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Hippocampal theta oscillations (4-12 Hz) are consistently recorded during memory tasks and spatial navigation. Despite several known circuits and structures that generate hippocampal theta locally in vitro, none of them were found to be critical in vivo, and the hippocampal theta rhythm is severely attenuated by disruption of external input from medial septum or entorhinal cortex. We investigated these discrepancies that question the sufficiency and robustness of hippocampal theta generation using a biophysical spiking network model of the CA3 region of the hippocampus that included an interconnected network of pyramidal cells, inhibitory basket cells (BC) and oriens-lacunosum moleculare (OLM) cells. The model was developed by matching biological data characterizing neuronal firing patterns, synaptic dynamics, short-term synaptic plasticity, neuromodulatory inputs, and the three-dimensional organization of the hippocampus. The model generated theta power robustly through five cooperating generators: spiking oscillations of pyramidal cells, recurrent connections between them, slow-firing interneurons and pyramidal cells subnetwork, the fast-spiking interneurons and pyramidal cells subnetwork, and non-rhythmic structured external input from entorhinal cortex to CA3. We used the modeling framework to quantify the relative contributions of each of these generators to theta power, across different cholinergic states. The largest contribution to theta power was that of the divergent input from the entorhinal cortex to CA3, despite being constrained to random Poisson activity. We found that the low cholinergic states engaged the recurrent connections in generating theta activity, whereas high cholinergic states utilized the OLM-pyramidal subnetwork. These findings revealed that theta might be generated differently across cholinergic states, and demonstrated a direct link between specific theta generators and neuromodulatory states.
Movements cause changes in cortical rhythms emanating from the sensorimotor area. It is known that alpha and beta brainwaves take an important role of motor activity and motor imagery. Besides, theta rhythm is considered to carry substantial information about movement initiation and execution. In this study, effect of theta brainwave on movement detection was investigated in four-right handed participants who performed extensions with fingers of right hand using electroencephalography (EEG). Movement and rest epochs from continuous EEG record were extracted using muscle signals. Channels located over sensorimotor area were selected and referenced according to common average and Laplacian reference methods. Power spectral density function was used to display existence of theta band in frequency domain. To analyze theta, alpha and beta rhythms of the epochs individually and together, we filtered them to their interval range with Butterworth bandpass infinite filter before feature extraction and classification stages. Then, principal component analysis and Hjorth parameters were chosen to extract efficient features in the study aiming to investigate the effect of theta brainwaves on finger movement detection. According to classification accuracies using support vector machine classifier, alpha, beta, theta rhythms and also their different combinations were compared with each other. The performance of the epochs including alpha, beta and theta rhythms were the best and they were classified ~2% to 4% higher value in accuracy than the signals including only alpha and beta rhythms. According to this, it has proved that theta brainwave takes a role and makes contribution to motor activity.
The present study was undertaken to identify the noradrenergic receptors underlying the production of hippocampal formation (HPC) type 2 theta rhythm. The experiments were performed on urethanized rats wherein type 2 theta is the only rhythm present. In three independent stages of experiments, the effects of noradrenaline (NE) and selective noradrenergic α and β agonists and antagonists were tested. We indicate that the selective activation of three HPC noradrenergic receptors, α1, α2 and β1, induced a similar effect (i.e., inhibition) on type 2 theta rhythm. The remaining HPC β2 and β3 noradrenergic receptors do not seem to be directly involved in the pharmacological mechanism responsible for the suppression of theta rhythm in anaesthetized rats. Obtained results provide evidence for the suppressant effect of exogenous NE on HPC type 2 theta rhythm and show the crucial role of α1, α2 and β1 noradrenergic receptors in the modulation of HPC mechanisms of oscillations and synchrony. This finding is in contrast to the effects of endogenous NE produced by electrical stimulation of the locus coeruleus (LC) and procaine injection into the LC (Broncel et al., 2020).
Rapid eye movement (REM) sleep onset is triggered by disinhibition of cholinergic neurons in the pons. During REM sleep, the brain exhibits prominent activity in the 5-8 Hz (theta) frequency range. How REM sleep onset and theta waves are regulated is poorly understood. Astrocytes, a non-neuronal cell type in the brain, respond to cholinergic signals by elevating their intracellular Ca2+ concentration. The goal of this study was to assess the sleep architecture of mice with attenuated IP3 mediated Ca2+ signaling in astrocytes. Vigilance states and cortical electroencephalograph power were measured in wild type mice and mice with attenuated IP3/Ca2+ signaling. Attenuating IP3/Ca2+ signaling specifically in astrocytes caused mice to spend more time in REM sleep and enter this state more frequently during their inactive phase. These mice also exhibited greater power in the theta frequency range. These data suggest a role for astrocytic IP3/Ca2+ signaling in modulating REM sleep and the associated physiological state of the cortex.
Epileptic spike is an indicator of hyper-excitability and hyper-synchrony of neural networks. While cognitive deficit in epilepsy is a common observation, how spikes transiently influence brain oscillations, especially those essential for cognitive functions, remains obscure. Here we aimed to quantify the transient impacts of sporadic spikes on theta oscillations and investigate how such impacts may evolve during epileptogenesis. Longitudinal depth EEG data were recorded in the CA1 area of pilocarpine temporal lobe epilepsy (TLE) rat models. Phase stability, a measure of synchrony, and theta power were estimated around spikes as well as in the protracted spike-free periods (FP) at least 1h after spike bursts. We found that the change in theta power did not correlate with the change in phase stability. More importantly, the impact of spikes on theta rhythm was highly time-dependent. While theta power decreased abruptly after spikes both in the latent and chronic stages, changes of theta phase stability demonstrated opposite trends in the latent and chronic stages, potentially due to the substantial reorganization of neural circuits along epileptogenesis. During FP, theta phase stability was significantly higher than the baseline level before injections, indicating that hyper-synchrony remained even hours after the spike bursts. We concluded that spikes have transient negative effects on theta rhythm, however, impacts are different during latent and chronic stages, implying that its influence on cognitive processes may also change over time during epileptogenesis.
The present study examines possible relationships between changes in electroencephalogram (EEG) power and in working memory (WM) due to brain maturation. Scores on the phonological loop, visuospatial sketchpad and executive components of WM, measured by the Working Memory Test Battery for Children (WMTB-C), were correlated with the power spectral density (PSD) values on the spontaneous EEG from 1 to 46 Hz. In order to control for non-specific processes of visuomotor abilities, the reaction time (RT) variable was measured with an Oddball task. One hundred and sixty seven subjects (82 males and 85 females) between 6 and 26 years old participated in the study. Three minutes of spontaneous EEG were recorded. The WMTB-C and the Oddball task were also administered. The scores on each WM component increased and the RT in the Oddball decreased with age, while PSD values in the different frequencies decreased with age. Significant negative correlations between each of the components and the PSD were obtained. The maximal negative correlations were obtained in the theta (4-7 Hz) range. A bivariate linear model including theta PSD and RT explained most of the WM variance due to age. The results suggest that spontaneous EEG maturation is closely related to WM maturation, particularly in the theta range.
Theta rhythms govern rodent sniffing and whisking, and human language processing. Human psychophysics suggests a role for theta also in visual attention. However, little is known about theta in visual areas and its attentional modulation. We used electrocorticography (ECoG) to record local field potentials (LFPs) simultaneously from areas V1, V2, V4, and TEO of two macaque monkeys performing a selective visual attention task. We found a ≈4-Hz theta rhythm within both the V1-V2 and the V4-TEO region, and theta synchronization between them, with a predominantly feedforward directed influence. ECoG coverage of large parts of these regions revealed a surprising spatial correspondence between theta and visually induced gamma. Furthermore, gamma power was modulated with theta phase. Selective attention to the respective visual stimulus strongly reduced these theta-rhythmic processes, leading to an unusually strong attention effect for V1. Microsaccades (MSs) were partly locked to theta. However, neuronal theta rhythms tended to be even more pronounced for epochs devoid of MSs. Thus, we find an MS-independent theta rhythm specific to visually driven parts of V1-V2, which rhythmically modulates local gamma and entrains V4-TEO, and which is strongly reduced by attention. We propose that the less theta-rhythmic and thereby more continuous processing of the attended stimulus serves the exploitation of this behaviorally most relevant information. The theta-rhythmic and thereby intermittent processing of the unattended stimulus likely reflects the ecologically important exploration of less relevant sources of information.
The hippocampus is crucial for episodic or declarative memory and the theta rhythm has been implicated in mnemonic processing, but the functional contribution of theta to memory remains the subject of intense speculation. Recent evidence suggests that the hippocampus might function as a network hub for volitional learning. In contrast to human experiments, electrophysiological recordings in the hippocampus of behaving rodents are dominated by theta oscillations reflecting volitional movement, which has been linked to spatial exploration and encoding. This literature makes the surprising cross-species prediction that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. We examined the links between theta, spatial exploration, and memory encoding by designing an interactive human spatial navigation paradigm combined with multimodal neuroimaging. We used both non-invasive whole-head Magnetoencephalography (MEG) to look at theta oscillations and Functional Magnetic Resonance Imaging (fMRI) to look at brain regions associated with volitional movement and learning. We found that theta power increases during the self-initiation of virtual movement, additionally correlating with subsequent memory performance and environmental familiarity. Performance-related hippocampal theta increases were observed during a static pre-navigation retrieval phase, where planning for subsequent navigation occurred. Furthermore, periods of the task showing movement-related theta increases showed decreased fMRI activity in the parahippocampus and increased activity in the hippocampus and other brain regions that strikingly overlap with the previously observed volitional learning network (the reverse pattern was seen for stationary periods). These fMRI changes also correlated with participant's performance. Our findings suggest that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. These findings directly extend the role of the hippocampus in spatial exploration in rodents to human memory and self-directed learning.
The phenomena of synchronization, rhythmogenesis and coherence observed in brain networks are believed to be a dynamic substrate for cognitive functions such as learning and memory. However, researchers are still debating whether the rhythmic activity emerges from the network morphology that developed during neurogenesis or as a result of neuronal dynamics achieved under certain conditions. In the present study, we observed self-organized spiking activity that converged to long, complex and rhythmically repeated superbursts in neural networks formed by mature hippocampal cultures with a high cellular density. The superburst lasted for tens of seconds and consisted of hundreds of short (50-100 ms) small bursts with a high spiking rate of 139.0 ± 78.6 Hz that is associated with high-frequency oscillations in the hippocampus. In turn, the bursting frequency represents a theta rhythm (11.2 ± 1.5 Hz). The distribution of spikes within the bursts was non-random, representing a set of well-defined spatio-temporal base patterns or motifs. The long superburst was classified into two types. Each type was associated with a unique direction of spike propagation and, hence, was encoded by a binary sequence with random switching between the two "functional" states. The precisely structured bidirectional rhythmic activity that developed in self-organizing cultured networks was quite similar to the activity observed in the in vivo experiments.
Electrical vagal nerve stimulation (VNS) has been used for years to treat patients with drug-resistant epilepsy. This technique also remains under investigation as a specific treatment of patients with Alzheimer's disease. Recently we discovered that VNS induced hippocampal formation (HPC) type II theta rhythm, which is involved in memory consolidation. In the present study, we have extended our previous observation and addressed the neuronal substrate and pharmacological profile of HPC type II theta rhythm induced by VNS in anesthetized rats.
The hippocampal theta rhythm is required for accurate navigation and spatial memory but its relation to the dynamics of locomotion is poorly understood. We used miniature accelerometers to quantify with high temporal and spatial resolution the oscillatory movements associated with running in rats. Simultaneously, we recorded local field potentials in the CA1 area of the hippocampus. We report that when rats run their heads display prominent vertical oscillations with frequencies in the same range as the hippocampal theta rhythm (i.e., 6-12 Hz). In our behavioral set-up, rats run mainly with speeds between 50 and 100 cm/s. In this range of speeds, both the amplitude and frequency of the "theta" head oscillations were increasing functions of running speed, demonstrating that the head oscillations are part of the locomotion dynamics. We found evidence that these rhythmical locomotor dynamics interact with the neuronal activity in the hippocampus. The amplitude of the hippocampal theta rhythm depended on the relative phase shift with the head oscillations, being maximal when the two signals were in phase. Despite similarity in frequency, the head movements and LFP oscillations only displayed weak phase and frequency locking. Our results are consistent with that neurons in the CA1 region receive inputs that are phase locked to the head acceleration signal and that these inputs are integrated with the ongoing theta rhythm.
The theta rhythm organizes neural activity across hippocampus and entorhinal cortex. A role for theta oscillations in spatial navigation is supported by half a century of research reporting that theta frequency encodes running speed linearly so that displacement can be estimated through theta frequency integration. We show that this relationship is an artifact caused by the fact that the speed of freely moving animals could not be systematically disentangled from acceleration. Using an experimental procedure that clamps running speed at pre-set values, we find that the theta frequency of local field potentials and spike activity is linearly related to positive acceleration, but not negative acceleration or speed. The modulation by positive-only acceleration makes rhythmic activity at theta frequency unfit as a code to compute displacement or any other kinematic variable. Temporally precise variations in theta frequency may instead serve as a mechanism for speeding up entorhinal-hippocampal computations during accelerated movement.
The subiculum is positioned at a critical juncture at the interface of the hippocampus with the rest of the brain. However, the exact roles of the subiculum in most hippocampal-dependent memory tasks remain largely unknown. One obstacle to make comparisons of neural firing patterns between the subiculum and hippocampus is the broad firing fields of the subicular cells. Here, we used spiking phases in relation to theta rhythm to parse the broad firing field of a subicular neuron into multiple subfields to find the unique functional contribution of the subiculum while male rats performed a hippocampal-dependent visual scene memory task. Some of the broad firing fields of the subicular neurons were successfully divided into multiple subfields similar to those in the CA1 by using the theta phase precession cycle. The new paradigm significantly improved the detection of task-relevant information in subicular cells without affecting the information content represented by CA1 cells. Notably, we found that multiple fields of a single subicular neuron, unlike those in the CA1, carried heterogeneous task-related information such as visual context and choice response. Our findings suggest that the subicular cells integrate multiple task-related factors by using theta rhythm to associate environmental context with action.
It has been proposed that sleep's contribution to memory consolidation is to reactivate prior encoded information. To elucidate the neural mechanisms carrying reactivation-related mnemonic information, we investigated whether content-specific memory signatures associated with memory reactivation during wakefulness reoccur during subsequent sleep. We show that theta oscillations orchestrate the reactivation of memories during both wakefulness and sleep. Reactivation patterns during sleep autonomously re-emerged at a rate of ∼1 Hz, indicating a coordination by slow oscillatory activity.
Previously obtained data suggests that noradrenaline (NE) released from the efferent locus coeruleus (LC) endings in hippocampal formation (HPC) may serve as an important modulating signal involved in the pharmacological mechanisms responsible for the production of type 2 theta rhythm in rats. Hence, two distinct hypotheses were tested in the present study: 1/ if the decrease in HPC level of NE is correlated with the desynchronization of HPC field potential, then the inhibition of LC would be expected to abolish HPC type 2 theta rhythm; 2/ if the increase in HPC NE level is correlated with synchronization of HPC field potential, then the stimulation of LC would be expected to produce type 2 theta. The experiments were performed using an experimental model of HPC type 2 theta rhythm recorded in urethanized rats. It was demonstrated that electrical stimulation of LC produced type 2 theta rhythm whereas procaine injection into LC, in contrast, reversibly abolished type 2 theta. The possible relation of type 2 theta rhythm with some disturbances of Alzheimer disease are addressed.
Previously we have demonstrated that vagal nerve stimulation (VNS) is capable of inducing hippocampal formation (HPC) theta rhythm (Broncel et al., 2017). The neuronal substrate underlying this novel phenomenon is poorly known, though the cholinergic and GABAergic profile of VNS-induced theta rhythm in anesthetized rats has just recently been addressed (Broncel et al., 2018a, 2019). In this study we extended our earlier observation concerning the pharmacological profile of VNS-induced theta oscillations. Specifically, the purpose of the present study was to test the hypothesis that VNS-induced hippocampal theta rhythm could be modulated by local HPC gap junctions (GJs) transmission. Two GJs agents were used: carbenoxolone, nonspecific GJs blocker and trimethylamine, a nonspecific opener of GJs. Two basic parameters of theta rhythm were evaluated: frequency and power. It was demonstrated that carbenoxolone inhibits VNS-induced theta while trimethylamine facilities it. These observations indicate that HPC electrical coupling mediates the theta rhythm induced by vagal nerve stimulation.
In our previous studies, we have shown that (D-Ser2) oxyntomodulin (Oxm), a glucagon-like peptide 1 (GLP-1) receptor (GLP1R)/glucagon receptor (GCGR) dual agonist peptide, protects hippocampal neurons against Aβ1-42-induced cytotoxicity, and stabilizes the calcium homeostasis and mitochondrial membrane potential of hippocampal neurons. Additionally, we have demonstrated that (D-Ser2) Oxm improves cognitive decline and reduces the deposition of amyloid-beta in Alzheimer's disease model mice. However, the protective mechanism remains unclear. In this study, we showed that 2 weeks of intraperitoneal administration of (D-Ser2) Oxm ameliorated the working memory and fear memory impairments of 9-month-old 3×Tg Alzheimer's disease model mice. In addition, electrophysiological data recorded by a wireless multichannel neural recording system implanted in the hippocampal CA1 region showed that (D-Ser2) Oxm increased the power of the theta rhythm. In addition, (D-Ser2) Oxm treatment greatly increased the expression level of synaptic-associated proteins SYP and PSD-95 and increased the number of dendritic spines in 3×Tg Alzheimer's disease model mice. These findings suggest that (D-Ser2) Oxm improves the cognitive function of Alzheimer's disease transgenic mice by recovering hippocampal synaptic function and theta rhythm.
Anxiety and panic are both elicited by threat and co-occur clinically. But, at the neural level, anxiety appears to inhibit the generation of panic; and vice versa. Anxiety and panic are thought to engage more anterior (a) and mid-posterior (m) parts of the periaqueductal gray (PAG), respectively. Anxiety also engages the hippocampus and medial prefrontal cortex. Here, we tested if mPAG but not aPAG stimulation would suppress prefrontal and hippocampal theta rhythm as do anxiolytic drugs. Twelve male rats with implanted electrodes were stimulated alternately (30 s interval) in the left PAG or right reticular formation (reticularis pontis oralis [RPO]-as a positive control) with recording in the left prelimbic cortex and left and right hippocampus. PAG stimulation was set to produce freezing and RPO to produce 7-8 Hz theta rhythm before tests lasting 10 min on each of 5 days. mPAG stimulation decreased, and aPAG increased, theta power at all sites during elicited freezing. mPAG, but not aPAG, stimulation decreased prefrontal theta frequency. Stimulation did not substantially change circuit dynamics (pairwise phase consistency and partial directed coherence). Together with previous reports, our data suggest that panic- and anxiety-control systems are mutually inhibitory, and neural separation of anxiety and panic extends down to the aPAG and mPAG, respectively. Our findings are consistent with recent proposals that fear and anxiety are controlled by parallel neural hierarchies extending from PAG to the prefrontal cortex.
Neuronal synchrony in the basolateral amygdala (BLA) is critical for emotional behavior. Coordinated theta-frequency oscillations between the BLA and the hippocampus and precisely timed integration of salient sensory stimuli in the BLA are involved in fear conditioning. We characterized GABAergic interneuron types of the BLA and determined their contribution to shaping these network activities. Using in vivo recordings in rats combined with the anatomical identification of neurons, we found that the firing of BLA interneurons associated with network activities was cell type specific. The firing of calbindin-positive interneurons targeting dendrites was precisely theta-modulated, but other cell types were heterogeneously modulated, including parvalbumin-positive basket cells. Salient sensory stimuli selectively triggered axo-axonic cells firing and inhibited firing of a disctinct projecting interneuron type. Thus, GABA is released onto BLA principal neurons in a time-, domain-, and sensory-specific manner. These specific synaptic actions likely cooperate to promote amygdalo-hippocampal synchrony involved in emotional memory formation.
Although the importance of the mammillary body for memory and learning processes is well known, its exact role has remained vague. The fact, that many neurons in one nucleus of the mammillary body in rats, i.e. the medial mammillary nucleus (MM), fires according with hippocampal theta rhythm, makes this structure crucial for a theta rhythm signaling in so-called extended hippocampal system. These neurons are driven by descending projections from the hippocampal formation, but it is still unknown whether the mammillary body only conveys theta rhythm or may also modulate it. In the present study, we investigated the effect of pharmacological inactivation (local infusion of 0.5μl of 20% procaine hydrochloride solution) of the MM on hippocampal theta rhythm in urethane-anesthetized rats. We found that intra-MM procaine microinjections suppress sensory-elicited theta rhythm in the hippocampus by reduction of its amplitude, but not the frequency. Procaine infusion decreased the EEG signal power of low theta frequency bands, i.e. 3-5Hz, down to 9.2% in 3-4Hz band in comparison to pre-injection conditions. After water infusion (control group) no changes of hippocampal EEG signal power were observed. Our findings showed for the first time that inactivation of the MM leads to a disruption of hippocampal theta rhythm in the rat, which may suggest that the mammillary body can regulate theta rhythm signaling in the extended hippocampal system.
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