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OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome. METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively). RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control. CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates. SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.
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Neuronal oscillations at about 10 Hz, called alpha oscillations, are often thought to arise from synchronous activity across occipital cortex, reflecting general cognitive states such as arousal and alertness. However, there is also evidence that modulation of alpha oscillations in visual cortex can be spatially specific. Here, we used intracranial electrodes in human patients to measure alpha oscillations in response to visual stimuli whose location varied systematically across the visual field. We separated the alpha oscillatory power from broadband power changes. The variation in alpha oscillatory power with stimulus position was then fit by a population receptive field (pRF) model. We find that the alpha pRFs have similar center locations to pRFs estimated from broadband power (70-180 Hz), but are several times larger. The results demonstrate that alpha suppression in human visual cortex can be precisely tuned. Finally, we show how the pattern of alpha responses can explain several features of exogenous visual attention. Significance Statement: The alpha oscillation is the largest electrical signal generated by the human brain. An important question in systems neuroscience is the degree to which this oscillation reflects system-wide states and behaviors such as arousal, alertness, and attention, versus much more specific functions in the routing and processing of information. We examined alpha oscillations at high spatial precision in human patients with intracranial electrodes implanted over visual cortex. We discovered a surprisingly high spatial specificity of visually driven alpha oscillations, which we quantified with receptive field models. We further use our discoveries about properties of the alpha response to show a link between these oscillations and the spread of visual attention.
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Neural responses to visual stimuli exhibit complex temporal dynamics, including subadditive temporal summation, response reduction with repeated or sustained stimuli (adaptation), and slower dynamics at low contrast. These phenomena are often studied independently. Here, we demonstrate these phenomena within the same experiment and model the underlying neural computations with a single computational model. We extracted time-varying responses from electrocorticographic recordings from patients presented with stimuli that varied in duration, interstimulus interval (ISI) and contrast. Aggregating data across patients from both sexes yielded 98 electrodes with robust visual responses, covering both earlier (V1-V3) and higher-order (V3a/b, LO, TO, IPS) retinotopic maps. In all regions, the temporal dynamics of neural responses exhibit several nonlinear features. Peak response amplitude saturates with high contrast and longer stimulus durations, the response to a second stimulus is suppressed for short ISIs and recovers for longer ISIs, and response latency decreases with increasing contrast. These features are accurately captured by a computational model composed of a small set of canonical neuronal operations, that is, linear filtering, rectification, exponentiation, and a delayed divisive normalization. We find that an increased normalization term captures both contrast- and adaptation-related response reductions, suggesting potentially shared underlying mechanisms. We additionally demonstrate both changes and invariance in temporal response dynamics between earlier and higher-order visual areas. Together, our results reveal the presence of a wide range of temporal and contrast-dependent neuronal dynamics in the human visual cortex and demonstrate that a simple model captures these dynamics at millisecond resolution.SIGNIFICANCE STATEMENT Sensory inputs and neural responses change continuously over time. It is especially challenging to understand a system that has both dynamic inputs and outputs. Here, we use a computational modeling approach that specifies computations to convert a time-varying input stimulus to a neural response time course, and we use this to predict neural activity measured in the human visual cortex. We show that this computational model predicts a wide variety of complex neural response shapes, which we induced experimentally by manipulating the duration, repetition, and contrast of visual stimuli. By comparing data and model predictions, we uncover systematic properties of temporal dynamics of neural signals, allowing us to better understand how the brain processes dynamic sensory information.
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Encéfalo , Corteza Visual , Masculino , Femenino , Humanos , Estimulación Luminosa/métodos , Encéfalo/fisiología , Mapeo Encefálico/métodos , Factores de Tiempo , Corteza Visual/fisiologíaRESUMEN
Intracranial human recordings are a valuable and rare resource of information about the brain. Making such data publicly available not only helps tackle reproducibility issues in science, it helps make more use of these valuable data. This is especially true for data collected using naturalistic tasks. Here, we describe a dataset collected from a large group of human subjects while they watched a short audiovisual film. The dataset has several unique features. First, it includes a large amount of intracranial electroencephalography (iEEG) data (51 participants, age range of 5-55 years, who all performed the same task). Second, it includes functional magnetic resonance imaging (fMRI) recordings (30 participants, age range of 7-47) during the same task. Eighteen participants performed both iEEG and fMRI versions of the task, non-simultaneously. Third, the data were acquired using a rich audiovisual stimulus, for which we provide detailed speech and video annotations. This dataset can be used to study neural mechanisms of multimodal perception and language comprehension, and similarity of neural signals across brain recording modalities.
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Electrocorticografía , Imagen por Resonancia Magnética , Adolescente , Adulto , Encéfalo/diagnóstico por imagen , Encéfalo/fisiología , Mapeo Encefálico/métodos , Niño , Preescolar , Humanos , Persona de Mediana Edad , Reproducibilidad de los Resultados , Habla , Adulto JovenRESUMEN
Electrocorticography (ECoG) is typically employed to accurately identify the seizure focus as well as the location of brain functions to be spared during surgical resection in participants with drug-resistant epilepsy. Increasingly, this technique has become a powerful tool to map cognitive functions onto brain regions. Cortical mapping is more commonly investigated with functional MRI (fMRI), which measures blood-oxygen level dependent (BOLD) changes induced by neuronal activity. The multimodal integration between typical 3T fMRI activity maps and ECoG measurements can provide unique insight into the spatiotemporal aspects of cognition. However, the optimal integration of fMRI and ECoG requires fundamental insight into the spatial smoothness of the BOLD signal under each electrode. Here we use ECoG as ground truth for the extent of activity, as each electrode is thought to record from the cortical tissue directly underneath the contact, to estimate the spatial smoothness of the associated BOLD response at 3T fMRI. We compared the high-frequency broadband (HFB) activity recorded with ECoG while participants performed a motor task. Activity maps were obtained with fMRI at 3T for the same task in the same participant prior to surgery. We then correlated HFB power with the fMRI BOLD signal change in the area around each electrode. This latter measure was quantified by applying a 3D Gaussian kernel of varying width (sigma between 1 mm and 20 mm) to the fMRI maps including only gray-matter. We found that the correlation between HFB and BOLD activity increased sharply up to the point when the kernel width was set to 4 mm, which we defined as the kernel width of maximal spatial specificity. After this point, as the kernel width increased, the highest level of explained variance was reached at a kernel width of 9 mm for most participants. Intriguingly, maximal specificity was also limited to 4 mm for low-frequency bands, such as alpha and beta, but the kernel width with the highest explained variance was less spatially limited than the HFB. In summary, spatial specificity is limited to a kernel width of 4 mm but explained variance keeps on increasing as you average over more and more voxels containing the relatively noisy BOLD signal. Future multimodal studies should choose the kernel width based on their research goal. For maximal spatial specificity, ECoG electrodes are best compared to 3T fMRI with a kernel width of 4 mm. When optimizing the correlation between modalities, highest explained variance can be obtained at larger kernel widths of 9 mm, at the expense of spatial specificity. Finally, we release the complete pipeline so that researchers can estimate the most appropriate kernel width from their multimodal datasets.
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Electrocorticografía/métodos , Imagen por Resonancia Magnética/métodos , Corteza Motora/diagnóstico por imagen , Adolescente , Adulto , Mapeo Encefálico/métodos , Niño , Electrodos Implantados , Electroencefalografía , Femenino , Humanos , Masculino , Persona de Mediana Edad , Estimulación Luminosa , Desempeño Psicomotor/fisiología , Adulto JovenRESUMEN
In vivo electrophysiology experiments require the collection of data from multiple subjects, often for extended periods. Studying multiple subjects for extended periods can be made more efficient through simultaneous recordings, but scaling up recordings to accommodate larger numbers of subjects simultaneously requires coordination and consideration of costs and flexibility. To facilitate this process, we have developed OpBox, an open source set of tools to acquire electroencephalography (EEG) and electromyography (EMG) flexibly from multiple rodent subjects simultaneously. OpBox combines open source hardware and software with off-the-shelf components to create a system that costs less than commercial solutions ($500 per subject), and can be easily deployed for multiple subjects. Coded in MATLAB, OpBox scripts can simultaneously and flexibly collect and display multiple analog and digital data streams, for instance real-time EEG and EMG, event triggers from a behavioral system, and rotary encoder data. OpBox also calculates and displays real-time spectral representations and event-related potentials (ERPs). To verify the performance of our system, we compare our amplifiers with two other commercial amplifiers, a Grass P55 AC preamplifier and an Intan RHD2000-series amplifier. The OpBox amplifier performs comparably to commercial amplifiers for signal-to-noise ratios (SNRs), noise floors, and common mode rejection. We also demonstrate that our acquisition system can reliably record multichannel data from multiple subjects, and has been successfully tested with 12 subjects running simultaneously on a single standard desktop computer. Together, OpBox increases the flexibility and lowers the cost for simultaneous acquisition of electrophysiology data from multiple subjects.
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Electroencefalografía , Programas Informáticos , Electromiografía , Potenciales Evocados , Procesamiento de Señales Asistido por Computador , Relación Señal-RuidoRESUMEN
During awake consciousness, the brain intrinsically maintains a dynamical state in which it can coordinate complex responses to sensory input. How the brain reaches this state spontaneously is not known. General anesthesia provides a unique opportunity to examine how the human brain recovers its functional capabilities after profound unconsciousness. We used intracranial electrocorticography and scalp EEG in humans to track neural dynamics during emergence from propofol general anesthesia. We identify a distinct transient brain state that occurs immediately prior to recovery of behavioral responsiveness. This state is characterized by large, spatially distributed, slow sensory-evoked potentials that resemble the K-complexes that are hallmarks of stage two sleep. However, the ongoing spontaneous dynamics in this transitional state differ from sleep. These results identify an asymmetry in the neurophysiology of induction and emergence, as the emerging brain can enter a state with a sleep-like sensory blockade before regaining responsivity to arousing stimuli.
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Periodo de Recuperación de la Anestesia , Corteza Cerebral/fisiología , Estado de Conciencia/fisiología , Propofol/administración & dosificación , Sueño/fisiología , Adulto , Corteza Cerebral/efectos de los fármacos , Estado de Conciencia/efectos de los fármacos , Electroencefalografía , Potenciales Evocados , Femenino , Humanos , Hipnóticos y Sedantes/farmacología , Masculino , Persona de Mediana Edad , Sensación/efectos de los fármacos , Adulto JovenRESUMEN
Human intracranial electroencephalography (iEEG) recordings provide data with much greater spatiotemporal precision than is possible from data obtained using scalp EEG, magnetoencephalography (MEG), or functional MRI. Until recently, the fusion of anatomical data (MRI and computed tomography (CT) images) with electrophysiological data and their subsequent analysis have required the use of technologically and conceptually challenging combinations of software. Here, we describe a comprehensive protocol that enables complex raw human iEEG data to be converted into more readily comprehensible illustrative representations. The protocol uses an open-source toolbox for electrophysiological data analysis (FieldTrip). This allows iEEG researchers to build on a continuously growing body of scriptable and reproducible analysis methods that, over the past decade, have been developed and used by a large research community. In this protocol, we describe how to analyze complex iEEG datasets by providing an intuitive and rapid approach that can handle both neuroanatomical information and large electrophysiological datasets. We provide a worked example using an example dataset. We also explain how to automate the protocol and adjust the settings to enable analysis of iEEG datasets with other characteristics. The protocol can be implemented by a graduate student or postdoctoral fellow with minimal MATLAB experience and takes approximately an hour to execute, excluding the automated cortical surface extraction.
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Encéfalo/anatomía & histología , Encéfalo/fisiología , Electrocorticografía/métodos , Procesamiento Automatizado de Datos/métodos , Neuroanatomía/métodos , Humanos , Programas InformáticosRESUMEN
OBJECTIVE: The treatment of focal epilepsies is largely predicated on the concept that there is a "focus" from which the seizure emanates. Yet, the physiological context that determines if and how ictal activity starts and propagates remains poorly understood. To delineate these phenomena more completely, we studied activity outside the seizure-onset zone prior to and during seizure initiation. METHODS: Stereotactic depth electrodes were implanted in 17 patients with longstanding pharmacoresistant epilepsy for lateralization and localization of the seizure-onset zone. Only seizures with focal onset in mesial temporal structures were used for analysis. Spectral analyses were used to quantify changes in delta, theta, alpha, beta, gamma, and high gamma frequency power, in regions inside and outside the area of seizure onset during both preictal and seizure initiation periods. RESULTS: In the 78 seizures examined, an average of 9.26% of the electrode contacts outside of the seizure focus demonstrated changes in power at seizure onset. Of interest, seizures that were secondarily generalized, on average, showed power changes in a greater number of extrafocus electrode contacts at seizure onset (16.7%) compared to seizures that remained focal (3.8%). The majority of these extrafocus changes occupied the delta and theta bands in electrodes placed in the ipsilateral, lateral temporal lobe. Preictally, we observed extrafocal high-frequency power decrements, which also correlated with seizure spread. SIGNIFICANCE: This widespread activity at and prior to the seizure-onset time further extends the notion of the ictogenic focus and its relationship to seizure spread. Further understanding of these extrafocus, periictal changes might help identify the neuronal dynamics underlying the initiation of seizures and how therapies can be devised to control seizure activity.
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Epilepsia Refractaria/fisiopatología , Electroencefalografía , Epilepsias Parciales/fisiopatología , Epilepsia Generalizada/fisiopatología , Adulto , Anciano , Correlación de Datos , Ritmo Delta/fisiología , Dominancia Cerebral/fisiología , Electrodos Implantados , Femenino , Humanos , Masculino , Persona de Mediana Edad , Lóbulo Temporal/fisiopatología , Ritmo Teta/fisiología , Adulto JovenRESUMEN
Perception is strongly affected by the intrinsic state of the brain, which controls the propensity to either maintain a particular perceptual interpretation or switch to another. To understand the mechanisms underlying the spontaneous drive of the brain to explore alternative interpretations of unchanging stimuli, we repeatedly recorded high-density EEG after normal sleep and after sleep deprivation while participants observed a Necker cube image and reported the durations of the alternating representations of their bistable perception. We found that local alpha power around the parieto-occipital sulcus within the first second after the emergence of a perceptual representation predicted the fate of its duration. An experimentally induced increase in alpha power by means of sleep deprivation increased the average duration of individual representations. Taken together, these findings show that high alpha power promotes the stability of a perceptual representation and suppresses switching to the alternative. The observations support the hypothesis that synchronization of alpha oscillations across a wide neuronal network promotes the maintenance and stabilization of its current perceptual representation. Elevated alpha power could also be key to the poorly understood cognitive deficits, that typically accompany sleep deprivation, such as the loss of mental flexibility and lapses of responsiveness.
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Ritmo alfa/fisiología , Atención , Encéfalo/fisiología , Estimulación Luminosa/métodos , Percepción Visual/fisiología , Adulto , Electroencefalografía , Femenino , Humanos , Masculino , Análisis y Desempeño de Tareas , Adulto JovenRESUMEN
Since their discovery almost one century ago, sleep spindles, 0.5-2s long bursts of oscillatory activity at 9-16Hz during NREM sleep, have been thought to be global and relatively uniform throughout the cortex. Recent work, however, has brought this concept into question but it remains unclear to what degree spindles are global or local and if their properties are uniform or location-dependent. We addressed this question by recording sleep in eight patients undergoing evaluation for epilepsy with intracranial electrocorticography, which combines high spatial resolution with extensive cortical coverage. We find that spindle characteristics are not uniform but are strongly influenced by the underlying cortical regions, particularly for spindle density and fundamental frequency. We observe both highly isolated and spatially distributed spindles, but in highly skewed proportions: while most spindles are restricted to one or very few recording channels at any given time, there are spindles that occur over widespread areas, often involving lateral prefrontal cortices and superior temporal gyri. Their co-occurrence is affected by a subtle but significant propagation of spindles from the superior prefrontal regions and the temporal cortices towards the orbitofrontal cortex. This work provides a brain-wide characterization of sleep spindles as mostly local graphoelements with heterogeneous characteristics that depend on the underlying cortical area. We propose that the combination of local characteristics and global organization reflects the dual properties of the thalamo-cortical generators and provides a flexible framework to support the many functions ascribed to sleep in general and spindles specifically.
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Corteza Cerebral/fisiología , Sueño , Adulto , Electrocorticografía , Epilepsia/fisiopatología , Femenino , Humanos , Masculino , Persona de Mediana Edad , Fases del Sueño , Adulto JovenRESUMEN
During sleep, the thalamus generates a characteristic pattern of transient, 11-15 Hz sleep spindle oscillations, which synchronize the cortex through large-scale thalamocortical loops. Spindles have been increasingly demonstrated to be critical for sleep-dependent consolidation of memory, but the specific neural mechanism for this process remains unclear. We show here that cortical spindles are spatiotemporally organized into circular wave-like patterns, organizing neuronal activity over tens of milliseconds, within the timescale for storing memories in large-scale networks across the cortex via spike-time dependent plasticity. These circular patterns repeat over hours of sleep with millisecond temporal precision, allowing reinforcement of the activity patterns through hundreds of reverberations. These results provide a novel mechanistic account for how global sleep oscillations and synaptic plasticity could strengthen networks distributed across the cortex to store coherent and integrated memories.
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Ondas Encefálicas , Corteza Cerebral/fisiología , Memoria , Sueño , Tálamo/fisiología , Electrocorticografía , Humanos , Análisis Espacio-TemporalRESUMEN
Sleep spindles arise from the interaction of thalamic and cortical neurons. Neurons in the thalamic reticular nucleus (TRN) inhibit thalamocortical neurons, which in turn excite the TRN and cortical neurons. A fundamental principle of anatomical organization of the thalamocortical projections is the presence of two pathways: the diffuse matrix pathway and the spatially selective core pathway. Cortical layers are differentially targeted by these two pathways with matrix projections synapsing in superficial layers and core projections impinging on middle layers. Based on this anatomical observation, we propose that spindles can be classified into two classes, those arising from the core pathway and those arising from the matrix pathway, although this does not exclude the fact that some spindles might combine both pathways at the same time. We find evidence for this hypothesis in EEG/MEG studies, intracranial recordings, and computational models that incorporate this difference. This distinction will prove useful in accounting for the multiple functions attributed to spindles, in that spindles of different types might act on local and widespread spatial scales. Because spindle mechanisms are often hijacked in epilepsy and schizophrenia, the classification proposed in this review might provide valuable information in defining which pathways have gone awry in these neurological disorders.
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Corteza Cerebral/fisiología , Neuronas/fisiología , Sueño/fisiología , Tálamo/fisiología , Electroencefalografía , Humanos , Vías Nerviosas/fisiología , Sinapsis/fisiologíaRESUMEN
Central brain network connections greatly contribute to overall network efficiency. Here we examined whether small vessel disease (SVD) related white matter alterations in central brain network connections have a greater impact on executive functioning than alterations in non-central brain network connections. Brain networks were reconstructed from diffusion-weighted MRI scans in 72 individuals (75 ± 8 years) with cognitive impairment and SVD on MRI. The centrality of white matter connections in the network was defined using graph theory. The association between the fractional anisotropy (FA) of central versus non-central connections, executive functioning, and markers of SVD was evaluated with linear regression and mediation analysis. Lower FA in central network connections was more strongly associated with impairment in executive functioning than FA in non-central network connections (r = 0.41 vs. r = 0.27; P < 0.05). Results were consistent across varying thresholds to define the central subnetwork (>50%-10% connections). Higher SVD burden was associated with lower FA in central as well as non-central network connections. However, only central network FA mediated the relationship between white matter hyperintensity volume and executive functioning [change in regression coefficient after mediation (95% CI): -0.15 (-0.35 to -0.02)]. The mediation effect was not observed for FA alterations in non-central network connections [-0.03 (-0.19 to 0.04)]. These findings suggest that the centrality of network connections, and thus their contribution to global network efficiency, appears to be relevant for understanding the relationship between SVD and cognitive impairment. Hum Brain Mapp 37:2446-2454, 2016. © 2016 Wiley Periodicals, Inc.
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Encéfalo/diagnóstico por imagen , Enfermedades de los Pequeños Vasos Cerebrales/diagnóstico por imagen , Enfermedades de los Pequeños Vasos Cerebrales/psicología , Disfunción Cognitiva/diagnóstico por imagen , Anciano , Enfermedades de los Pequeños Vasos Cerebrales/complicaciones , Cognición , Disfunción Cognitiva/etiología , Imagen de Difusión por Resonancia Magnética , Imagen de Difusión Tensora , Función Ejecutiva , Femenino , Humanos , Procesamiento de Imagen Asistido por Computador , Modelos Lineales , Estudios Longitudinales , Masculino , Vías Nerviosas/diagnóstico por imagen , Tamaño de los Órganos , Sustancia Blanca/diagnóstico por imagenRESUMEN
Cognition involves coordinated activity across distributed neuronal networks. Neuronal activity during learning triggers cortical plasticity that allows for reorganization of the neuronal network and integration of new information. Animal studies have shown post-learning reactivation of learning-elicited neuronal network activity during subsequent sleep, supporting consolidation of the reorganization. However, no previous studies, to our knowledge, have demonstrated reactivation of specific learning-elicited long-range functional connectivity during sleep in humans. We here show reactivation of learning-induced long-range synchronization of magnetoencephalography power fluctuations in human sleep. Visuomotor learning elicited a specific profile of long-range cortico-cortical synchronization of slow (0.1 Hz) fluctuations in beta band (12-30 Hz) power. The parieto-occipital part of this synchronization profile reappeared in delta band (1-3.5 Hz) power fluctuations during subsequent sleep, but not during the intervening wakefulness period. Individual differences in the reactivated synchronization predicted postsleep performance improvement. The presleep resting-state synchronization profile was not reactivated during sleep. The findings demonstrate reactivation of long-range coordination of neuronal activity in humans, more specifically of reactivation of coupling of infra-slow fluctuations in oscillatory power. The spatiotemporal profile of delta power fluctuations during sleep may subserve memory consolidation by echoing coordinated activation elicited by prior learning.
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Mapeo Encefálico , Corteza Cerebral/fisiología , Sincronización Cortical/fisiología , Memoria/fisiología , Sueño/fisiología , Adulto , Electroencefalografía , Femenino , Lateralidad Funcional , Humanos , Aprendizaje , Magnetoencefalografía , Masculino , Movimiento/fisiología , Estimulación Luminosa , Estadística como Asunto , Adulto JovenRESUMEN
BACKGROUND AND AIM: The role of sleep in the enhancement of motor skills has been studied extensively in adults. We aimed to determine involvement of sleep and characteristics of spindles and slow waves in a motor skill in children. HYPOTHESIS: We hypothesized sleep-dependence of skill enhancement and an association of interindividual differences in skill and sleep characteristics. METHODS: 30 children (19 females, 10.7 ± 0.8 years of age; mean ± SD) performed finger sequence tapping tasks in a repeated-measures design spanning 4 days including 1 polysomnography (PSG) night. Initial and delayed performance were assessed over 12 h of wake; 12 h with sleep; and 24 h with wake and sleep. For the 12 h with sleep, children were assigned to one of three conditions: modulation of slow waves and spindles was attempted using acoustic perturbation, and compared to yoked and no-sound control conditions. ANALYSES: Mixed effect regression models evaluated the association of sleep, its macrostructure and spindles and slow wave parameters with initial and delayed speed and accuracy. RESULTS AND CONCLUSIONS: Children enhance their accuracy only over an interval with sleep. Unlike previously reported in adults, children enhance their speed independent of sleep, a capacity that may to be lost in adulthood. Individual differences in the dominant frequency of spindles and slow waves were predictive for performance: children performed better if they had less slow spindles, more fast spindles and faster slow waves. On the other hand, overnight enhancement of accuracy was most pronounced in children with more slow spindles and slower slow waves, i.e., the ones with an initial lower performance. Associations of spindle and slow wave characteristics with initial performance may confound interpretation of their involvement in overnight enhancement. Slower frequencies of characteristic sleep events may mark slower learning and immaturity of networks involved in motor skills.
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BACKGROUND: The restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connectivity characteristics in different brain regions, we performed a within-subject study of resting state brain activity using the graph theory framework adapted for the individual electrode level.In balanced order, we obtained high-density resting state electroencephalography (EEG) in 8 healthy participants, during a day following normal sleep and during a day following total sleep deprivation. We computed topographical maps of graph theoretical parameters describing local clustering and path length characteristics from functional connectivity matrices, based on synchronization likelihood, in five different frequency bands. A non-parametric permutation analysis with cluster correction for multiple comparisons was applied to assess significance of topographical changes in clustering coefficient and path length. RESULTS: Significant changes in graph theoretical parameters were only found on the scalp overlying the prefrontal cortex, where the clustering coefficient (local integration) decreased in the alpha frequency band and the path length (global integration) increased in the theta frequency band. These changes occurred regardless, and independent of, changes in power due to the sleep deprivation procedure. CONCLUSIONS: The findings indicate that sleep deprivation most strongly affects the functional connectivity of prefrontal cortical areas. The findings extend those of previous studies, which showed sleep deprivation to predominantly affect functions mediated by the prefrontal cortex, such as working memory. Together, these findings suggest that the restorative effect of sleep is especially relevant for the maintenance of functional connectivity of prefrontal brain regions.
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Encéfalo/fisiopatología , Privación de Sueño/fisiopatología , Ritmo alfa , Electroencefalografía , Femenino , Humanos , Masculino , Vías Nerviosas/fisiopatología , Corteza Prefrontal/fisiopatología , Descanso , Procesamiento de Señales Asistido por Computador , Ritmo Teta , Vigilia/fisiología , Adulto JovenRESUMEN
The cingulate cortex is regarded as the backbone of structural and functional connectivity of the brain. While its functional connectivity has been intensively studied, little is known about its effective connectivity, its modulation by behavioral states, and its involvement in cognitive performance. Given the previously reported effects on cingulate functional connectivity, we investigated how eye-closure and sleep deprivation changed cingulate effective connectivity, estimated from resting-state high-density electroencephalography (EEG) using a novel method to calculate Granger Causality directly in source space. Effective connectivity along the cingulate cortex was dominant in the forward direction. Eyes-open connectivity in the forward direction was greater compared to eyes-closed, in well-rested participants. The difference between eyes-open and eyes-closed connectivity was attenuated and no longer significant after sleep deprivation. Individual variability in the forward connectivity after sleep deprivation predicted subsequent task performance, such that those subjects who showed a greater increase in forward connectivity between the eyes-open and the eyes-closed periods also performed better on a sustained attention task. Effective connectivity in the opposite, backward, direction was not affected by whether the eyes were open or closed or by sleep deprivation. These findings indicate that the effective connectivity from posterior to anterior cingulate regions is enhanced when a well-rested subject has his eyes open compared to when they are closed. Sleep deprivation impairs this directed information flow, proportional to its deleterious effect on vigilance. Therefore, sleep may play a role in the maintenance of waking effective connectivity.
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Mapeo Encefálico , Giro del Cíngulo/fisiopatología , Red Nerviosa/fisiopatología , Vías Nerviosas/fisiopatología , Plasticidad Neuronal , Privación de Sueño/fisiopatología , Adulto , Nivel de Alerta , Electroencefalografía , Femenino , Humanos , MasculinoRESUMEN
Deep sleep is characterized by slow waves of electrical activity in the cerebral cortex. They represent alternating down states and up states of, respectively, hyperpolarization with accompanying neuronal silence and depolarization during which neuronal firing resumes. The up states give rise to faster oscillations, notably spindles and gamma activity which appear to be of major importance to the role of sleep in brain function and cognition. Unfortunately, while spindles are easily detectable, gamma oscillations are of very small amplitude. No previous sleep study has succeeded in demonstrating modulations of gamma power along the time course of slow waves in human scalp EEG. As a consequence, progress in our understanding of the functional role of gamma modulation during sleep has been limited to animal studies and exceptional human studies, notably those of intracranial recordings in epileptic patients. Because high synaptic density, which peaks some time before puberty depending on the brain region (Huttenlocher and Dabholkar, 1997), generates oscillations of larger amplitude, we considered that the best chance to demonstrate a modulation of gamma power by slow wave phase in regular scalp sleep EEG would be in school-aged children. Sleep EEG was recorded in 30 healthy children (aged 10.7 ± 0.8 years; mean ± s.d.). Time-frequency analysis was applied to evaluate the time course of spectral power along the development of a slow wave. Moreover, we attempted to modify sleep architecture and sleep characteristics through automated acoustic stimulation coupled to the occurrence of slow waves in one subset of the children. Gamma power increased on the rising slope and positive peak of the slow wave. Gamma and spindle activity is strongly suppressed during the negative peak. There were no differences between the groups who received and did not receive acoustic stimulation in the sleep parameters and slow wave-locked time-frequency analysis. Our findings show, for the first time in scalp EEG in humans, that gamma activity is associated with the up-going slope and peak of the slow wave. We propose that studies in children provide a uniquely feasible opportunity to conduct investigations into the role of gamma during sleep.
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Estimulación Acústica/métodos , Ondas Encefálicas/fisiología , Polisomnografía/métodos , Cuero Cabelludo/fisiología , Fases del Sueño/fisiología , Niño , Electroencefalografía/métodos , Femenino , Humanos , MasculinoRESUMEN
The characteristic oscillations of the sleeping brain, spindles and slow waves, show trait-like, within-subject stability and a remarkable interindividual variability that correlates with functionally relevant measures such as memory performance and intelligence. Yet, the mechanisms underlying these interindividual differences are largely unknown. Spindles and slow waves are affected by the recent history of learning and neuronal activation, indicating sensitivity to changes in synaptic strength and thus to the connectivity of the neuronal network. Because the structural backbone of this network is formed by white matter tracts, we hypothesized that individual differences in spindles and slow waves depend on the white matter microstructure across a distributed network. We recorded both diffusion-weighted magnetic resonance images and whole-night, high-density electroencephalography and investigated whether individual differences in sleep spindle and slow wave parameters were associated with diffusion tensor imaging metrics; white matter fractional anisotropy and axial diffusivity were quantified using tract-based spatial statistics. Individuals with higher spindle power had higher axial diffusivity in the forceps minor, the anterior corpus callosum, fascicles in the temporal lobe, and the tracts within and surrounding the thalamus. Individuals with a steeper rising slope of the slow wave had higher axial diffusivity in the temporal fascicle and frontally located white matter tracts (forceps minor, anterior corpus callosum). These results indicate that the profiles of sleep oscillations reflect not only the dynamics of the neuronal network at the synaptic level, but also the localized microstructural properties of its structural backbone, the white matter tracts.