Coherent Oscillatory Activity Research Articles

Active Sleep Promotes Coherent Oscillatory Activity in the Cortico-Hippocampal System of Infant Rats.

Active sleep (AS) provides a unique developmental context for synchronizing neural activity within and between cortical and subcortical structures. In week-old rats, sensory feedback from myoclonic twitches, the phasic motor activity that characterizes AS, promotes coherent theta oscillations (4-8Hz) in the hippocampus and red nucleus, a midbrain motor structure. Sensory feedback from twitches also triggers rhythmic activity in sensorimotor cortex in the form of spindle bursts, which are brief oscillatory events composed of rhythmic components in the theta, alpha/beta (8-20Hz), and beta2 (20-30Hz) bands. Here we ask whether one or more of these spindle-burst components are communicated from sensorimotor cortex to hippocampus. By recording simultaneously from whisker barrel cortex and dorsal hippocampus in 8-day-old rats, we show that AS, but not other behavioral states, promotes cortico-hippocampal coherence specifically in the beta2 band. By cutting the infraorbital nerve to prevent the conveyance of sensory feedback from whisker twitches, cortical-hippocampal beta2 coherence during AS was substantially reduced. These results demonstrate the necessity of sensory input, particularly during AS, for coordinating rhythmic activity between these two developing forebrain structures.

Functional Connectome from Phase Synchrony at Resting State is a Neural Fingerprint.

Coherent oscillatory activity across brain regions provides a variety of individual-specific characteristics, sometimes referred to as a neural fingerprint. This information, however, may not be directly retrieved from raw functional magnetic resonance imaging (fMRI) time series. In this study, we examined the data of 205 participants who completed two resting-state fMRI scanning sessions, separated by an average of 2.63 years. In the first step, we tested the long-term reliability of functional connectomes derived from amplitude-based functional connectivity (the conventional method) and found that they remained accurate markers (>85%, p < 0.001, permutation test) for identifying individuals, even after a period longer than 800 days. Using the same data set, we further expanded our exploration of the extent to which two analytic components of oscillatory activity (amplitude envelope and instantaneous phase) may function as reliable fingerprints. Both analytic signals-in particular, the instantaneous phase-were identified as useful indices in shaping functional connectivity fingerprints (86%, p < 0.001, permutation test). Connectivity profiles derived from the ventral attention, frontoparietal, and default mode networks were the largest contributing factors to identification. The current results suggest that neural synchronization tapped by analytical signal from a low-frequency resting-state fMRI blood oxygen level-dependent oscillation could be a reliable and useful fingerprint for identifying individuals and might provide an alternative method for characterizing dynamic functional connectivity profiles.

Network-based brain stimulation selectively impairs spatial retrieval

BackgroundDirect brain stimulation via electrodes implanted for intracranial electroencephalography (iEEG) permits the modulation of endogenous electrical signals with significantly greater spatial and temporal specificity than non-invasive approaches. It also allows for the stimulation of deep brain structures important to memory, such as the hippocampus, that are difficult, if not impossible, to target non-invasively. Direct stimulation studies of these deep memory structures, though, have produced mixed results, with some reporting improvement, some impairment, and others, no consistent changes. Objective/hypothesisWe hypothesize that to modulate cognitive function using brain stimulation, it is essential to modulate connected nodes comprising a network, rather than just alter local activity. MethodsiEEG data collected while patients performed a spatiotemporal memory retrieval task were used to map frequency-specific, coherent oscillatory activity between different brain regions associated with successful memory retrieval. We used these to identify two target nodes that exhibited selectively stronger coupling for spatial vs. temporal retrieval. In a subsequent session, electrical stimulation - theta-bursts with a fixed phase-lag (0° or 180°) – was applied to the two target regions while patients performed spatiotemporal retrieval. ResultsStimulation selectively impaired spatial retrieval while not affecting temporal retrieval, and this selective impairment was associated with theta decoupling of the spatial retrieval network. ConclusionThese findings suggest that stimulating tightly connected nodes in a functional network at the appropriate phase-lag may effectively modulate the network function, and while in this case it impaired memory processes, it sets a foundation for further network-based perturbation studies.

Induced cortical oscillations in turtle cortex are coherent at the mesoscale of population activity, but not at the microscale of the membrane potential of neurons.

Bursts of oscillatory neural activity have been hypothesized to be a core mechanism by which remote brain regions can communicate. Such a hypothesis raises the question to what extent oscillations are coherent across spatially distant neural populations. To address this question, we obtained local field potential (LFP) and membrane potential recordings from the visual cortex of turtle in response to visual stimulation of the retina. The time-frequency analysis of these recordings revealed pronounced bursts of oscillatory neural activity and a large trial-to-trial variability in the spectral and temporal properties of the observed oscillations. First, local bursts of oscillations varied from trial to trial in both burst duration and peak frequency. Second, oscillations of a given recording site were not autocoherent; i.e., the phase did not progress linearly in time. Third, LFP oscillations at spatially separate locations within the visual cortex were more phase coherent in the presence of visual stimulation than during ongoing activity. In contrast, the membrane potential oscillations from pairs of simultaneously recorded pyramidal neurons showed smaller phase coherence, which did not change when switching from black screen to visual stimulation. In conclusion, neuronal oscillations at distant locations in visual cortex are coherent at the mesoscale of population activity, but coherence is largely absent at the microscale of the membrane potential of neurons.NEW & NOTEWORTHY Coherent oscillatory neural activity has long been hypothesized as a potential mechanism for communication across locations in the brain. In this study we confirm the existence of coherent oscillations at the mesoscale of integrated cortical population activity. However, at the microscopic level of neurons, we find no evidence for coherence among oscillatory membrane potential fluctuations. These results raise questions about the applicability of the communication through coherence hypothesis to the level of the membrane potential.

Predictive coding in visual search as revealed by cross-frequency EEG phase synchronization.

Our experience, memories, and knowledge have modulatory influence on how we perceive the world. Top-down expectancies are supposed to be implemented as templates in our minds. Mental templates are compared against the current sensory input, which can match or mismatch with the aim of minimizing prediction error (Friston, 2005). But what are the underlying neuronal mechanisms leading to the activation of mental templates and their comparison with sensory input, i.e., predictive coding? Biasing sensory processing by expectancies has been strongly associated with prefrontal brain activity influencing responses in visual cortex (e.g., Summerfield et al., 2006; Olivers et al., 2011; Spaak et al., 2015). Moreover, electrophysiological evidence gathered in patients with prefrontal cortex lesions (Yago et al., 2004) suggests that the prefrontal cortex acts with excitatory drive on extrastriate cortex within three time windows during template matching in visual attention tasks: as early as 100 ms after target onset through selection of spatial locations; during the analysis of non-spatial features of attended objects around 250 ms after target onset; and in a later phase around 300 ms during which discrimination and template matching occur. This recurrent prefrontal drive on higher visual areas can be interpreted as top-down reactivation of target memory traces, thus, the activation of a mental template that needs to be compared to visual input (Desimone and Duncan, 1995). A common way of analysing interregional transfer of neural signals in the human brain is by means of coherent oscillatory brain activity. Rhythmical brain activity as recorded with the electroencephalogram (EEG) is an indicator for locally highly synchronized neuronal activity. If two distant brain areas are functionally coupled, it is assumed that a higher level of coherent, synchronous neuronal activity can be found between these distant areas than one would expect from chance. Comprehensive work by von Stein and co-workers suggests that long-range interaction between prefrontal and posterior cortices necessary in top-down control of cognitive processes is reflected by neural activity resonating in large-scale networks and therefore oscillating at rather slow frequencies: so called theta and alpha oscillations (von Stein et al., 1999, 2000; von Stein and Sarnthein, 2000). In humans, coherent, synchronous prefrontal to parietal brain oscillatory activity particularly in slower frequency bands (around 5 and 10 Hz) has been observed when a high level of top-down activity is necessary in a range of different visual tasks (see Sauseng and Klimesch, 2008; Sauseng et al., 2010 for reviews). Long-range communication in the monkey brain has also been attributed to rather slow oscillatory activity (in the theta and delta frequency range) whereas it has been suggested that local, fast rhythmical cortical activity (in the gamma frequency band) is associated more strongly with bottom-up visual processing (Bruns and Eckhorn, 2004; Eckhorn et al., 2004; Bastos et al., 2015; Zheng and Colgin, 2015).

Fast network oscillations in the hippocampus

Abstract Neuronal networks often express coherent oscillatory activity. These rhythms can pro­vide a temporal reference for the activity of single neurons and allow the formation of spatiotemporal activity patterns with a de­fined phase relationship of action potentials. In a single brain nucleus, oscillations at dif­ferent frequencies might be simultaneous­ly generated, but isolated rhythms might also be characteristic for specific functional brain states. During the last two decades the mam­malian hippocampus has become an impor­tant model system for the study of neuronal network oscillations. In this brain area, cel­lular mechanisms underlying neuronal syn­chronization have been described, but also models were developed to explain the con­tribution of oscillations in encoding, con­solidation, and recall of memories. Neuro­nal rhythmic activities provide an impor­tant field of analysis bringing together cel­lular mechanisms and systemic functions of the brain. Here, we use a particularly fast type of neuronal oscillation, hippocampal “rip­ples”, as an example to outline current knowl­edge and open questions related with this re­search field.

Neuromagnetic Indicators of Tinnitus and Tinnitus Masking in Patients with and without Hearing Loss

Tinnitus is an auditory phenomenon characterised by the perception of a sound in the absence of an external auditory stimulus. Chronic subjective tinnitus is almost certainly maintained via central mechanisms, and this is consistent with observed measures of altered spontaneous brain activity. A number of putative central auditory mechanisms for tinnitus have been proposed. The influential thalamocortical dysrhythmia model suggests that tinnitus can be attributed to the disruption of coherent oscillatory activity between thalamus and cortex following hearing loss. However, the extent to which this disruption specifically contributes to tinnitus or is simply a consequence of the hearing loss is unclear because the necessary matched controls have not been tested. Here, we rigorously test several predictions made by this model in four groups of participants (tinnitus with hearing loss, tinnitus with clinically normal hearing, no tinnitus with hearing loss and no tinnitus with clinically normal hearing). Magnetoencephalography was used to measure oscillatory brain activity within different frequency bands in a ‘resting’ state and during presentation of a masking noise. Results revealed that low-frequency activity in the delta band (1–4 Hz) was significantly higher in the ‘tinnitus with hearing loss’ group compared to the ‘no tinnitus with normal hearing’ group. A planned comparison indicated that this effect was unlikely to be driven by the hearing loss alone, but could possibly be a consequence of tinnitus and hearing loss. A further interpretative linkage to tinnitus was given by the result that the delta activity tended to reduce when tinnitus was masked. High-frequency activity in the gamma band (25–80 Hz) was not correlated with tinnitus (or hearing loss). The findings partly support the thalamocortical dysrhythmia model and suggest that slow-wave (delta band) activity may be a more reliable correlate of tinnitus than high-frequency activity.

Synaptic Interactions Underlying Synchronized Inhibition in the Basal Amygdala: Evidence for Existence of Two Types of Projection Cells

The basal amygdala (BA) plays a key role in mediating the facilitating effects of emotions on memory. Recent findings indicate that this function depends on the ability of BA neurons to generate coherent oscillatory activity, facilitating synaptic plasticity in target neurons. However, the mechanisms allowing BA neurons to synchronize their activity remain poorly understood. Here, we aimed to shed light on this question, focusing on a slow periodic inhibitory oscillation previously observed in the BA in vitro. Paired patch recordings showed that these large inhibitory postsynaptic potentials (IPSPs) occur almost synchronously in BA projection neurons, that they were typically not preceded by excitatory postsynaptic potentials (EPSPs), and that they had little or no correlate in neighboring amygdala nuclei or cortical fields. The initial phase of the IPSPs was associated with an increase in membrane potential fluctuations at 50-100 Hz. In keeping with this, the IPSPs seen in projection cells were correlated with repetitive firing at 50-100 Hz in presumed interneurons and they could be abolished by picrotoxin. However, the IPSPs were also sensitive to 6-cyano-7-nitroquinoxaline-2,3-dione, implying that they arose from the interplay between glutamatergic and GABAergic BA neurons. In support of this idea, we identified a small subset of projection cells (15%), positively identified as such by retrograde labeling from BA projection sites, that began firing shortly before the IPSP onset and presumably drove interneuronal firing. These results add to a rapidly growing body of data indicating that the BA contains at least two distinct types of projection cells that vary in their relation with interneurons and extra-amygdala targets.

Scale and frequency chauvinism in brain dynamics: too much emphasis on gamma band oscillations

In the early 1990s, Wolf Singer advanced a very provocative idea: Different features of an animal’s world are represented by distinct cell assemblies that can be bound together by oscillatory synchrony (Singer 1993; Singer and Gray 1995). In particular, simultaneous recordings from animal visual, association, somatosensory, and motor areas reveal that the cortical areas involved in task execution synchronize local field potentials (LFPs) when the animals prepare for the task and focus attention on the relevant stimulus. These findings emphasize LFP oscillations at frequencies in the gamma band (above 20–30 Hz). In perceptual and perceptual-motor tasks, gamma band synchrony is maintained until the task is completed, at which time the coherent patterns collapse and give way to low frequency incoherent oscillatory activity (Singer 2001). This “binding by synchrony” idea may well qualify as “a paradigm shift” in neuroscience by suggesting that coherent oscillatory activity across different cell assemblies is a critical feature underlying cognition rather than just fixed anatomical connections (Buzsaki 2006). This letter does not challenge the importance of gamma oscillations, nor do we deny the compelling notion of binding by synchrony. Rather, we question the (perhaps implicit) assumption by many neuroscientists that the most important aspects of human cognition are based mainly or even exclusively on the catch-all category labeled “gamma oscillations.” For one thing, the theoretical idea proposed by Singer that synchronization facilitates binding does not depend on or specify any particular frequency band. Our objections to the extreme gamma focus are based on several interrelated arguments as follows.

Highly selective processing of temporal information from attended stimuli in macaque’s visual area V4

Highly selective processing of temporal information from attended stimuli in macaque’s visual area V4

Stochastic Emergence of Repeating Cortical Motifs in Spontaneous Membrane Potential Fluctuations In Vivo

It was recently discovered that subthreshold membrane potential fluctuations of cortical neurons can precisely repeat during spontaneous activity, seconds to minutes apart, both in brain slices and in anesthetized animals. These repeats, also called cortical motifs, were suggested to reflect a replay of sequential neuronal firing patterns. We searched for motifs in spontaneous activity, recorded from the rat barrel cortex and from the cat striate cortex of anesthetized animals, and found numerous repeating patterns of high similarity and repetition rates. To test their significance, various statistics were compared between physiological data and three different types of stochastic surrogate data that preserve dynamical characteristics of the recorded data. We found no evidence for the existence of deterministically generated cortical motifs. Rather, the stochastic properties of cortical motifs suggest that they appear by chance, as a result of the constraints imposed by the coarse dynamics of subthreshold ongoing activity.

Ghosts in the Machine

It is a generally accepted notion that there is little room for plasticity of functions in a connectivity system based on a “wiring” that is rigidly predetermined by some blueprint. Conversely, a certain degree of plasticity is intuitively acceptable in a system in which there are inbuilt dynamic possibilities for alternative routes.–Janos Szentagothai, 1978

Relevance of EEG alpha and theta oscillations during task switching

In a task switching design, we investigated the question whether long-range theta coupling primarily reflects top-down control processes. Switch and stay trials did not differ with respect to memory load or global working memory (WM) demands. The results revealed significantly stronger theta coupling (in a range of 4-7 Hz) between prefrontal and posterior regions during switch as compared to stay trials. Power differences, reflecting more local effects, were largest in the upper alpha band (10-13 Hz) and over posterior brain areas, possibly reflecting long-term memory activation. The conclusion of the present study is that long-range coherent oscillatory activity in the theta band reflects top-down activation rather than global WM functions.

Role of Gap Junctions in Synchronized Neuronal Oscillations in the Inferior Olive

Inferior olivary (IO) neurons are electrically coupled through gap junctions and generate synchronous subthreshold oscillations of their membrane potential at a frequency of 1-10 Hz. Whereas the ionic mechanisms of these oscillatory responses are well understood, their origin and ensemble properties remain controversial. Here, the role of gap junctions in generating and synchronizing IO oscillations was examined by combining intracellular recordings with high-speed voltage-sensitive dye imaging in rat brain stem slices. Single cell responses and ensemble synchronized responses of IO neurons were compared in control conditions and in the presence of 18beta-glycyrrhetinic acid (18beta-GA), a pharmacological gap junction blocker. Under our experimental conditions, 18beta-GA had no adverse effects on intrinsic electroresponsive properties of IO neurons, other than the block of gap junction-dependent dye coupling and the resulting change in cells' passive properties. Application of 18beta-GA did not abolish single cell oscillations. Pharmacologically uncoupled IO neurons continued to oscillate with a frequency and amplitude that were similar to those recorded in control conditions. However, these oscillations were no longer synchronized across a population of IO neurons. Our optical recordings did not detect any clusters of synchronous oscillatory activity in the presence of the blocker. These results indicate that gap junctions are not necessary for generating subthreshold oscillations, rather, they are required for clustering of coherent oscillatory activity in the IO. The findings support the view that oscillatory properties of single IO neurons endow the system with important reset dynamics, while gap junctions are mainly required for synchronized neuronal ensemble activity.

Coherent Oscillatory Activity in Monkey Area V4 Predicts Successful Allocation of Attention

Attention serves to select objects from often complex scenes for enhanced processing and perception. In particular, the perception of shape depends critically on attention for integrating the various parts of the selected object into a coherent representation of object shape. To study whether oscillatory neuronal synchrony may serve as a mechanism of attention in shape perception, we introduced a novel shape-tracking task requiring sustained attention to a morphing shape. Attention was found to strongly increase oscillatory currents underlying the recorded field potentials in the gamma-frequency range, thus indicating enhanced neuronal synchrony within the population of V4 neurons representing the attended stimulus. Errors indicating a misdirection of attention to the distracter instead of the target were preceded by a corresponding shift of oscillatory activity from the target's neuronal representation to that of the distracter. No such effect was observed for errors unrelated to attention. Modulations of the attention-dependent enhancement of oscillatory activity occurred in correspondence with changing attentional demands during the course of a trial. The specificity of the effect of attentional errors together with the close coupling between attentional demand and oscillatory activity support the hypothesis that oscillatory neuronal synchrony serves as a mechanism of attention.

Brain State-Dependence of Coherent Oscillatory Activity along the Cortico-Striatal Axis of the Rat

Brain State-Dependence of Coherent Oscillatory Activity along the Cortico-Striatal Axis of the Rat

Brain state-dependency of coherent oscillatory activity in the cerebral cortex and basal ganglia of the rat.

The nature of the coupling between neuronal assemblies in the cerebral cortex and basal ganglia (BG) is poorly understood. We tested the hypothesis that coherent population activity is dependent on brain state, frequency range, and/or BG nucleus using data from simultaneous recordings of electrocorticogram (ECoG) and BG local field potentials (LFPs) in anesthetized rats. The coherence between ECoG and LFPs simultaneously recorded from subthalamic nucleus (STN), globus pallidus (GP), and substantia nigra pars reticulata (SNr) was largely confined to slow- ( approximately 1 Hz) and spindle- (7-12 Hz) frequency oscillations during slow-wave activity (SWA). In contrast, during cortical activation, coherence was mostly restricted to high-frequency oscillations (15-60 Hz). The coherence between ECoG and LFPs also depended on BG recording site. Partial coherence analyses showed that, during SWA, STN and SNr shared the same temporal coupling with cortex, thereby forming a single functional axis. Cortex was also tightly, but independently, correlated with GP in a separate functional axis. During activation, STN, GP, and, to a lesser extent, SNr shared the same coherence with cortex as part of one functional axis. In addition, GP formed a second, independently coherent loop with cortex. These data suggest that coherent oscillatory activity is present at the level of LFPs recorded in cortico-basal ganglia circuits, and that synchronized population activity is dynamically organized according to brain state, frequency, and nucleus. These attributes further suggest that synchronized activity should be considered as one of a number of candidate mechanisms underlying the functional organization of these brain circuits.

Optical recording of oscillatory neural activities in the molluscan brain

The procerebrum (PC) of the terrestrial slug shows a coherent oscillatory activity. Information is encoded in the PC by neurons with synchronized oscillatory activity, and the oscillatory activity will propagate to other brain regions as the PC transmits information. Using the optical recording of membrane potentials and the correlation analysis, we showed that the metacerebrum/mesocerebrum (MC) region also shows an oscillatory activity coherent with that of the PC. The MC oscillation was either inphase or antiphase with the PC oscillation, and its amplitude was larger when it was antiphase than it was inphase. These results indicate that the MC is capable of producing an oscillatory activity, possibly driven by synaptic input from the PC.

Mechanisms of anesthesia: towards integrating network, cellular, and molecular level modeling.

The mechanisms of anesthesia are surprisingly little understood. The present article summarizes current knowledge about the function of general anesthetics at different organization levels of the nervous system. It argues that a consensus view can be constructed, assuming that general anesthetics modulate the activity of ion channels, the main targets being GABA and NMDA channels and possibly voltage-gated and background channels, thereby hyperpolarizing neurons in thalamocortical loops, which lead to disruption of coherent oscillatory activity in the cortex. Two computational cases are used to illustrate the possible importance of molecular level effects on cellular level activity. Subtle differences in the mechanism of ion channel block can be shown to cause considerable differences in the modification of the oscillatory activity in a single neuron, and consequently in an associated network. Finally, the relation between the anesthesia problem and the classical consciousness problem is discussed, and some consequences of introducing the phenomenon of degeneracy into the picture are pointed out.

Correlated multisecond oscillations in firing rate in the basal ganglia: modulation by dopamine and the subthalamic nucleus

Previous studies from this laboratory have shown that many neurons in the basal ganglia have multisecond (<0.5 Hz) periodicities in firing rate in awake rats. The frequency and regularity of these oscillations are significantly increased by systemically injected dopamine (DA) agonists. Because oscillatory activity should have greater functional impact if shared by many neurons, the level of correlation of multisecond oscillations was assessed by recording pairs of neurons in the globus pallidus and substantia nigra pars reticulata in the same hemisphere, or pairs of globus pallidus neurons in opposite hemispheres in awake, immobilized rats. Cross-correlation (90–180 s lags) and spectral analysis were used to characterize correlated oscillations. Thirty-eight percent of pairs recorded in baseline ( n=50) demonstrated correlated multisecond oscillations. Phase relationships were near 0 or 180°. DA agonist injection significantly increased the incidence of correlation (intra- and interhemispheric) to 94% ( n=17). After DA agonist injection, phase relationships of globus pallidus/substantia nigra neuron pairs were exclusively concentrated near 180°, and phases of interhemispheric pairs of globus pallidus neurons were concentrated near 0°. After subthalamic nucleus lesion ( n=8), the incidence of correlated multisecond oscillations (or of multisecond oscillations per se) was not changed, although the consistent phase relationship between the globus pallidus and substantia nigra pars reticulata was disrupted. Subthalamic lesion also blocked apomorphine-induced decreases in oscillatory period and increases in oscillation amplitude, and significantly attenuated apomorphine-induced changes in mean firing rate. The data demonstrate that multisecond oscillations in the basal ganglia can be correlated between nuclei, and that DA receptor activation increases the level of correlation and organizes internuclear phase relationships at these multisecond time scales. While the subthalamic nucleus is not necessary for generating or transmitting these slow oscillations, it is involved in DA agonist-induced modulation of mean firing rate, oscillatory period, and internuclear phase relationship. These data further support a role for DA in modulating coherent oscillatory activity in the basal ganglia, and for the subthalamic nucleus in shaping the effects of DA receptor stimulation on basal ganglia output.