Human amygdala activation during rapid eye movements of rapid eye movement sleep: an intracranial study.

The amygdaloid complex plays a crucial role in processing emotional signals and in the formation of emotional memories. Neuroimaging studies have shown human amygdala activation during rapid eye movement sleep (REM). Stereotactically implanted electrodes for presurgical evaluation in epileptic patients provide a unique opportunity to directly record amygdala activity. The present study analysed amygdala activity associated with REM sleep eye movements on the millisecond scale. We propose that phasic activation associated with rapid eye movements may provide the amygdala with endogenous excitation during REM sleep. Standard polysomnography and stereo-electroencephalograph (SEEG) were recorded simultaneously during spontaneous sleep in the left amygdala of four patients. Time-frequency analysis and absolute power of gamma activity were obtained for 250 ms time windows preceding and following eye movement onset in REM sleep, and in spontaneous waking eye movements in the dark. Absolute power of the 44-48 Hz band increased significantly during the 250 ms time window after REM sleep rapid eye movements onset, but not during waking eye movements. Transient activation of the amygdala provides physiological support for the proposed participation of the amygdala in emotional expression, in the emotional content of dreams and for the reactivation and consolidation of emotional memories during REM sleep, as well as for next-day emotional regulation, and its possible role in the bidirectional interaction between REM sleep and such sleep disorders as nightmares, anxiety and post-traumatic sleep disorder. These results provide unique, direct evidence of increased activation of the human amygdala time-locked to REM sleep rapid eye movements.

Stationary stable cross-correlation pattern and task specific deviations in unresponsive wakefulness syndrome as well as clinically healthy subjects.

Brain dynamics is highly non-stationary, permanently subject to ever-changing external conditions and continuously monitoring and adjusting internal control mechanisms. Finding stationary structures in this system, as has been done recently, is therefore of great importance for understanding fundamental dynamic trade relationships. Here we analyse electroencephalographic recordings (EEG) of 13 subjects with unresponsive wakefulness syndrome (UWS) during rest and while being influenced by different acoustic stimuli. We compare the results with a control group under the same experimental conditions and with clinically healthy subjects during overnight sleep. The main objective of this study is to investigate whether a stationary correlation pattern is also present in the UWS group, and if so, to what extent this structure resembles the one found in healthy subjects. Furthermore, we extract transient dynamical features via specific deviations from the stationary interrelation pattern. We find that (i) the UWS group is more heterogeneous than the two groups of healthy subjects, (ii) also the EEGs of the UWS group contain a stationary cross-correlation pattern, although it is less pronounced and shows less similarity to that found for healthy subjects and (iii) deviations from the stationary pattern are notably larger for the UWS than for the two groups of healthy subjects. The results suggest that the nervous system of subjects with UWS receive external stimuli but show an overreaching reaction to them, which may disturb opportune information processing.

Amygdala and hippocampus dialogue with neocortex during human sleep and wakefulness.

ABSTRACT: Previous studies have described synchronic electroencephalographic (EEG) patterns of the background activity that is characteristic of several vigilance states. STUDY OBJECTIVES: To explore whether the background synchronous activity of the amygdala-hippocampal-neocortical circuit is modified during sleep in the delta, theta, alpha, sigma, beta, and gamma bands characteristic of each sleep state. METHODS: By simultaneously recording intracranial and noninvasive scalp EEG (10-20 system) in epileptic patients who were candidates for neurosurgery, we explored synchronous activity among the amygdala, hippocampus, and neocortex during wakefulness (W), Non-Rapid Eye Movement (NREM), and Rapid-Eye Movement (REM) sleep. RESULTS: Our findings reveal that hippocampal-cortical synchrony in the sleep spindle frequencies was spread across the cortex and was higher during NREM versus W and REM, whereas the amygdala showed punctual higher synchronization with the temporal lobe. Contrary to expectations, delta synchrony between the amygdala and frontal lobe and between the hippocampus and temporal lobe was higher during REM than NREM. Gamma and alpha showed higher synchrony between limbic structures and the neocortex during wakefulness versus sleep, while synchrony among deep structures showed a mixed pattern. On the one hand, amygdala-hippocampal synchrony resembled cortical activity (i.e. higher gamma and alpha synchrony in W); on the other, it showed its own pattern in slow frequency oscillations. CONCLUSIONS: This is the first study to depict diverse patterns of synchronic interaction among the frequency bands during distinct vigilance states in a broad human brain circuit with direct anatomical and functional connections that play a crucial role in emotional processes and memory.

Simultaneous and independent electroencephalography and magnetic resonance imaging: A multimodal neuroimaging dataset.

We introduce an open access, multimodal neuroimaging dataset comprising simultaneously and independently collected Electroencephalography (EEG) and Magnetic Resonance Imaging (MRI) data from twenty healthy, young male individuals (mean age = 26 years; SD = 3.8 years). The dataset adheres to the BIDS standard specification and is structured into two components: 1) EEG data recorded outside the Magnetic Resonance (MR) environment, inside the MR scanner without image collection and during simultaneous functional MRI acquisition (EEG-fMRI) and 2) Functional MRI data acquired with and without simultaneous EEG recording and structural MRI data obtained with and without the participants wearing the EEG cap. EEG data were recorded with an MR-compatible EEG recording system (GES 400 MR, Electrical Geodesics Inc.) using a 32-channel sponge-based EEG cap (Geodesic Sensor Net). Eyes-closed resting-state EEG data were recorded for two minutes in both the outside and inside scanner conditions and for ten minutes during simultaneous EEG-fMRI. Eyes-open resting-state EEG data were recorded for two minutes under each condition. Participants also performed an eyes opening-eyes closure block-design task outside the scanner (two minutes) and during simultaneous EEG-fMRI (four minutes). The EEG data recorded outside the scanner provides a reference signal devoid of MR-related artifacts. The data collected inside the scanner without image acquisition captures the contribution of the ballistocardiographic (BCG) without the gradient artifact, making it suitable for testing and validating BCG artifact correction methods. The EEG-fMRI data is affected by both the gradient and BCG artifacts. Brain images were acquired using a 3T GE MR750-Discovery MR scanner equipped with a 32-channel head coil. Whole-brain functional images were obtained using a GRE-EPI T2* weighted sequence (TR = 2000 ms, TE = 40 ms, 35 interleaved axial slices with 4 mm isometric voxels). Structural images were acquired using an SPGR sequence (TR = 8.1 ms, TE = 3.2 ms, flip angle = 12°, 176 sagittal slices with 1 mm isometric voxels). This stands as one of the largest open access EEG-fMRI datasets available, which allows researchers to: 1) Assess the impact of gradient and BCG artifacts on EEG data, 2) Evaluate the effectiveness of novel artifact removal techniques to minimize artifact contribution and preserve EEG signal integrity, 3) Conduct hardware/setup comparison studies, 4) Evaluate the quality of structural and functional MRI data obtained with this particular EEG system, and 5) Implement and validate multimodal integrative analysis approaches on simultaneous EEG-fMRI data.

Preservation of EEG spectral power features during simultaneous EEG-fMRI.

Introduction: Electroencephalographic (EEG) data quality is severely compromised when recorded inside the magnetic resonance (MR) environment. Here we characterized the impact of the ballistocardiographic (BCG) artifact on resting-state EEG spectral properties and compared the effectiveness of seven common BCG correction methods to preserve EEG spectral features. We also assessed if these methods retained posterior alpha power reactivity to an eyes closure-opening (EC-EO) task and compared the results from EEG-informed fMRI analysis using different BCG correction approaches. Method: Electroencephalographic data from 20 healthy young adults were recorded outside the MR environment and during simultaneous fMRI acquisition. The gradient artifact was effectively removed from EEG-fMRI acquisitions using Average Artifact Subtraction (AAS). The BCG artifact was corrected with seven methods: AAS, Optimal Basis Set (OBS), Independent Component Analysis (ICA), OBS followed by ICA, AAS followed by ICA, PROJIC-AAS and PROJIC-OBS. EEG signal preservation was assessed by comparing the spectral power of traditional frequency bands from the corrected rs-EEG-fMRI data with the data recorded outside the scanner. We then assessed the preservation of posterior alpha functional reactivity by computing the ratio between the EC and EO conditions during the EC-EO task. EEG-informed fMRI analysis of the EC-EO task was performed using alpha power-derived BOLD signal predictors obtained from the EEG signals corrected with different methods. Results: The BCG artifact caused significant distortions (increased absolute power, altered relative power) across all frequency bands. Artifact residuals/signal losses were present after applying all correction methods. The EEG reactivity to the EC-EO task was better preserved with ICA-based correction approaches, particularly when using ICA feature extraction to isolate alpha power fluctuations, which allowed to accurately predict hemodynamic signal fluctuations during the EEG-informed fMRI analysis. Discussion: Current software solutions for the BCG artifact problem offer limited efficiency to preserve the EEG spectral power properties using this particular EEG setup. The state-of-the-art approaches tested here can be further refined and should be combined with hardware implementations to better preserve EEG signal properties during simultaneous EEG-fMRI. Existing and novel BCG artifact correction methods should be validated by evaluating signal preservation of both ERPs and spontaneous EEG spectral power.

How to orchestrate a soccer team: Generalized synchronization promoted by rhythmic acoustic stimuli.

Interpersonal coordination requires precise actions concerted in space and time in a self-organized manner. We found, using soccer teams as a testing ground, that a common timeframe provided by adequate acoustic stimuli improves the interplay between teammates. We provide quantitative evidence that the connectivity between teammates and the scoring rate of male soccer teams improve significantly when playing under the influence of an appropriate acoustic environment. Unexpectedly, female teams do not show any improvement under the same experimental conditions. We show by follow-up experiments that the acoustic rhythm modulates the attention level of the participants with a pronounced tempo preference and a marked gender difference in the preferred tempo. These results lead to a consistent explanation in terms of the dynamical system theory, nonlinear resonances, and dynamic attention theory, which may illuminate generic mechanisms of the brain dynamics and may have an impact on the design of novel training strategies in team sports.

Facial muscle activation during sleep and its relation to the rapid eye movements of REM sleep.

Facial muscle contractions (FMC) are a commonly observed feature during sleep stages in human subjects. Previous studies have associated FMC to emotional expression during waking. Phasic features of rapid eye movement (REM) sleep, such as REMs have also been linked to an increase in limbic structure activity with a subsequent relation to emotional dream content. We hypothesized that FMC would be more frequent during REM sleep, and that FMC would correlate with the characteristic REMs of this sleep stage. The present study was designed to evaluate the density per minute of the phasic and sustained FMC of five facial muscles (frontalis, corrugator, orbicularis oculi, zygomatic major left and right) during all sleep stages, and to explore their relation with REMs density in six healthy participants during an 8 h sleep recording. Results showed a significant increase in FMC of all recorded muscles during REM sleep, both in frequency and duration. Additionally, as expected, during REM sleep there was a positive correlation among the facial muscles and between these and REMs. Nevertheless, although associated in number, both features (FMC and REMs) were never simultaneous. Our results suggest that limbic activation during REM sleep may be responsible for the enhancement of facial muscle activity, which may be consistent with the theoretical perspective of a higher emotional activity during REM sleep.

León Cintra's contribution to the field of protein malnutrition effects on sleep and the brain.

On June 19 2009, everyone who knew Leon Cintra was shocked by the terrible news of the automobile accident that took his life. The feeling within the scientific community was that his passing was not only a great loss for Mexican science but also the loss of a beloved friend. He will be missed and forever remembered for his brilliant mind and noble heart. His scientific career was focused, since the beginning, on the study of protein malnutrition effects on brain morphometry, somato-sensory transmission, sleep, circadian rhythms and behavior. His findings showed that malnutrition has long lasting adverse effects on morphometry of systems involved in sleep regulation such as locus coeruleus, nucleus raphe dorsalis and susprachiasmatic nucleus, and on hippocampal circuit implicated in theta activity generation. His results on spectral analysis of electrical field potential at every 4 sec from 24-h baseline recording and 72-h of recovery sleep after total sleep deprivation or selective REM sleep deprivation demonstrated that protein malnutrition induced alterations on homeostatic as well as on circadian sleep regulation; brain oscillations and theta coherent activity between left and right hemisphere and between hippocampus and cerebral cortex are also affected by malnutrition.

[Sleep medicine: development, contributions and perspectives. Report of the work group on sleep medicine]. / Medicina del dormir: desarrollo, contribuciones y perspectivas. Reporte del grupo de trabajo en medicina del dormir.

Sleep is a basic biological process that has an impact on all the functions of the body, and interacts bidirectionally with virtually all of the body systems, so that the sleep disorders are associated with disturbances in other systems, either respiratory, neurological, cardiovascular, endocrine, immune, etc., and vice versa. The complexity of the regulatory mechanisms of sleep and the variety of their disorders, together with the clinical evidence accumulated in recent decades, have led to the birth of a new branch in medicine: the Sleep Medicine, with well defined intrinsic disorders. The consequences of sleep deprivation or fragmentation induced by changes in social and work dynamics, as well as sleep disorders have harmful effects on individuals in the short and long-term, the most important are an elevated risk for vehicular and occupational accidents, cardiovascular damage, cognitive impairment, obesity, diabetes mellitus, among others, impacting individuals of all ages. The sleep clinics and laboratories in Mexico, have made significant contributions, at both the basic and clinical levels, for the diagnosis and treatment of sleep disorders; however, without a specific health policy, we will continue to commit resources only on the attention of its effects and not on prevention, making the impact on the economy and quality of life of patients with sleep disorders, much higher than in developed countries. It is necessary to build a program of medical care to incorporate the Sleep Medicine in the priorities of medical care in the National Institutions of Health at all levels. Solutions and guides to optimize the achievement of the proposed results, and increase efficiency and effectiveness of the resources applied in this new field of Medicine are offered.

Week-by-week changes in sleep EEG in healthy full-term newborns.

Spectral analysis of neonatal sleep is useful for studying brain maturation; however, most studies have analyzed conventional broad bands described for awake adults, so a distinct approach for EEG analysis may disclose new findings. STUDY OBJECTIVES: To extract independent EEG broad bands using principal component analysis (PCA) and describe week-by-week EEG changes in quiet sleep (QS) and active sleep (AS) during the first 5 weeks of postnatal life in healthy, full-term newborns. METHODS: Polysomnography of spontaneous sleep was recorded in 60 newborns in 5 groups at 41, 42, 43, 44, and 45 weeks (n = 12 each) postconceptional age (POST-C). QS and AS stages were identified. Absolute power (AP) for 1 Hz bins between 1 and 30 Hz was subjected to PCA to extract independent broad bands. RESULTS: PCA rendered three independent broad bands distinct from conventional bands. They explained 82.8% of variance: 2-10 Hz, 10-16 Hz, and 17-30 Hz. ANOVAs (group × age × derivations) showed significant higher power at 2-10 Hz with greater age, higher power in QS than AS in all three bands, and significantly higher AP in the left central region, and in the right occipital and temporal areas, in both sleep stages. CONCLUSION: A different method of analyzing sleep EEG generated new information on brain maturation. The Sigma frequencies identified suggest that sleep spindle maturation begins by at least 41 weeks of POST-C age. Interhemispheric asymmetries during sleep suggest earlier development of the central left region and the right occipital and temporal areas.

Differential alpha coherence hemispheric patterns in men and women during pleasant and unpleasant musical emotions.

Potential sex differences in EEG coherent activity during pleasant and unpleasant musical emotions were investigated. Musical excerpts by Mahler, Bach, and Prodromidès were played to seven men and seven women and their subjective emotions were evaluated in relation to alpha band intracortical coherence. Different brain links in specific frequencies were associated to pleasant and unpleasant emotions. Pleasant emotions (Mahler, Bach) increased upper alpha couplings linking left anterior and posterior regions. Unpleasant emotions (Prodromidès) were sustained by posterior midline coherence exclusively in the right hemisphere in men and bilateral in women. Combined music induced bilateral oscillations among posterior sensory and predominantly left association areas in women. Consistent with their greater positive attributions to music, the coherent network is larger in women, both for musical emotion and for unspecific musical effects. Musical emotion entails specific coupling among cortical regions and involves coherent upper alpha activity between posterior association areas and frontal regions probably mediating emotional and perceptual integration. Linked regions by combined music suggest more working memory contribution in women and attention in men.

How to Obtain Reliable Visual Event-related Potentials in Newborns.

The present study discusses the characteristics of visual event-related potentials (VEPs) and outlines methodological steps for obtaining reliable measurements in newborns. Obtaining high-quality, reliable VEPs is crucial for the early detection of abnormal development of the central nervous system in at-risk newborns, and for implementing successful early interventions. Recommendations are based on a previous study which showed that when post-conceptional age, polysomnography-identified sleep stages, and light-emitting diodes (LEDs) googles as the luminous source are controlled, no more than 4 repetitions of VEP averages are required to obtain replicable recordings, variability decreases, and reliable VEPs can be obtained. By controlling for these sources of variability and using statistical analyses, we were able to clearly and reliably identify the amplitude and latency of three main components (NII, PII and NIII) present in 100% of newborns (n = 20) during active sleep. Recording VEPs during awake states, quiet sleep and transitional sleep is not recommended because VEP morphology may differ significantly from one average to the next, leading to the risk of misleading clinical prognoses. Moreover, it is easier to obtain VEPs during active sleep because this state can be clearly and reliably identified at this stage of development, sleep cycles are short enough to allow measurements to be taken in a reasonable time, and the method does not require new o expensive equipment.

The Influence of EEG References on the Analysis of Spatio-Temporal Interrelation Patterns.

The characterization of the functional network of the brain dynamics has become a prominent tool to illuminate novel aspects of brain functioning. Due to its excellent time resolution, such research is oftentimes based on electroencephalographic recordings (EEG). However, a particular EEG-reference might cause crucial distortions of the spatiotemporal interrelation pattern and may induce spurious correlations as well as diminish genuine interrelations originally present in the dataset. Here we investigate in which manner correlation patterns are affected by a chosen EEG reference. To this end we evaluate the influence of 7 popular reference schemes on artificial recordings derived from well controlled numerical test frameworks. In this respect we are not only interested in the deformation of spatial interrelations, but we test additionally in which way the time evolution of the functional network, estimated via some bi-variate interrelation measures, gets distorted. It turns out that the median reference as well as the global average show the best performance in most situations considered in the present study. However, if a collective brain dynamics is present, where most of the signals get correlated, these schemes may also cause crucial deformations of the functional network, such that the parallel use of different reference schemes seems advisable.

Brain activity and temporal coupling related to eye movements during REM sleep: EEG and MEG results.

EEG and MEG REM sleep gamma activity was studied immediately before rapid eye movement onset (PRE-EM), during REM sleep with eye movements away from eye movement onset -phasic-REM (Ph-REM)--and during REM sleep without eye movements, or tonic REM (T-REM). For this purpose, activity was segmented into three different time windows: of 62.5, 250 and 500 ms. Two strategies were used: one a statistical comparison of changes between T-REM, Ph-REM and PRE-EM; the other a descriptive approach using principal component analysis. Significant findings showed that both EEG and MEG gamma activity are higher directly before eye movement onset in PRE-EM periods and during Ph-REM than during T-REM; temporal coupling of electrical activity between the frontal and parietal regions is decreased, while temporal coupling between the right frontal and midline is increased. Just before eye movement onset, larger recording sites become related. For the first time, results showed a close temporal link between power and temporal coupling of fast oscillations andrapid eye movements in REM sleep, indicating increased activation, uncoupling between the left frontal executive areas and posterior sensory association regions and increased coupling between the right frontal attentional and midline alerting systems. Brain activity is reorganized by phasic events.

Patterns of covariant power and coherent EEG activity during rest in young adults.

Functional cortical organization is not dependent on cognition only, but also reflects basic intrinsic individual characteristics stable over time and across physiological conditions that suggest the existence of self-organization patterns operating even during rest. The aim of the present study was to investigate the pattern of functional organization of EEG broad bands and coherent activity during rest by means of Principal Component Analysis (PCA) with closed and open eyes of 28 men and women. PCA revealed patterns of covariant oscillatory activity and functionally related regions with covariant coherent activity present during resting conditions, different for open and closed eyes. Different patterns of covariant oscillations within alpha frequencies were identified consistent with current notions on overlapping frequencies with different origin and behavioral context. Covariant coherent cortical networks were revealed congruent with functional systems described during cognitive processes; one, linking regions involved in visuo-motor coordination, another in language, and a third one in visuo-spatial processes suggesting that strong functional links are present during rest.

Visual evoked potentials are similar in polysomnographically defined quiet and active sleep in healthy newborns.

Morphology and late components of evoked potentials change depending on wake-sleep stages in adults. Visual Evoked potentials (VEPs) have been frequently studied in newborns to identify abnormal development of visual pathways; however, large variability has been reported and there is uncertainty as to the effect of sleep stages on VEPs in neonates. OBJECTIVE: To describe the characteristics of VEPs in one month old, healthy full-term newborns during active sleep (AS) and quiet sleep (QS), defined by simultaneous polysomnography (PSG). METHODS: VEPs were obtained by monocular LEDs stimulation of each eye during AS and QS, in 20 healthy full-term newborns (gestational age 37-40 weeks) with normal birth weights and normal prenatal Doppler ultrasound indices. Latencies and amplitudes of N2, P2 and N3 components in AS and QS were compared, and their association with absolute power of EEG frequency bands, assessed. RESULTS: There were no significant differences in VEP morphology, latencies and amplitudes between sleep states. Typical wave forms were obtained in all newborns in AS; however, no VEPs could be identified clearly in 3 newborns in QS; QS VEPs were less reliable than in AS: more averaging was required; correlation was significantly lower between the VEP averages; and a larger number of babies needed more than two averages to obtain replicable responses needed for clinical purposes. CONCLUSIONS: These results indicate that changes in amplitude and latency of some VEP components observed in NREM and REM sleep in adults are not yet present in one month old newborns probably due to immaturity of cortical and sleep mechanisms. VEPs are more reliable during AS than QS in newborns. Systematic VEP recording during AS, and polysomnographic control to identify this stage, are highly recommended as methods that can increase there liability of neonatal VEPs.

Electrical activity of the human amygdala during all-night sleep and wakefulness.

OBJECTIVE: The aim of the present work was to characterize the dynamics of the human amygdala across the different sleep stages and during wakefulness. METHODS: Simultaneous intracranial electrical recordings of the amygdala, hippocampus, and scalp electroencephalography during spontaneous sleep polysomnography in four patients suffering from epilepsy were analyzed. RESULTS: Power spectrum of the amygdala revealed no differences between rapid eye movement (REM) and wakefulness for all frequencies except higher power at 9 Hz during wakefulness and some low Gamma frequencies. Conversely, higher power was observed in non-REM (NREM) sleep than wakefulness for Delta, Theta and Sigma. CONCLUSIONS: Our results showed similar activity in the amygdala between wakefulness and REM sleep suggesting that the amygdala is as active in REM as during wakefulness. The higher power in Sigma frequencies during NREM sleep suggests that amygdala slow activity may play a significant role during NREM in concurrence with hippocampal activity. SIGNIFICANCE: While studies have described the metabolic activity of the human amygdala during sleep, our results show the corresponding electrical pattern during the whole night, pointing out an increase of slow activity during NREM sleep that might be subjected to similar influences as other subcortical brain structures, such as the hippocampus.

Characteristic Fluctuations Around Stable Attractor Dynamics Extracted from Highly Nonstationary Electroencephalographic Recordings.

Since the discovery of electrical activity of the brain, electroencephalographic (EEG) recordings constitute one of the most popular techniques of brain research. However, EEG signals are highly nonstationary and one should expect that averages of the cross-correlation coefficient, which may take positive and negative values with equal probability, (almost) vanish when estimated over long data segments. Instead, we found that the average zero-lag cross-correlation matrix estimated with a running window over the whole night of sleep EEGs, or of resting state during eyes-open and eyes-closed conditions of healthy subjects shows a characteristic correlation pattern containing pronounced nonzero values. A similar correlation structure has already been encountered in scalp EEG signals containing focal onset seizures. Therefore, we conclude that this structure is independent of the physiological state. Because of its pronounced similarity across subjects, we believe that it depicts a generic feature of the brain dynamics. Namely, we interpret this pattern as a manifestation of a dynamical ground state of the brain activity, necessary to preserve an efficient operational mode, or, expressed in terms of dynamical system theory, we interpret it as a "shadow" of the evolution on (or close to) an attractor in phase space. Nonstationary dynamical aspects of higher cerebral processes should manifest in deviations from this stable pattern. We confirm this hypothesis through a correlation analysis of EEG recordings of 10 healthy subjects during night sleep, 20 recordings of 9 epilepsy patients, and 42 recordings of 21 healthy subjects in resting state during eyes-open and eyes-closed conditions. In particular, we show that the estimation of deviations from the stationary correlation structures provides a more significant differentiation of physiological states and more homogeneous results across subjects.