Ultra-slow Oscillations Research Articles

Minute-scale oscillatory sequences in medial entorhinal cortex

The medial entorhinal cortex (MEC) hosts many of the brain’s circuit elements for spatial navigation and episodic memory, operations that require neural activity to be organized across long durations of experience1. Whereas location is known to be encoded by spatially tuned cell types in this brain region2,3, little is known about how the activity of entorhinal cells is tied together over time at behaviourally relevant time scales, in the second-to-minute regime. Here we show that MEC neuronal activity has the capacity to be organized into ultraslow oscillations, with periods ranging from tens of seconds to minutes. During these oscillations, the activity is further organized into periodic sequences. Oscillatory sequences manifested while mice ran at free pace on a rotating wheel in darkness, with no change in location or running direction and no scheduled rewards. The sequences involved nearly the entire cell population, and transcended epochs of immobility. Similar sequences were not observed in neighbouring parasubiculum or in visual cortex. Ultraslow oscillatory sequences in MEC may have the potential to couple neurons and circuits across extended time scales and serve as a template for new sequence formation during navigation and episodic memory formation.

Identifying the distinct spectral dynamics of laminar-specific interhemispheric connectivity with bilateral line-scanning fMRI

Despite extensive efforts to identify interhemispheric functional connectivity (FC) with resting-state (rs-) fMRI, correlated low-frequency rs-fMRI signal fluctuation across homotopic cortices originates from multiple sources. It remains challenging to differentiate circuit-specific FC from global regulation. Here, we developed a bilateral line-scanning fMRI method to detect laminar-specific rs-fMRI signals from homologous forepaw somatosensory cortices with high spatial and temporal resolution in rat brains. Based on spectral coherence analysis, two distinct bilateral fluctuation spectral features were identified: ultra-slow fluctuation (<0.04 Hz) across all cortical laminae versus Layer (L) 2/3-specific evoked BOLD at 0.05 Hz based on 4 s on/16 s off block design and resting-state fluctuations at 0.08–0.1 Hz. Based on the measurements of evoked BOLD signal at corpus callosum (CC), this L2/3-specific 0.05 Hz signal is likely associated with neuronal circuit-specific activity driven by the callosal projection, which dampened ultra-slow oscillation less than 0.04 Hz. Also, the rs-fMRI power variability clustering analysis showed that the appearance of L2/3-specific 0.08–0.1 Hz signal fluctuation is independent of the ultra-slow oscillation across different trials. Thus, distinct laminar-specific bilateral FC patterns at different frequency ranges can be identified by the bilateral line-scanning fMRI method.

Intrinsic macroscale oscillatory modes driving long range functional connectivity in female rat brains detected by ultrafast fMRI

Spontaneous fluctuations in functional magnetic resonance imaging (fMRI) signals correlate across distant brain areas, shaping functionally relevant intrinsic networks. However, the generative mechanism of fMRI signal correlations, and in particular the link with locally-detected ultra-slow oscillations, are not fully understood. To investigate this link, we record ultrafast ultrahigh field fMRI signals (9.4 Tesla, temporal resolution = 38 milliseconds) from female rats across three anesthesia conditions. Power at frequencies extending up to 0.3 Hz is detected consistently across rat brains and is modulated by anesthesia level. Principal component analysis reveals a repertoire of modes, in which transient oscillations organize with fixed phase relationships across distinct cortical and subcortical structures. Oscillatory modes are found to vary between conditions, resonating at faster frequencies under medetomidine sedation and reducing both in number, frequency, and duration with the addition of isoflurane. Peaking in power within clear anatomical boundaries, these oscillatory modes point to an emergent systemic property. This work provides additional insight into the origin of oscillations detected in fMRI and the organizing principles underpinning spontaneous long-range functional connectivity.

Multimodal Integration and Phenomenal Spatiotemporal Binding: A Perspective From the Default Space Theory.

How does the integrated and unified conscious experience arise from the vastly distributed activities of the nervous system? How is the information from the many cones of the retina bound with information coming from the cochlea to create the association of sounds with objects in visual space? In this perspective article, we assert a novel viewpoint on the “binding problem” in which we explain a metastable operation of the brain and body that may provide insight into this problem. In our view which is a component of the Default Space Theory (DST), consciousness arises from a metastable synchronization of local computations into a global coherence by a framework of widespread slow and ultraslow oscillations coordinated by the thalamus. We reinforce a notion shared by some consciousness researchers such as Revonsuo and the Fingelkurts that a spatiotemporal matrix is the foundation of phenomenological experience and that this phenomenology is directly tied to bioelectric operations of the nervous system. Through the oscillatory binding system we describe, cognitive neuroscientists may be able to more accurately correlate bioelectric activity of the brain and body with the phenomenology of human experience.

The role of neuron-glia interactions in the emergence of ultra-slow oscillations.

Ultra-slow cortical oscillatory activity of 1-100mHz has been recorded in human by electroencephalography and in dissociated cultures of cortical rat neurons, but the underlying mechanisms remain to be elucidated. This study presents a computational model of ultra-slow oscillatory activity based on the interaction between neurons and astrocytes. We predict that the frequency of these oscillations closely depends on activation of astrocytes in the network, which is reflected by oscillations of their intracellular calcium concentrations with periods between tens of seconds and minutes. An increase of intracellular calcium in astrocytes triggers the release of adenosine triphosphate from these cells which may alter transmission at nearby synapses by increasing or decreasing neurotransmitter release. These results provide theoretical support for the emerging awareness of astrocytes as active players in the regulation of neural activity and identify neuron-astrocyte interactions as a potential primary mechanism for the emergence of ultra-slow cortical oscillations.

Ultraslow Oscillation of Nematic Disclination after Abrupt Switching of DC Voltage

The slow damped oscillation of a nematic disclination was observed after an abrupt (stepwise) change in the DC electric field. The oscillation was not observed under a high-frequency AC field. These results imply that molecular reorientation influences disclination dynamics after abrupt switching. An effective model, which is not a simple elastic theory, was proposed to analyze the results.

Monochromatic Ultra-Slow (~ 0.1 Hz) Oscillations in the human electroencephalogram and their relation to hemodynamics

Previous studies demonstrated the presence of Monochromatic Ultra-Slow Oscillations (MUSO) in human EEG. In the present study we explored the biological origin of MUSO by simultaneous recordings of EEG, Near-Infrared Spectroscopy (NIRS), arterial blood pressure, respiration and Laser Doppler flowmetry. We used a head-up tilt test in order to check whether MUSO might relate to Mayer waves in arterial blood pressure, known to be enhanced by the tilting procedure. MUSO were detected in 8 out of 10 subjects during rest and showed a striking monochromatic spectrum (0.07–0.14Hz). The spatial topography of MUSO was complex, showing multiple foci variable across subjects. While the head-up tilt test increased the relative power of Mayer waves, it had no effect on MUSO. On the other hand, the relative spectral power of 0.1Hz oscillations in EEG, NIRS and blood pressure signals were positively correlated across subjects in the tilted condition. Eight subjects showed a coherence between MUSO and NIRS/arterial blood pressure. Moreover, MUSO at different electrode sites demonstrated coherence not reducible to volume conduction, thus indicating that MUSO are unlikely to be generated by one source. We related our experimental findings to known biological phenomena being generated at about 0.1Hz, i.e.: arterial blood pressure, cerebral and skin vasomotion, respiration and neuronal activity. While no definite conclusion can yet be drawn as to an exact physiological mechanism of MUSO, we suggest that these oscillations might be of a rather extraneuronal origin reflecting cerebral vasomotion.

Monochromatic ultra-slow oscillations in the human electroencephalogram

Introduction: Ultra-slow electroencephalographic oscillations (< 0.1 Hz) have been extensively investigated in humans and animals and were found to occur in a variety of conditions. Despite the ample evidence for their presence in the human brain, less is known about their biological mechanisms. Here, we report on the existence of monochromatic ultra-slow oscillations (MUSO) in the human scalp electroencephalogram (EEG).

Hierarchical clustering of brain activity during human nonrapid eye movement sleep

Consciousness is reduced during nonrapid eye movement (NREM) sleep due to changes in brain function that are still poorly understood. Here, we tested the hypothesis that impaired consciousness during NREM sleep is associated with an increased modularity of brain activity. Cerebral connectivity was quantified in resting-state functional magnetic resonance imaging times series acquired in 13 healthy volunteers during wakefulness and NREM sleep. The analysis revealed a modification of the hierarchical organization of large-scale networks into smaller independent modules during NREM sleep, independently from EEG markers of the slow oscillation. Such modifications in brain connectivity, possibly driven by sleep ultraslow oscillations, could hinder the brain's ability to integrate information and account for decreased consciousness during NREM sleep.

Ultra-slow oscillations in cortical networks in vitro

An ultra-slow oscillation (<0.01 Hz) in the network-wide activity of dissociated cortical networks is described in this article. This slow rhythm is characterized by the recurrence of clusters of large synchronized bursts of activity lasting approximately 1–3 min, separated by an almost equivalent interval of relatively smaller bursts. Such rhythmic activity was detected in cultures starting from the fourth week in vitro. Our analysis revealed that the propagation motifs of constituent bursts were strongly conserved across multiple oscillation cycles, and these motifs were more consistent at the electrode level compared with the neuronal level.

Simulation of Ultra-slow Oscillations Using the Integrate and Fire Neuron Model

The Integrate and Fire (IF) neuron model wasusedto simulate ultra-slow oscillations that were observed in cortical cultures. Simulation of a network with 2 sub-networks is conducted in this study. We introduced an additional equation that governs the generation and dissipation of an inhibitory property to each of the sub-network.Sub-networks that fire at different rate are generated from the simulation. The network activity from the simulation oscillates at frequencies that are comparable to ultra-slow oscillations observed in cortical cultures.

Broadband neurophysiological abnormalities in the medial prefrontal region of the default‐mode network in adults with ADHD

Previous investigations of the default-mode network (DMN) in persons with attention-deficit/hyperactivity disorder (ADHD) have shown reduced functional connectivity between the anterior and posterior aspects. This finding was originally demonstrated in adults with ADHD, then in youth with ADHD, and has been tentatively linked to ultra low frequency oscillations within the DMN. The current study evaluates the specificity of DMN abnormalities to neuronal oscillations in the ultra low frequency range, and examines the regional specificity of these DMN aberrations in medicated and unmedicated adults with, and those without ADHD. An individually matched sample of adults with and without ADHD completed 6-minute sessions of resting-state magnetoencephalography (MEG). Participants with ADHD were known responders to stimulant medications and completed two sessions (predrug/postdrug). MEG data were coregistered to the participant's MRI, corrected for head motion, fitted to a regional-level source model, and subjected to spectral analyses to extract neuronal population activity in regions of the DMN. The unmedicated adults with ADHD exhibited broadband deficits in medial prefrontal cortices (MPFC), but not other DMN regions compared to adults without ADHD. Unmedicated patients also showed abnormal cross-frequency coupling in the gamma range between the MPFC and posterior cingulate areas, and disturbed balance within the DMN as activity in posterior regions was stronger than frontal regions at beta and lower frequencies, which dissipated at higher γ-frequencies. Administration of pharmacotherapy significantly increased prefrontal alpha activity (8-14 Hz) in adults with ADHD, and decreased the cross-frequency gamma coupling. These results indicate that neurophysiological aberrations in the DMN of patients with ADHD are not limited to ultra slow oscillations, and that they may be primarily attributable to abnormal broadband activity in the MPFC.

Spectral power, phase-amplitude coupling and ultra-slow oscillations during rest in the human posteromedial cortex

Spectral power, phase-amplitude coupling and ultra-slow oscillations during rest in the human posteromedial cortex

Finding coherence in spontaneous oscillations

Spontaneous ultra-slow oscillations in brain signals are ubiquitous, although their source and function remain unknown. A new study now reports that this activity is correlated between functionally related areas across hemispheres in humans.

Corticofugal Modulation of the Tactile Response Coherence of Projecting Neurons in the Gracilis Nucleus

Precise and reproducible spike timing is one of the alternatives of the sensory stimulus encoding. We test coherence (repeatability) of the response patterns elicited in projecting gracile neurons by tactile stimulation and its modulation provoked by electrical stimulation of the corticofugal feedback from the somatosensory (SI) cortex. To gain the temporal structure we adopt the wavelet-based approach for quantification of the functional stimulus-neural response coupling. We show that the spontaneous firing patterns (when they exist) are essentially random. Tactile stimulation of the neuron receptive field strongly increases the spectral power in the stimulus and 5- to 15-Hz frequency bands. However, the functional coupling (coherence) between the sensory stimulus and the neural response exhibits ultraslow oscillation (0.07 Hz). During this oscillation the stimulus coherence can temporarily fall below the statistically significant level, i.e., the functional stimulus-response coupling may be temporarily lost for a single neuron. We further demonstrate that electrical stimulation of the SI cortex increases the stimulus coherence for about 60% of cells. We find no significant correlation between the increment of the firing rate and the stimulus coherence, but we show that there is a positive correlation with the amplitude of the peristimulus time histogram. The latter argues that the observed facilitation of the neural response by the corticofugal pathway, at least in part, may be mediated through an appropriate ordering of the stimulus-evoked firing pattern, and the coherence enhancement is more relevant in gracilis nucleus than an increase of the number of spikes elicited by the tactile stimulus.

Memory as the “whole brain work”: A large-scale model based on “oscillations in super-synergy”

According to recent trends, memory depends on several brain structures working in concert across many levels of neural organization; memory is a constant work—in progress.” The proposition of a brain theory based on super-synergy in neural populations is most pertinent for the understanding of this constant work in progress. This report introduces a new model on memory basing on the processes of EEG oscillations and Brain Dynamics. This model is shaped by the following conceptual and experimental steps: 1. The machineries of super-synergy in the whole brain are responsible for formation of sensory–cognitive percepts. 2. The expression “ dynamic memory” is used for memory processes that evoke relevant changes in alpha, gamma, theta and delta activities. The concerted action of distributed multiple oscillatory processes provides a major key for understanding of distributed memory. It comprehends also the phyletic memory and reflexes. 3. The evolving memory, which incorporates reciprocal actions or reverberations in the APLR alliance and during working memory processes, is especially emphasized. 4. A new model related to “ hierarchy of memories as a continuum” is introduced. 5. The notions of “ longer activated memory” and “ persistent memory” are proposed instead of long-term memory. 6. The new analysis to recognize faces emphasizes the importance of EEG oscillations in neurophysiology and Gestalt analysis. 7. The proposed basic framework called “ Memory in the Whole Brain Work” emphasizes that memory and all brain functions are inseparable and are acting as a “ whole” in the whole brain. 8. The role of genetic factors is fundamental in living system settings and oscillations and accordingly in memory, according to recent publications. 9. A link from the “ whole brain” to “ whole body,” and incorporation of vegetative and neurological system, is proposed, EEG oscillations and ultraslow oscillations being a control parameter.

Ultra-slow oscillation (0.025 Hz) triggers hippocampal afterdischarges in Wistar rats

Oscillations in neuronal networks are assumed to serve various physiological functions, from coordination of motor patterns to perceptual binding of sensory information. Here, we describe an ultra-slow oscillation (0.025 Hz) in the hippocampus. Extracellular and intracellular activity was recorded from the CA1 and subicular regions in rats of the Wistar and Sprague–Dawley strains, anesthetized with urethane. In a subgroup of Wistar rats (23%), spontaneous afterdischarges (4.7±1.6 s) occurred regularly at 40.8±15.7 s. The afterdischarge was initiated by a fast increase of population synchrony (100–250 Hz oscillation; “tonic” phase), followed by large-amplitude rhythmic waves and associated action potentials at gamma and beta frequency (15–50 Hz; “clonic” phase). The afterdischarges were bilaterally synchronous and terminated relatively abruptly without post-ictal depression. Single-pulse stimulation of the commissural input could trigger afterdischarges, but only at times when they were about to occur. Commissural stimulation evoked inhibitory postsynaptic potentials in pyramidal cells. However, when the stimulus triggered an afterdischarge, the inhibitory postsynaptic potential was absent and the cells remained depolarized during most of the afterdischarge. Afterdischarges were not observed in the Sprague–Dawley rats. Long-term analysis of interneuronal activity in intact, drug-free rats also revealed periodic excitability changes in the hippocampal network at 0.025 Hz. These findings indicate the presence of an ultra-slow oscillation in the hippocampal formation. The ultra-slow clock induced afterdischarges in susceptible animals. We hypothesize that a transient failure of GABAergic inhibition in a subset of Wistar rats is responsible for the emergence of epileptiform patterns.

Oscillatory electrographic activity in the hippocampus: A mathematical model

This model of hippocampal function describes the bilaterally symmetrical interactions of the various intrahippocampal populations of neurons that are functionally homogeneous (septal and entorhinal sources of input, granule cells, CA field pyramidal cells, and basket cells). Activity of each homogeneous population is described as a first order nonlinear differential equation. Parameters are simulated, with activity defined in relative units ranging from 0 to 1.0. The 26 equations (13 identified pools in each hemisphere) were solved simultaneously by computer to produce plots of the time course of activity changes in each of the populations. The simulations performed thus far show that the model parallels certain known properties of the system: (1) there is the expected reciprocal relationship between pyramidal cells and basket cells; (2) activity can be made to oscillate or achieve steady-state, simulating EEG “theta” rhythm or low voltage, fast activity; (3) oscillation occurs where it is known to occur (CA 1 pyramidal cells and the dentate region), where it is presumed to occur (in basket cells), and does not occur where it is known not to occur (CA 2 pyramidal cells); (4) there is a narrow range of frequency, and attempts to increase frequency readily terminate oscillation to cause steady-state activity: (5) oscillation requires excitatory drive from the medial septum, whereas entorhinal input is relatively less important: and (6) increases in medial septal activity can increase oscillation frequency. The results also predict certain undiscovered phenomena: (1) there is a major influence of variations in decay rate of activity in various neuronal pools; (2) there is probably an ultra-slow oscillation in the CA 2 area; and (3) the CA 1 projection to the entorhinal cortex seems to be important in modulating frequency and amplitude of theta rhythm.