Hub structure in functional network of EEG signals supporting high cognitive functions in older individuals.

Introduction: Maintaining high cognitive functions is desirable for "wellbeing" in old age and is particularly relevant to a super-aging society. According to their individual cognitive functions, optimal intervention for older individuals facilitates the maintenance of cognitive functions. Cognitive function is a result of whole-brain interactions. These interactions are reflected in several measures in graph theory analysis for the topological characteristics of functional connectivity. Betweenness centrality (BC), which can identify the "hub" node, i.e., the most important node affecting whole-brain network activity, may be appropriate for capturing whole-brain interactions. During the past decade, BC has been applied to capture changes in brain networks related to cognitive deficits arising from pathological conditions. In this study, we hypothesized that the hub structure of functional networks would reflect cognitive function, even in healthy elderly individuals. Method: To test this hypothesis, based on the BC value of the functional connectivity obtained using the phase lag index from the electroencephalogram under the eyes closed resting state, we examined the relationship between the BC value and cognitive function measured using the Five Cognitive Functions test total score. Results: We found a significant positive correlation of BC with cognitive functioning and a significant enhancement in the BC value of individuals with high cognitive functioning, particularly in the frontal theta network. Discussion: The hub structure may reflect the sophisticated integration and transmission of information in whole-brain networks to support high-level cognitive function. Our findings may contribute to the development of biomarkers for assessing cognitive function, enabling optimal interventions for maintaining cognitive function in older individuals.

Enhanced temporal complexity of EEG signals in older individuals with high cognitive functions.

Recent studies suggest that the maintenance of cognitive function in the later life of older people is an essential factor contributing to mental wellbeing and physical health. Particularly, the risk of depression, sleep disorders, and Alzheimer's disease significantly increases in patients with mild cognitive impairment. To develop early treatment and prevention strategies for cognitive decline, it is necessary to individually identify the current state of cognitive function since the progression of cognitive decline varies among individuals. Therefore, the development of biomarkers that allow easier measurement of cognitive function in older individuals is relevant for hyperaged societies. One of the methods used to estimate cognitive function focuses on the temporal complexity of electroencephalography (EEG) signals. The characteristics of temporal complexity depend on the time scale, which reflects the range of neuron functional interactions. To capture the dynamics, composed of multiple time scales, multiscale entropy (MSE) analysis is effective for comprehensively assessing the neural activity underlying cognitive function in the brain. Thus, we hypothesized that EEG complexity analysis could serve to assess a wide range of cognitive functions in older adults. To validate our hypothesis, we divided older participants into two groups based on their cognitive function test scores: a high cognitive function group and a low cognitive function group, and applied MSE analysis to the measured EEG data of all participants. The results of the repeated-measures analysis of covariance using age and sex as a covariate in the MSE profile showed a significant difference between the high and low cognitive function groups (F = 10.18, p = 0.003) and the interaction of the group × electrodes (F = 3.93, p = 0.002). Subsequently, the results of the post-hoc t-test showed high complexity on a slower time scale in the frontal, parietal, and temporal lobes in the high cognitive function group. This high complexity on a slow time scale reflects the activation of long-distance neural interactions among various brain regions to achieve high cognitive functions. This finding could facilitate the development of a tool for diagnosis of cognitive decline in older individuals.

Long-Tailed Characteristic of Spiking Pattern Alternation Induced by Log-Normal Excitatory Synaptic Distribution.

Studies of structural connectivity at the synaptic level show that in synaptic connections of the cerebral cortex, the excitatory postsynaptic potential (EPSP) in most synapses exhibits sub-mV values, while a small number of synapses exhibit large EPSPs ( >~1.0 [mV]). This means that the distribution of EPSP fits a log-normal distribution. While not restricting structural connectivity, skewed and long-tailed distributions have been widely observed in neural activities, such as the occurrences of spiking rates and the size of a synchronously spiking population. Many studies have been modeled this long-tailed EPSP neural activity distribution; however, its causal factors remain controversial. This study focused on the long-tailed EPSP distributions and interlateral synaptic connections primarily observed in the cortical network structures, thereby having constructed a spiking neural network consistent with these features. Especially, we constructed two coupled modules of spiking neural networks with excitatory and inhibitory neural populations with a log-normal EPSP distribution. We evaluated the spiking activities for different input frequencies and with/without strong synaptic connections. These coupled modules exhibited intermittent intermodule-alternative behavior, given moderate input frequency and the existence of strong synaptic and intermodule connections. Moreover, the power analysis, multiscale entropy analysis, and surrogate data analysis revealed that the long-tailed EPSP distribution and intermodule connections enhanced the complexity of spiking activity at large temporal scales and induced nonlinear dynamics and neural activity that followed the long-tailed distribution.

High Phase Synchronization in Alpha Band Activity in Older Subjects With High Creativity.

Despite growing evidence that high creativity leads to mental well-being in older individuals, the neurophysiological bases of creativity remain elusive. Creativity reportedly involves multiple brain areas and their functional interconnections. In particular, functional magnetic resonance imaging (fMRI) is used to investigate the role of patterns of functional connectivity between the default network and other networks in creative activity. These interactions among networks play the role of integrating various neural processes to support creative activity and involve attention, cognitive control, and memory. The electroencephalogram (EEG) enables researchers to capture a pattern of band-specific functional connectivity, as well as moment-to-moment dynamics of brain activity; this can be accomplished even in the resting-state by exploiting the excellent temporal resolution of the EEG. Furthermore, the recent advent of functional connectivity analysis in EEG studies has focused on the phase-difference variable because of its fine spatio-temporal resolution. Therefore, we hypothesized that the combining method of EEG signals having high-temporal resolution and the phase synchronization analysis having high-spatio-temporal resolutions brings a new insight of functional connectivity regarding high creative activity of older participants. In this study, we examined the resting-state EEG signal in 20 healthy older participants and estimated functional connectivities using the phase lag index (PLI), which evaluates the phase synchronization of EEG signals. Individual creativity was assessed using the S-A creativity test in a separate session before the EEG recording. In the analysis of associations of EEG measures with the S-A test scores, the covariate effect of the intelligence quotient was evaluated. As a result, higher individual S-A scores were significantly associated with higher node degrees, defined as the average PLI of a node (electrode) across all links with the remaining nodes, across all nodes at the alpha band. A conventional power spectrum analysis revealed no significant association with S-A scores in any frequency band. Older participants with high creativity exhibited high functional connectivity even in the resting-state, irrespective of intelligence quotient, which supports the theory that creativity entails widespread brain connectivity. Thus, PLIs derived from EEG data may provide new insights into the relationship between functional connectivity and creativity in healthy older people.

Classification Methods Based on Complexity and Synchronization of Electroencephalography Signals in Alzheimer's Disease.

Electroencephalography (EEG) has long been studied as a potential diagnostic method for Alzheimer's disease (AD). The pathological progression of AD leads to cortical disconnection. These disconnections may manifest as functional connectivity alterations, measured by the degree of synchronization between different brain regions, and alterations in complex behaviors produced by the interaction among wide-spread brain regions. Recently, machine learning methods, such as clustering algorithms and classification methods, have been adopted to detect disease-related changes in functional connectivity and classify the features of these changes. Although complexity of EEG signals can also reflect AD-related changes, few machine learning studies have focused on the changes in complexity. Therefore, in this study, we compared the ability of EEG signals to detect characteristics of AD using different machine learning approaches one focused on functional connectivity and the other focused on signal complexity. We examined functional connectivity, estimated by phase lag index (PLI) in EEG signals in healthy older participants [healthy control (HC)] and patients with AD. We estimated signal complexity using multi-scale entropy. Utilizing a support vector machine, we compared the identification accuracy of AD based on functional connectivity at each frequency band and complexity component. Additionally, we evaluated the relationship between synchronization and complexity. The identification accuracy of functional connectivity of the alpha, beta, and gamma bands was significantly high (AUC 1.0), and the identification accuracy of complexity was sufficiently high (AUC 0.81). Moreover, the relationship between functional connectivity and complexity exhibited various temporal-scale-and-regional-specific dependency in both HC participants and patients with AD. In conclusion, the combination of functional connectivity and complexity might reflect complex pathological process of AD. Applying a combination of both machine learning methods to neurophysiological data may provide a novel understanding of the neural network processes in both healthy brains and pathological conditions.

Temporal-specific complexity of spiking patterns in spontaneous activity induced by a dual complex network structure.

Temporal fluctuation of neural activity in the brain has an important function in optimal information processing. Spontaneous activity is a source of such fluctuation. The distribution of excitatory postsynaptic potentials (EPSPs) between cortical pyramidal neurons can follow a log-normal distribution. Recent studies have shown that networks connected by weak synapses exhibit characteristics of a random network, whereas networks connected by strong synapses have small-world characteristics of small path lengths and large cluster coefficients. To investigate the relationship between temporal complexity spontaneous activity and structural network duality in synaptic connections, we executed a simulation study using the leaky integrate-and-fire spiking neural network with log-normal synaptic weight distribution for the EPSPs and duality of synaptic connectivity, depending on synaptic weight. We conducted multiscale entropy analysis of the temporal spiking activity. Our simulation demonstrated that, when strong synaptic connections approach a small-world network, specific spiking patterns arise during irregular spatio-temporal spiking activity, and the complexity at the large temporal scale (i.e., slow frequency) is enhanced. Moreover, we confirmed through a surrogate data analysis that slow temporal dynamics reflect a deterministic process in the spiking neural networks. This modelling approach may improve the understanding of the spatio-temporal complex neural activity in the brain.

Resonance phenomena controlled by external feedback signals and additive noise in neural systems.

Chaotic resonance is a phenomenon that can replace the fluctuation source in stochastic resonance from additive noise to chaos. We previously developed a method to control the chaotic state for suitably generating chaotic resonance by external feedback even when the external adjustment of chaos is difficult, establishing a method named reduced region of orbit (RRO) feedback. However, a feedback signal was utilized only for dividing the merged attractor. In addition, the signal sensitivity in chaotic resonance induced by feedback signals and that of stochastic resonance by additive noise have not been compared. To merge the separated attractor, we propose a negative strength of the RRO feedback signal in a discrete neural system which is composed of excitatory and inhibitory neurons. We evaluate the features of chaotic resonance and compare it to stochastic resonance. The RRO feedback signal with negative strength can merge the separated attractor and induce chaotic resonance. We also confirm that additive noise induces stochastic resonance through attractor merging. The comparison of these resonance modalities verifies that chaotic resonance provides more applicability than stochastic resonance given its capability to handle attractor separation and merging.

Atypical temporal-scale-specific fractal changes in Alzheimer's disease EEG and their relevance to cognitive decline.

Recent advances in nonlinear analytic methods for electroencephalography have clarified the reduced complexity of spatiotemporal dynamics in brain activity observed in Alzheimer's disease (AD). However, there are far fewer studies exploring temporal scale dependent fractal properties in AD, despite the importance of studying the dynamics of brain activity within physiologically relevant frequency ranges. Higuchi's fractal dimension is a widely used index for evaluating fractality in brain activity, but temporal-scale-specific characteristics are lost due to its requirement of averaging over the entire range of temporal scales. In this study, we adapted Higuchi's fractal algorithm into a method for investigating temporal-scale-specific fractal properties. We then compared the values of the temporal-scale-specific fractal dimension between healthy control (HC) and AD patient groups. Our data indicate that relative to the HC group, the AD group demonstrated reduced fractality at both slow and fast temporal scales. Moreover, we confirmed that the fractality at fast temporal scales correlates with cognitive decline. These properties might serve as a basis for a useful approach to characterizing temporal neural dynamics in AD or other neurodegenerative disorders.

Routes to Chaos Induced by a Discontinuous Resetting Process in a Hybrid Spiking Neuron Model.

Several hybrid spiking neuron models combining continuous spike generation mechanisms and discontinuous resetting processes following spiking have been proposed. The Izhikevich neuron model, for example, can reproduce many spiking patterns. This model clearly possesses various types of bifurcations and routes to chaos under the effect of a state-dependent jump in the resetting process. In this study, we focus further on the relation between chaotic behaviour and the state-dependent jump, approaching the subject by comparing spiking neuron model versions with and without the resetting process. We first adopt a continuous two-dimensional spiking neuron model in which the orbit in the spiking state does not exhibit divergent behaviour. We then insert the resetting process into the model. An evaluation using the Lyapunov exponent with a saltation matrix and a characteristic multiplier of the Poincar'e map reveals that two types of chaotic behaviour (i.e. bursting chaotic spikes and near-period-two chaotic spikes) are induced by the resetting process. In addition, we confirm that this chaotic bursting state is generated from the periodic spiking state because of the slow- and fast-scale dynamics that arise when jumping to the hyperpolarization and depolarization regions, respectively.

Band-specific atypical functional connectivity pattern in childhood autism spectrum disorder.

OBJECTIVE: Altered brain connectivity has been theorized as a key neural underpinning of autism spectrum disorder (ASD), but recent investigations have revealed conflicting patterns of connectivity, particularly hyper-connectivity and hypo-connectivity across age groups. The application of graph theory to neuroimaging data has become an effective approach for characterizing topographical patterns of large-scale functional networks. We used a graph approach to investigate alteration of functional networks in childhood ASD. METHOD: Magnetoencephalographic signals were quantified using graph-theoretic metrics with a phase lag index (PLI) for specific bands in 24 children with autism spectrum disorder and 24 typically developing controls. RESULTS: No significant group difference of PLI was found. Regarding topological organization, enhanced and reduced small-worldness, representing the efficiency of information processing, were observed respectively in ASD children, particularly in the gamma band and delta band. CONCLUSIONS: Analyses revealed frequency-dependent atypical neural network topologies in ASD children. SIGNIFICANCE: Our findings underscore the recently proposed atypical neural network theory of ASD during childhood. Graph theory with PLI applied to magnetoencephalographic signals might be a useful approach for characterizing the frequency-specific neurophysiological bases of ASD.

Chaotic Resonance in Typical Routes to Chaos in the Izhikevich Neuron Model.

Chaotic resonance (CR), in which a system responds to a weak signal through the effects of chaotic activities, is a known function of chaos in neural systems. The current belief suggests that chaotic states are induced by different routes to chaos in spiking neural systems. However, few studies have compared the efficiency of signal responses in CR across the different chaotic states in spiking neural systems. We focused herein on the Izhikevich neuron model, comparing the characteristics of CR in the chaotic states arising through the period-doubling or tangent bifurcation routes. We found that the signal response in CR had a unimodal maximum with respect to the stability of chaotic orbits in the tested chaotic states. Furthermore, the efficiency of signal responses at the edge of chaos became especially high as a result of synchronization between the input signal and the periodic component in chaotic spiking activity.

Analysis of Chaotic Resonance in Izhikevich Neuron Model.

In stochastic resonance (SR), the presence of noise helps a nonlinear system amplify a weak (sub-threshold) signal. Chaotic resonance (CR) is a phenomenon similar to SR but without stochastic noise, which has been observed in neural systems. However, no study to date has investigated and compared the characteristics and performance of the signal responses of a spiking neural system in some chaotic states in CR. In this paper, we focus on the Izhikevich neuron model, which can reproduce major spike patterns that have been experimentally observed. We examine and classify the chaotic characteristics of this model by using Lyapunov exponents with a saltation matrix and Poincaré section methods in order to address the measurement challenge posed by the state-dependent jump in the resetting process. We found the existence of two distinctive states, a chaotic state involving primarily turbulent movement and an intermittent chaotic state. In order to assess the signal responses of CR in these classified states, we introduced an extended Izhikevich neuron model by considering weak periodic signals, and defined the cycle histogram of neuron spikes as well as the corresponding mutual correlation and information. Through computer simulations, we confirmed that both chaotic states in CR can sensitively respond to weak signals. Moreover, we found that the intermittent chaotic state exhibited a prompter response than the chaotic state with primarily turbulent movement.

Modeling fluctuations in default-mode brain network using a spiking neural network.

Recently, numerous attempts have been made to understand the dynamic behavior of complex brain systems using neural network models. The fluctuations in blood-oxygen-level-dependent (BOLD) brain signals at less than 0.1 Hz have been observed by functional magnetic resonance imaging (fMRI) for subjects in a resting state. This phenomenon is referred to as a "default-mode brain network." In this study, we model the default-mode brain network by functionally connecting neural communities composed of spiking neurons in a complex network. Through computational simulations of the model, including transmission delays and complex connectivity, the network dynamics of the neural system and its behavior are discussed. The results show that the power spectrum of the modeled fluctuations in the neuron firing patterns is consistent with the default-mode brain network's BOLD signals when transmission delays, a characteristic property of the brain, have finite values in a given range.