Hopf Bifurcation in Mean Field Explains Critical Avalanches in Excitation-Inhibition Balanced Neuronal Networks: A Mechanism for Multiscale Variability
Cortical neural circuits display highly irregular spiking in individual neurons but variably sized collective firing, oscillations and critical avalanches at the population level, all of which have functional importance for information processing. Theoretically, the balance of excitation and inhibition inputs is thought to account for spiking irregularity and critical avalanches may originate from an underlying phase transition. However, the theoretical reconciliation of these multilevel dynamic aspects in neural circuits remains an open question. Herein, we study excitation-inhibition (E-I) balanced neuronal network with biologically realistic synaptic kinetics. It can maintain irregular spiking dynamics with different levels of synchrony and critical avalanches emerge near the synchronous transition point. We propose a novel semi-analytical mean-field theory to derive the field equations governing the network macroscopic dynamics. It reveals that the E-I balanced state of the network manifesting irregular individual spiking is characterized by a macroscopic stable state, which can be either a fixed point or a periodic motion and the transition is predicted by a Hopf bifurcation in the macroscopic field. Furthermore, by analyzing public data, we find the coexistence of irregular spiking and critical avalanches in the spontaneous spiking activities of mouse cortical slice in vitro, indicating the universality of the observed phenomena. Our theory unveils the mechanism that permits complex neural activities in different spatiotemporal scales to coexist and elucidates a possible origin of the criticality of neural systems. It also provides a novel tool for analyzing the macroscopic dynamics of E-I balanced networks and its relationship to the microscopic counterparts, which can be useful for large-scale modeling and computation of cortical dynamics.
Many systems in Nature exhibit avalanche dynamics with scale-free features. A general scaling theory has been proposed for critical avalanche profiles in crackling noise, predicting the collapse onto a universal avalanche shape, as well as the scaling behaviour of the activity power spectrum as Brown noise. Recently, much attention has been given to the profile of neuronal avalanches, measured in neuronal systems in vitro and in vivo. Although a universal profile was evidenced, confirming the validity of the general scaling theory, the parallel study of the power spectrum scaling under the sam…
The repertoire of neural activity patterns that a cortical network can produce constrains the network's ability to transfer and process information. Here, we measured activity patterns obtained from multi-site local field potential (LFP) recordings in cortex cultures, urethane anesthetized rats, and awake macaque monkeys. First, we quantified the information capacity of the pattern repertoire of ongoing and stimulus-evoked activity using Shannon entropy. Next, we quantified the efficacy of information transmission between stimulus and response using mutual information. By systematically changi…
Recently, neuronal avalanches have been observed to display oscillations, a phenomenon regarded as the co-existence of a scale-free behaviour (the avalanches close to criticality) and scale-dependent dynamics (the oscillations). Ordinary continuous-time branching processes with constant extinction and branching rates are commonly used as models of neuronal activity, yet they lack any such time-dependence. In the present work, we extend a basic branching process by allowing the extinction rate to oscillate in time as a new model to describe cortical dynamics. By means of a perturbative field th…
Power-law-shaped avalanche-size distributions are widely used to probe for critical behavior in many different systems, particularly in neural networks. The definition of avalanche is ambiguous. Usually, theoretical avalanches are defined as the activity between a stimulus and the relaxation to an inactive absorbing state. On the other hand, experimental neuronal avalanches are defined by the activity between consecutive silent states. We claim that the latter definition may be extended to some theoretical models to characterize their power-law avalanches and critical behavior. We study a syst…
As shown recently (arXiv:0801.3056), several types of neuronal complex networks involving non-linear integration-and-fire dynamics exhibit an abrupt activation along their transient regime. Interestingly, such an avalanche of activation has also been found to depend strongly on the topology of the networks: while the Erdős-Rény, Barabási-Albert, path-regular and path-transformed BA models exhibit well-defined avalanches; Watts-Strogatz and geographical structures present instead a gradual dispersion of activation amongst their nodes. The current work investigates such phenomena by considering …
Columbia University（哥伦比亚大学）；Edmond and Lily Safra Center for Brain Sciences（埃德蒙和莉莉·萨弗拉脑科学中心）；Racah Institute of Physics（拉卡物理研究所）；The Hebrew University of Jerusalem（耶路撒冷希伯来大学）；Center for Brain Science（脑科学中心）；Harvard University（哈佛大学）
Neurons and networks in the cerebral cortex must operate reliably despite multiple sources of noise. To evaluate the impact of both input and output noise, we determine the robustness of single-neuron stimulus selective responses, as well as the robustness of attractor states of networks of neurons performing memory tasks. We find that robustness to output noise requires synaptic connections to be in a balanced regime in which excitation and inhibition are strong and largely cancel each other. We evaluate the conditions required for this regime to exist and determine the properties of networks…
The model of the current paper is an extension of a previous publication, wherein we used the leaky integrate-and-fire model on a regular lattice with periodic boundary conditions, and introduced the temporal complexity as a genuine signature of criticality. In that work, the power-law distribution of neural avalanches was manifestation of supercriticality rather than criticality. Here, however, we show that continuous solution of the model and replacing the stochastic noise with a Gaussian zero-mean noise leads to the coincidence of power-law display of temporal complexity and spatiotemporal …
Recent experiments on cortical neural networks have revealed the existence of well-defined avalanches of electrical activity. Such avalanches have been claimed to be generically scale-invariant -- i.e. power-law distributed -- with many exciting implications in Neuroscience. Recently, a self-organized model has been proposed by Levina, Herrmann and Geisel to justify such an empirical finding. Given that (i) neural dynamics is dissipative and (ii) there is a loading mechanism "charging" progressively the background synaptic strength, this model/dynamics is very similar in spirit to forest-fire …
How the information microscopically processed by individual neurons is integrated and used in organizing the behavior of an animal is a central question in neuroscience. The coherence of neuronal dynamics over different scales has been suggested as a clue to the mechanisms underlying this integration. Balanced excitation and inhibition may amplify microscopic fluctuations to a macroscopic level, thus providing a mechanism for generating coherent multiscale dynamics. Previous theories of brain dynamics, however, were restricted to cases in which inhibition dominated excitation and suppressed fl…
We consider a simple Markovian class of the stochastic Wilson-Cowan type models of neuronal network dynamics, which incorporates stochastic delay caused by the existence of a refractory period of neurons. From the point of view of the dynamics of the individual elements, we are dealing with a network of non-Markovian stochastic two-state oscillators with memory which are coupled globally in a mean-field fashion. This interrelation of a higher-dimensional Markovian and lower-dimensional non-Markovian dynamics is discussed in its relevance to the general problem of the network dynamics of comple…
To date, it is still impossible to sample the entire mammalian brain with single-neuron precision. This forces one to either use spikes (focusing on few neurons) or to use coarse-sampled activity (averaging over many neurons, e.g. LFP). Naturally, the sampling technique impacts inference about collective properties. Here, we emulate both sampling techniques on a simple spiking model to quantify how they alter observed correlations and signatures of criticality. We describe a general effect: when the inter-electrode distance is small, electrodes sample overlapping regions in space, which increa…
We consider two neuronal networks coupled by long-range excitatory interactions. Oscillations in the gamma frequency band are generated within each network by local inhibition. When long-range excitation is weak, these oscillations phase-lock with a phase-shift dependent on the strength of local inhibition. Increasing the strength of long-range excitation induces a transition to chaos via period-doubling or quasi-periodic scenarios. In the chaotic regime oscillatory activity undergoes fast temporal decorrelation. The generality of these dynamical properties is assessed in firing-rate models as…
We investigate the synaptic noise as a novel mechanism for creating critical avalanches in the activity of neural networks. We model neurons and chemical synapses by dynamical maps with a uniform noise term in the synaptic coupling. An advantage of utilizing maps is that the dynamical properties (action potential profile, excitability properties, post synaptic potential summation etc.) are not imposed to the system, but occur naturally by solving the system equations. We discuss the relevant neuronal and synaptic properties to achieve the critical state. We verify that networks of excitatory b…
Neurons in the brain are wired into adaptive networks that exhibit a range of collective dynamics. Oscillations, for example, are paradigmatic synchronous patterns of neural activity with a defined temporal scale. Neuronal avalanches, in contrast, are scale-free cascades of neural activity, often considered as evidence of brain tuning to criticality. While models have been developed to account for oscillations or avalanches separately, they typically do not explain both phenomena, are too complex to analyze analytically, or intractable to infer from data rigorously. Here we propose a non-equil…
The "edge of chaos" phase transition in artificial neural networks is of renewed interest in light of recent evidence for criticality in brain dynamics. Statistical mechanics traditionally studied this transition with connectivity $k$ as the control parameter and an exactly balanced excitation-inhibition ratio. While critical connectivity has been found to be low in these model systems, typically around $k=2$, which is unrealistic for natural systems, a recent study utilizing the excitation-inhibition ratio as the control parameter found a new, nearly degree independent, critical point when co…
The collective dynamics of a network of excitable nodes changes dramatically when inhibitory nodes are introduced. We consider inhibitory nodes which may be activated just like excitatory nodes but, upon activating, decrease the probability of activation of network neighbors. We show that, although the direct effect of inhibitory nodes is to decrease activity, the collective dynamics becomes self-sustaining. We explain this counterintuitive result by defining and analyzing a "branching function" which may be thought of as an activity-dependent branching ratio. The shape of the branching functi…
We study a neural network model of interacting stochastic discrete two--state cellular automata on a regular lattice. The system is externally tuned to a critical point which varies with the degree of stochasticity (or the effective temperature). There are avalanches of neuronal activity, namely spatially and temporally contiguous sites of activity; a detailed numerical study of these activity avalanches is presented, and single, joint and marginal probability distributions are computed. At the critical point, we find that the scaling exponents for the variables are in good agreement with a me…
Through evolution, animals have acquired central nervous systems (CNSs), which are extremely efficient information processing devices that improve an animal's adaptability to various environments. It has been proposed that the process of information maximization (infomax), which maximizes the information transmission from the input to the output of a feedforward network, may provide an explanation of the stimulus selectivity of neurons in CNSs. However, CNSs contain not only feedforward but also recurrent synaptic connections, and little is known about information retention over time in such r…
Using an exactly solvable cortical model of a neuronal network, we show that, by increasing the intensity of shot noise (flow of random spikes bombarding neurons), the network undergoes first- and second-order non-equilibrium phase transitions. We study the nature of the transitions, bursts and avalanches of neuronal activity. Saddle-node and supercritical Hopf bifurcations are the mechanisms of emergence of sustained network oscillations. We show that the network stimulated by shot noise behaves similar to the Morris-Lecar model of a biological neuron stimulated by an applied current.
Thermodynamic criticality describes emergent phenomena in a wide variety of complex systems. In the mammalian brain, the complex dynamics that spontaneously emerge from neuronal interactions have been characterized as neuronal avalanches, a form of critical branching dynamics. Here, we show that neuronal avalanches also reflect that the brain dynamics are organized close to a thermodynamic critical point. We recorded spontaneous cortical activity in monkeys and humans at rest using high-density intracranial microelectrode arrays and magnetoencephalography, respectively. By numerically changing…
The critical brain hypothesis receives increasing support from recent experimental results. It postulates that the brain is at a critical point between an ordered and a chaotic regime, sometimes referred to as the "edge of chaos." Another central observation of neuroscience is the principle of excitation-inhibition balance: Certain brain networks exhibit a remarkably constant ratio between excitation and inhibition. When this balance is perturbed, the network shifts away from the critical point, as may for example happen during epileptic seizures. However, it is as of yet unclear what mechanis…
We investigate the stability of synchronization in networks of delay-coupled excitable neural oscillators. On the basis of the master stability function formalism, we demonstrate that synchronization is always stable for excitatory coupling independently of the delay and coupling strength. Superimposing inhibitory links randomly on top of a regular ring of excitatory coupling, which yields a small-world-like network topology, we find a phase transition to desynchronization as the probability of inhibitory links exceeds a critical value. We explore the scaling of the critical value in dependenc…
The presence of both critical behavior and oscillating patterns in brain dynamics is a very interesting issue. In this paper, we consider a model for a neuron population, where each neuron is modeled by an over-damped rotator. We find that in the space of external parameters, there exist some regions that system shows synchronization. Interestingly, just at the transition point, the avalanche statistics show a power-law behavior. Also, in the case of small systems, the (partially) synchronization and power-law behavior can happen at the same time.
Experiments in various neural systems found avalanches: bursts of activity with characteristics typical for critical dynamics. A possible explanation for their occurrence is an underlying network that self-organizes into a critical state. We propose a simple spiking model for developing neural networks, showing how these may "grow into" criticality. Avalanches generated by our model correspond to clusters of widely applied Hawkes processes. We analytically derive the cluster size and duration distributions and find that they agree with those of experimentally observed neuronal avalanches.
A certain degree of inhibition is a common trait of dynamical networks in nature, ranging from neuronal and biochemical networks, to social and technological networks. We study here the role of inhibition in a representative dynamical network model, characterizing the dynamics of random threshold networks with both excitatory and inhibitory links. Varying the fraction of excitatory links has a strong effect on the network's population activity and its sensitivity to perturbation. The average degree $K$, known to have a strong effect on the dynamics when small, loses its influence on the dynami…
In this article, a correlation metric $κ_C$ is proposed for the inference of the dynamical state of neuronal networks. $κ_C$ is computed from the scaling of the correlation length with the size of the observation region, which shows qualitatively different behavior near and away from the critical point of a continuous phase transition. The implementation is first studied on a neuronal network model, where the results of this new metric coincide with those obtained from neuronal avalanche analysis, thus well characterizing the critical state of the network. The approach is further tested with b…
Motivated by recent experiments in neuroscience which indicate that neuronal avalanches exhibit scale invariant behavior similar to self-organized critical systems, we study the role of noisy (non-conservative) local dynamics on the critical behavior of a sandpile model which can be taken to mimic the dynamics of neuronal avalanches. We find that despite the fact that noise breaks the strict local conservation required to attain criticality, our system exhibit true criticality for a wide range of noise in various dimensions, given that conservation is respected \textit{on the average}. Althoug…
The pairwise maximum entropy model, also known as the Ising model, has been widely used to analyze the collective activity of neurons. However, controversy persists in the literature about seemingly inconsistent findings, whose significance is unclear due to lack of reliable error estimates. We therefore develop a method for accurately estimating parameter uncertainty based on random walks in parameter space using adaptive Markov Chain Monte Carlo after the convergence of the main optimization algorithm. We apply our method to the spiking patterns of excitatory and inhibitory neurons recorded …
We characterize the distributions of size and duration of avalanches propagating in complex networks. By an avalanche we mean the sequence of events initiated by the externally stimulated `excitation' of a network node, which may, with some probability, then stimulate subsequent firings of the nodes to which it is connected, resulting in a cascade of firings. This type of process is relevant to a wide variety of situations, including neuroscience, cascading failures on electrical power grids, and epidemology. We find that the statistics of avalanches can be characterized in terms of the larges…
We use mean field theory to study the response properties of a simple randomly-connected model cortical network of leaky integrate-and-fire neurons with balanced excitation and inhibition. The formulation permits arbitrary temporal variation of the input to the network and takes exact account of temporal firing correlations. We find that neuronal firing statistics depend sensitively on the firing threshold. In particular, spike count variances can be either significantly greater than or significantly less than those for a Poisson process. These findings may help in understanding the variabilit…
Recent experiments suggest that inhibitory networks of interneurons can synchronize the neuronal discharge in in vitro hippocampal slices. Subsequent theoretical work has shown that strong synchronization by mutual inhibition is only moderately robust against neuronal heterogeneities in the current drive, provided by activation of metabotropic glutamate receptors. In vivo neurons display greater variability in the interspike intervals due to the presence of synaptic noise. Noise and heterogeneity affect synchronization properties differently. In this paper we study using model simulations how …
The study of neuronal interactions is currently at the center of several big collaborative neuroscience projects (including the Human Connectome Project, the Blue Brain Project, the Brainome, etc.) which attempt to obtain a detailed map of the entire brain. Under certain constraints, mathematical theory can advance predictions of the expected neural dynamics based solely on the statistical properties of the synaptic interaction matrix. This work explores the application of free random variables to the study of large synaptic interaction matrices. Besides recovering in a straightforward way kno…
We investigate the dynamics of a neural network where each neuron evolves according to the combined effects of deterministic integrate-and-fire dynamics and purely inhibitory coupling with K randomly-chosen "neighbors". The inhibition reduces the voltage of a given neuron by an amount Delta when one of its neighbors fires. The interplay between the integration and inhibition leads to a steady state which is determined by solving the rate equations for the neuronal voltage distribution. We also study the evolution of a single neuron and find that the mean lifetime between firing events equals 1…
Imperial College London（帝国理工学院）；University of Surrey（萨里大学）；Tokyo Institute of Technology（东京工业大学）
Neuronal network computation and computation by avalanche supporting networks are of interest to the fields of physics, computer science (computation theory as well as statistical or machine learning) and neuroscience. Here we show that computation of complex Boolean functions arises spontaneously in threshold networks as a function of connectivity and antagonism (inhibition), computed by logic automata (motifs) in the form of computational cascades. We explain the emergent inverse relationship between the computational complexity of the motifs and their rank-ordering by function probabilities…
Recent experiments suggested that homeostatic regulation of synaptic balance leads the visual system to recover and maintain a regime of power-law avalanches. Here we study an excitatory/inhibitory (E/I) mean-field neuronal network that has a critical point with power-law avalanches and synaptic balance. When short term depression in inhibitory synapses and firing threshold adaptation are added, the system hovers around the critical point. This homeostatically self-organized quasi-critical (SOqC) dynamics generates E/I synaptic current cancellation in fast time scales, causing fluctuation-driv…
Avalanches of electrochemical activity in brain networks have been empirically reported to obey scale-invariant behavior --characterized by power-law distributions up to some upper cut-off-- both in vitro and in vivo. Elucidating whether such scaling laws stem from the underlying neural dynamics operating at the edge of a phase transition is a fascinating possibility, as systems poised at criticality have been argued to exhibit a number of important functional advantages. Here we employ a well-known model for neural dynamics with synaptic plasticity, to elucidate an alternative scenario in whi…
Large sparse circuits of spiking neurons exhibit a balanced state of highly irregular activity under a wide range of conditions. It occurs likewise in sparsely connected random networks that receive excitatory external inputs and recurrent inhibition as well as in networks with mixed recurrent inhibition and excitation. Here we analytically investigate this irregular dynamics in finite networks keeping track of all individual spike times and the identities of individual neurons. For delayed, purely inhibitory interactions we show that the irregular dynamics is not chaotic but in fact stable. M…
This review gives a short historical account of the excitable maps approach for modeling neurons and neuronal networks. Some early models, due to Pasemann (1993), Chialvo (1995) and Kinouchi and Tragtenberg (1996), are compared with more recent proposals by Rulkov (2002) and Izhikevich (2003). We also review map-based schemes for electrical and chemical synapses and some recent findings as critical avalanches in map-based neural networks. We conclude with suggestions for further work in this area like more efficient maps, compartmental modeling and close dynamical comparison with conductance-b…
Networks of excitable nodes have recently attracted much attention particularly in regards to neuronal dynamics, where criticality has been argued to be a fundamental property. Refractory behavior, which limits the excitability of neurons is thought to be an important dynamical property. We therefore consider a simple model of excitable nodes which is known to exhibit a transition to instability at a critical point ($λ=1$), and introduce refractory period into its dynamics. We use mean-field analytical calculations as well as numerical simulations to calculate the activity dependent branching …
