the single subject level and were specific to prefrontal stimulation C_LIO_LIPrefrontal excitability changes and midfrontal theta power showed parallel scaling with cognitive load, linking causal probing to established oscillatory markers C_LIO_LIThis noninvasive technique provides causal measurement of prefrontal engagement during cognitive processing C_LIO_LIThe methodology demonstrates potential for tracking brain state dynamics in both healthy cognition and neuropsychiatric disorders C_LI

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Transcranial magnetic stimulation to the dorsolateral prefrontal cortex modulates single-neuron activity in humans

Transcranial magnetic stimulation (TMS) to the dorsolateral prefrontal cortex (dlPFC) is an FDA-cleared treatment for depression, yet how cortical stimulation influences single neurons in deep brain circuits remains unknown. Using intracranial microelectrode recordings in four neurosurgical patients, we resolved single-neuron spikes as early as 8 ms from 185 single neurons after single-pulse left dlPFC TMS. TMS elicited time-locked firing responses in 46% of neurons across deep cortical and subcortical structures bilaterally. TMS facilitated putative interneuron spiking in striato-thalamic regions from [~]8 ms, peaking at [~]80-100 ms, and lasting to [~]1000 ms, while suppressing putative pyramidal cell spiking with a delayed and slower time course. Trial-by-trial single-neuron modulations were positively correlated with cortico-striato-thalamic network activity and anti-correlated with limbic network activity. These findings reveal that dlPFC TMS facilitates inhibitory firing in executive control networks while suppressing limbic excitatory drive, providing a cellular mechanism for how cortical stimulation modulates distributed brain networks.

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Development and Validation of the Transcranial Magnetic Stimulation Reporting Assessment Tool(TMS-RAT)

HighlightsO_LIWe introduce the TMS-RAT, a reporting (assessment) tool for TMS studies C_LIO_LIDeveloped within a community-informed, iterative process rating 333 TMS studies C_LIO_LIEmpirically evaluated for usability, inter-rater, and test-retest reliability C_LIO_LIA validated subset enables reliable retrospective assessment of reporting C_LIO_LIThe modular structure enables use across a wide range of TMS study designs C_LI BackgroundA standardised tool for comprehensive reporting can improve transparency, support consistent documentation, and enable comparison across transcranial magnetic stimulation (TMS) studies. The most used reporting checklist lacks clear definitions of full reporting and was not initially evaluated for usability or inter-rater reliability. A scoping review of studies using this checklist shows that its items are reported only 50% of the time, suggesting that method descriptions are often incomplete. MethodsWe developed the TMS Reporting Assessment Tool (TMS-RAT), a comprehensive reporting framework that provides clear definitions and examples for its items, covering a wide range of TMS protocols. We tested the usability and reliability of the TMS-RAT by rating all studies published between 1991 and 2025 using afferent conditioning (n = 333), a protocol encompassing many reporting categories identified during tool development. Seventeen independent raters contributed across three development phases, a validation phase, and a retest phase, with naive raters introduced in each phase. Iterative refinements of the tool were informed by inter-rater reliability, qualitative rater feedback, and consultation with external TMS experts. ResultsWe present two versions of the tool: the 72-item TMS-RAT v1.0, designed to guide comprehensive reporting, and the TMS-RAT v1.1, a subset of 50 items with the highest inter-rater (overall AC1 = 0.78, range = [0.60-0.99]) and test-retest reliability (overall AC1 = 0.82, range = [0.65-1.0]), intended for retrospective evaluation of reporting in systematic reviews, meta-analyses. ConclusionThe TMS-RAT is a comprehensive, reliable tool that seeks to improve transparency and reproducibility in TMS research.

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TMS timed to interictal epileptiform discharges

Interictal epileptiform discharges (IEDs) are pathological hypersynchronous bursts of electrical brain activity that occur between seizures in patients with epilepsy. IEDs are caused by transient brain states that are difficult to predict, making them a challenging neurophysiological and technological case for brain-state-dependent stimulation. Administering stimulation at IED onset may provide insight into the epileptic network and optimize neurostimulation therapies. Here, we assessed the feasibility of IED-triggered transcranial magnetic stimulation (TMS) in two children with self-limited epilepsy with centrotemporal spikes (SeLECTS), a common pediatric epilepsy in which IEDs emerge from the motor cortex. A convolutional neural network (CNN) was trained on the participants pre-recorded electroencephalography (EEG) data with IEDs annotated by an epileptologist. The CNN was integrated into an EEG-processing pipeline that classified EEG segments as "IED" or "non-IED" in real time. With this pipeline, TMS pulses were administered during IED or non-IED periods in an interleaved, randomized design. We stimulated both the motor cortex generating the IEDs and the contralateral motor cortex and tested the impact of IEDs on TMS-evoked potentials (TEPs). Our study demonstrated that TMS can be timed to IEDs and that there is a site-specific increase in TEP amplitude when stimulating during IEDs. Out of the TMS pulses aimed at an IED, 39% and 19% were successfully delivered during an IED for the two participants, respectively. For future research, we propose ways to address the methodological challenges of IED-timed TMS, enabling brain-state-dependent TMS for epilepsy research and treatment.

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Noninvasive profiling of input-output excitability curves in human prefrontal cortex

Abstract.O_ST_ABSBackgroundC_ST_ABSThe prefrontal cortex plays a critical role in cognitive control and behavior, and its dysfunction has been linked to numerous psychiatric and neurological disorders. However, noninvasive measurement of prefrontal activity remains challenging, limiting our understanding of how to optimize prefrontal treatments. Input-output relationships reveal how neural circuits respond to different inputs and are essential for determining optimal treatment parameters and understanding individual variability in treatment response, yet systematic investigation of prefrontal input-output relationships has been lacking. ObjectiveTo characterize human prefrontal excitability with input-output (I/O) curves. MethodsWe employed transcranial magnetic stimulation (TMS) with electroencephalography in a randomized mixed-block design with 28 healthy participants receiving single-pulse TMS to left dorsolateral prefrontal cortex (dlPFC) across 12 stimulation intensities (60-140% of resting motor threshold). We quantified prefrontal excitability using early local TMS-evoked potentials (EL-TEPs), cortical responses measured locally 20-60 ms post-stimulus. ResultsWe observed a strong effect of TMS intensity on prefrontal EL-TEP amplitudes. Sigmoidal EL-TEP I/O curves were observed in 57% of participants, with the sigmoidality partially explained by EL-TEP signal quality. Correlations were observed between EL-TEP and motor-evoked potential curve parameters, but intensity parameterization approaches did not significantly differ in explaining inter-individual EL-TEP response variability. Reliable EL-TEPs could be obtained using fewer TMS pulses at high intensities, and test- retest assessments revealed robust I/O curve profiles. ConclusionsThese findings provide a systematic noninvasive characterization of prefrontal input-output physiology, establishing a framework for estimating prefrontal excitability. The comparison of various intensity parameterizations motivates the need for enhanced models and individualized measurement of stimulation responses. HighlightsO_LIWe present noninvasive input-output curves for prefrontal TMS. C_LIO_LIEL-TEPs exhibit robust dose-dependent responses to TMS intensity. C_LIO_LISigmoidal I/O curves observed in 57% of participants, with a strong dependence on signal quality. C_LIO_LICorrelations observed between MEP and prefrontal EL-TEP curve parameters. C_LIO_LIHigh test-retest reliability and rapid protocols at [≥]110% rMT C_LI

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A Practical Preprocessing Pipeline for Concurrent TMS-iEEG: Critical Steps and Methodological Considerations

Transcranial magnetic stimulation combined with intracranial EEG (TMS-iEEG) has emerged as a powerful approach for probing the causal organization and dynamics of the human brain. Despite its promise, the presence of TMS-induced artifacts poses significant challenges for accurately characterizing and interpreting evoked neural responses. In this study, we present a practical preprocessing pipeline for single pulse TMS-iEEG data, incorporating key steps of re-referencing, filtering, artifact interpolation, and detrending. Using both real and simulated data, we systematically evaluated the effects of each step and compared alternative methodological choices. Our results demonstrate that this pipeline effectively attenuated various types of artifacts and noise, yielding cleaner signals for the subsequent analysis of intracranial TMS-evoked potentials (iTEPs). Moreover, we showed that methodological choices can substantially influence iTEPs outcomes. In particular, referencing methods might strongly affect iTEP morphology and amplitude, underscoring the importance of tailoring the referencing strategy to specific signal characteristics and research objectives. For filtering, we recommend a segment-based strategy, i.e., applying filters to data segments excluding the artifact window, to minimize distortion from abrupt TMS-related transients. Overall, this work represents an important step toward establishing a general preprocessing framework for TMS-iEEG data. We hope it encourages broader adoption and methodological development in concurrent TMS-iEEG research, ultimately advancing our understanding of brain organization and TMS mechanisms. HighlightsO_LIWe presented a practical preprocessing pipeline for single pulse TMS-iEEG data, incorporating key steps of re-referencing, filtering, artifact interpolation, and detrending. C_LIO_LIThe pipeline effectively attenuates multiple types of artifacts and noise, enabling accurate characterization of evoked neural responses. C_LIO_LIMethodological alternatives for each preprocessing step were evaluated using real and/or simulated datasets. C_LIO_LIRe-referencing substantially affects the morphology and amplitude of intracranial TMS-evoked potentials and requires careful consideration. C_LIO_LIA segment-based filtering strategy is recommended to better minimize distortion from TMS-related artifacts. C_LI

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Sensory Entrained TMS (seTMS) enhances motor cortex plasticity

Neural excitability fluctuates with sensory events, creating windows of opportunity to enhance brain stimulation. Repetitive transcranial magnetic stimulation (TMS), including intermittent theta burst stimulation (iTBS), is a promising treatment for neurological and psychiatric disorders, but does not account for fluctuations in neural excitability, likely contributing to variable outcomes. Sensory Entrained TMS (seTMS) leverages sensorimotor oscillations to enhance corticospinal responses, but the sustained effects as a repetitive protocol are unknown. We extended seTMS to iTBS measuring motor-evoked potentials (MEPs) as a physiological readout in a randomized crossover study comparing standard iTBS with sensory entrained iTBS (se-iTBS, n=20). se-iTBS more than doubled the MEP effect (55% vs. 26% MEP enhancement) and persisted for at least 30 minutes. Notably, more than 80% of participants showed larger responses with se-iTBS at all time points. se-iTBS may provide a robust and practical framework for optimizing TMS that bridges electrophysiological mechanisms and clinical applications.

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An increased excitation and inhibition onto CA1 pyramidal cells sets the path to Alzheimer s disease

Synapses are critical targets of Alzheimers disease (AD), a highly prevalent neurodegenerative disease associated with accumulation of extracellular amyloid-{beta} peptides. Although amyloidosis and aggregation of the 42-amino acid amyloid-{beta} (A{beta}42) have long been considered pathogenic triggers for AD, clinical evidence linking high levels of A{beta}42 with normal cognition challenges this hypothesis. To resolve this conundrum on the role of A{beta}42 in regulating synaptic activity, we used an adeno-associated viral vector approach that triggers extracellular accumulation of A{beta}42 and spatial memory impairment. We show that A{beta}42 leads to an early increase in excitatory and proximal inhibitory synaptic transmission onto hippocampal CA1 pyramidal cells, and an increased expression of the glutamate transporter GLT-1 in these cells. A{beta}42 accumulation does not cause early cognitive deficits unless accompanied by an increased neuronal GLT-1 expression, suggesting this transporter is a critical mediator of A{beta}42s effects. These findings unveil key molecular and cellular mechanisms implicated with AD pathogenesis.

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DLPFC Stimulation Suppresses High-Frequency Neural Activity in the Human sgACC

Transcranial magnetic stimulation (TMS) to the dorsolateral prefrontal cortex (DLPFC) is hypothesized to relieve symptoms of depression by inhibiting activity in the subgenual anterior cingulate cortex (sgACC). However, we have a limited understanding of how TMS influences neural activity in the sgACC, owing to its deep location within the brain. To better understand the mechanism of antidepressant response to TMS, we recruited two neurosurgical patients with indwelling electrodes and delivered TMS pulses to the DLPFC while simultaneously recording local field potentials from the sgACC. Spectral analysis revealed a decrease in high-frequency activity (HFA; 70-180 Hz) after each stimulation pulse, which was especially pronounced in the sgACC relative to other regions. TMS-evoked HFA power was generally anticorrelated between the DLPFC and sgACC, even while low-frequency phase locking between the two regions was enhanced. Together, these findings support the notion that TMS to the DLPFC can suppress neural firing in the sgACC, suggesting a possible mechanism by which this treatment regulates mood.

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Sensory Entrained TMS (seTMS) enhances motor cortex excitability

Transcranial magnetic stimulation (TMS) applied to the motor cortex has revolutionized the study of motor physiology in humans. Despite this, TMS-evoked electrophysiological responses show significant variability, due in part to inconsistencies between TMS pulse timing and ongoing brain oscillations. Variable responses to TMS limit mechanistic insights and clinical efficacy, necessitating the development of methods to precisely coordinate the timing of TMS pulses to the phase of relevant oscillatory activity. We introduce Sensory Entrained TMS (seTMS), a novel approach that uses musical rhythms to synchronize brain oscillations and time TMS pulses to enhance cortical excitability. Focusing on the sensorimotor alpha rhythm, a neural oscillation associated with motor cortical inhibition, we examine whether rhythm-evoked sensorimotor alpha phase alignment affects primary motor cortical (M1) excitability in healthy young adults (n=33). We first confirmed using electroencephalography (EEG) that passive listening to musical rhythms desynchronizes inhibitory sensorimotor brain rhythms (mu oscillations) around 200 ms before auditory rhythmic events (27 participants). We then targeted this optimal time window by delivering single TMS pulses over M1 200 ms before rhythmic auditory events while recording motor-evoked potentials (MEPs; 19 participants), which resulted in significantly larger MEPs compared to standard single pulse TMS and an auditory control condition. Neither EEG measures during passive listening nor seTMS-induced MEP enhancement showed dependence on musical experience or training. These findings demonstrate that seTMS effectively enhances corticomotor excitability and establishes a practical, cost-effective method for optimizing non-invasive brain stimulation outcomes.

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Pulsed inhibition of corticospinal excitability by the thalamocortical sleep spindle

Thalamocortical sleep spindles, i.e., oscillatory bursts at [~]12-15 Hz of waxing and waning amplitude, are a hallmark feature of non-rapid eye movement (NREM) sleep and believed to play a key role in sleep-dependent memory reactivation and consolidation. Generated in the thalamus and projecting to neocortex and hippocampus, they are phasically modulated by neocortical slow oscillations (<1 Hz) and in turn phasically modulate hippocampal sharp-wave ripples (>80 Hz). This hierarchical cross-frequency nesting may enable phase-dependent plasticity in the neocortex, and spindles have thus been considered windows of plasticity in the sleeping brain. However, the assumed phasic excitability modulation had not yet been demonstrated for spindles. Utilizing a recently developed real-time spindle detection algorithm, we applied spindle phase-triggered transcranial magnetic stimulation (TMS) to the primary motor cortex (M1) hand area and measured motor evoked potentials (MEP) to characterize corticospinal excitability during sleep spindles. We found a net suppression of MEP amplitudes during spindles, driven by selective inhibition during the falling flank of the spindle oscillation, but no inhibition during its peak, rising flank, and trough. Importantly, this phasic inhibition occurred on top of the general sleep-related inhibition observed during spindle-free NREM sleep and did not extend into the immediate refractory post-spindle periods. We conclude that spindles exert asymmetric "pulsed inhibition" of corticospinal excitability, which is assumedly relevant for processes of phase-dependent plasticity. These findings and the developed real-time spindle targeting methods will enable future studies to uncover the causal role of spindles in synaptic plasticity and systems memory consolidation.

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Auditory confounds can drive online effects of transcranial ultrasonic stimulation in humans

Transcranial ultrasonic stimulation (TUS) is rapidly emerging as a promising non-invasive neuromodulation technique. TUS is already well-established in animal models, providing foundations to now optimize neuromodulatory efficacy for human applications. Across multiple studies, one promising protocol, pulsed at 1000 Hz, has consistently resulted in motor cortical inhibition in humans (Fomenko et al., 2020). At the same time, a parallel research line has highlighted the potentially confounding influence of peripheral auditory stimulation arising from TUS pulsing at audible frequencies. In this study, we disentangle direct neuromodulatory and indirect auditory contributions to motor inhibitory effects of TUS. To this end, we include tightly matched control conditions across four experiments, one preregistered, conducted independently at three institutions. We employed a combined transcranial ultrasonic and magnetic stimulation paradigm, where TMS-elicited motor-evoked potentials (MEPs) served as an index of corticospinal excitability. First, we replicated motor inhibitory effects of TUS but showed through both tight controls and manipulation of stimulation intensity, duration, and auditory masking conditions that this inhibition was driven by peripheral auditory stimulation, not direct neuromodulation. Further, we consider neuromodulation beyond driving overall excitation/inhibition and show preliminary evidence of how TUS might interact with ongoing neural dynamics instead. Primarily, this study highlights the substantial shortcomings in accounting for the auditory confound in prior TUS-TMS work where only a flip-over sham and no active control was used. The field must critically reevaluate previous findings given the demonstrated impact of peripheral confounds. Further, rigorous experimental design via (in)active control conditions is required to make substantiated claims in future TUS studies. Only when direct effects are disentangled from those driven by peripheral confounds can TUS fully realize its potential for research and clinical applications.

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Automated real-time EEG sleep spindle detection for brain state-dependent brain stimulation

Sleep spindles are a hallmark electroencephalographic (EEG) feature of non-rapid eye movement (NREM) sleep and believed to be instrumental for sleep-dependent memory reactivation and consolidation. However, direct proof of their causal relevance is hard to obtain, and our understanding of their immediate neurophysiological consequences is limited. To investigate their causal role, spindles need to be targeted in real-time with sensory or non-invasive brain stimulation techniques. While fully automated offline detection algorithms are well established, spindle detection in real time is highly challenging due to their spontaneous and transient nature. Here, we present the real-time spindle detector (RTSD), a robust multi-channel EEG signal processing algorithm that enables the automated triggering of stimulation during sleep spindles in a phase-specific manner. We validated the RTSD method by streaming pre-recorded sleep EEG datasets to a real-time computer system running a Simulink(R) Real-Time implementation of the algorithm. Sleep spindles were detected with high levels of sensitivity ([~]83%) and precision ([~]78%) and an F1-score of [~]0.81 in reference to state-of-the-art offline algorithms (which reached similar levels when compared to each other), for both naps and full nights, and largely independent of sleep scoring information. Detected spindles were comparable in frequency, duration, amplitude, and symmetry, and showed the typical time-frequency characteristics as well as a centroparietal topography. Spindles were detected close to their center and reliably at the predefined target phase. The RTSD algorithm therefore empowers researchers to target spindles during human sleep and apply the stimulation method and experimental paradigm of their choice.

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