The geometry of spontaneous spiking in neuronal networks

The mathematical theory of pattern formation in electrically coupled networks of excitable neurons forced by small noise is presented in this work. Using the Freidlin-Wentzell large deviation theory for randomly perturbed dynamical systems and the elements of the algebraic graph theory, we identify and analyze the main regimes in the network dynamics in terms of the key control parameters: excitability, coupling strength, and network topology. The analysis reveals the geometry of spontaneous dynamics in electrically coupled network. Specifically, we show that the location of the minima of a certain continuous function on the surface of the unit n-cube encodes the most likely activity patterns generated by the network. By studying how the minima of this function evolve under the variation of the coupling strength, we describe the principal transformations in the network dynamics. The minimization problem is also used for the quantitative description of the main dynamical regimes and transitions between them. In particular, for the weak and strong coupling regimes, we present asymptotic formulas for the network activity rate as a function of the coupling strength and the degree of the network. The variational analysis is complemented by the stability analysis of the synchronous state in the strong coupling regime. The stability estimates reveal the contribution of the network connectivity and the properties of the cycle subspace associated with the graph of the network to its synchronization properties. This work is motivated by the experimental and modeling studies of the ensemble of neurons in the Locus Coeruleus, a nucleus in the brainstem involved in the regulation of cognitive performance and behavior

Asynchronous response of coupled pacemaker neurons

We study a network model of two conductance-based pacemaker neurons of differing natural frequency, coupled with either mutual excitation or inhibition, and receiving shared random inhibitory synaptic input. The networks may phase-lock spike-to-spike for strong mutual coupling. But the shared input can desynchronize the locked spike-pairs by selectively eliminating the lagging spike or modulating its timing with respect to the leading spike depending on their separation time window. Such loss of synchrony is also found in a large network of sparsely coupled heterogeneous spiking neurons receiving shared input.Comment: 11 pages, 4 figures. To appear in Phys. Rev. Let

Synchronization and oscillatory dynamics in heterogeneous mutually inhibited neurons

We study some mechanisms responsible for synchronous oscillations and loss of synchrony at physiologically relevant frequencies (10-200 Hz) in a network of heterogeneous inhibitory neurons. We focus on the factors that determine the level of synchrony and frequency of the network response, as well as the effects of mild heterogeneity on network dynamics. With mild heterogeneity, synchrony is never perfect and is relatively fragile. In addition, the effects of inhibition are more complex in mildly heterogeneous networks than in homogeneous ones. In the former, synchrony is broken in two distinct ways, depending on the ratio of the synaptic decay time to the period of repetitive action potentials ($\tau_s/T$), where $T$ can be determined either from the network or from a single, self-inhibiting neuron. With $\tau_s/T > 2$, corresponding to large applied current, small synaptic strength or large synaptic decay time, the effects of inhibition are largely tonic and heterogeneous neurons spike relatively independently. With $\tau_s/T < 1$, synchrony breaks when faster cells begin to suppress their less excitable neighbors; cells that fire remain nearly synchronous. We show numerically that the behavior of mildly heterogeneous networks can be related to the behavior of single, self-inhibiting cells, which can be studied analytically.Comment: 17 pages, 6 figures, Kluwer.sty. Journal of Compuational Neuroscience (in press). Originally submitted to the neuro-sys archive which was never publicly announced (was 9802001

The Utility of Phase Models in Studying Neural Synchronization

Synchronized neural spiking is associated with many cognitive functions and thus, merits study for its own sake. The analysis of neural synchronization naturally leads to the study of repetitive spiking and consequently to the analysis of coupled neural oscillators. Coupled oscillator theory thus informs the synchronization of spiking neuronal networks. A crucial aspect of coupled oscillator theory is the phase response curve (PRC), which describes the impact of a perturbation to the phase of an oscillator. In neural terms, the perturbation represents an incoming synaptic potential which may either advance or retard the timing of the next spike. The phase response curves and the form of coupling between reciprocally coupled oscillators defines the phase interaction function, which in turn predicts the synchronization outcome (in-phase versus anti-phase) and the rate of convergence. We review the two classes of PRC and demonstrate the utility of the phase model in predicting synchronization in reciprocally coupled neural models. In addition, we compare the rate of convergence for all combinations of reciprocally coupled Class I and Class II oscillators. These findings predict the general synchronization outcomes of broad classes of neurons under both inhibitory and excitatory reciprocal coupling.Comment: 18 pages, 5 figure

Phase-locking in weakly heterogeneous neuronal networks

We examine analytically the existence and stability of phase-locked states in a weakly heterogeneous neuronal network. We consider a model of N neurons with all-to-all synaptic coupling where the heterogeneity is in the firing frequency or intrinsic drive of the neurons. We consider both inhibitory and excitatory coupling. We derive the conditions under which stable phase-locking is possible. In homogeneous networks, many different periodic phase-locked states are possible. Their stability depends on the dynamics of the neuron and the coupling. For weak heterogeneity, the phase-locked states are perturbed from the homogeneous states and can remain stable if their homogeneous conterparts are stable. For enough heterogeneity, phase-locked solutions either lose stability or are destroyed completely. We analyze the possible states the network can take when phase-locking is broken.Comment: RevTex, 27 pages, 3 figure

The Local Field Potential Reflects Surplus Spike Synchrony

The oscillatory nature of the cortical local field potential (LFP) is commonly interpreted as a reflection of synchronized network activity, but its relationship to observed transient coincident firing of neurons on the millisecond time-scale remains unclear. Here we present experimental evidence to reconcile the notions of synchrony at the level of neuronal spiking and at the mesoscopic scale. We demonstrate that only in time intervals of excess spike synchrony, coincident spikes are better entrained to the LFP than predicted by the locking of the individual spikes. This effect is enhanced in periods of large LFP amplitudes. A quantitative model explains the LFP dynamics by the orchestrated spiking activity in neuronal groups that contribute the observed surplus synchrony. From the correlation analysis, we infer that neurons participate in different constellations but contribute only a fraction of their spikes to temporally precise spike configurations, suggesting a dual coding scheme of rate and synchrony. This finding provides direct evidence for the hypothesized relation that precise spike synchrony constitutes a major temporally and spatially organized component of the LFP. Revealing that transient spike synchronization correlates not only with behavior, but with a mesoscopic brain signal corroborates its relevance in cortical processing.Comment: 45 pages, 8 figures, 3 supplemental figure

Internetwork and intranetwork communications during bursting dynamics: Applications to seizure prediction

We use a simple dynamical model of two interacting networks of integrate-and-fire neurons to explain a seemingly paradoxical result observed in epileptic patients indicating that the level of phase synchrony declines below normal levels during the state preceding seizures (preictal state). We model the transition from the seizure free interval (interictal state) to the seizure (ictal state) as a slow increase in the mean depolarization of neurons in a network corresponding to the epileptic focus. We show that the transition from the interictal to preictal and then to the ictal state may be divided into separate dynamical regimes: the formation of slow oscillatory activity due to resonance between the two interacting networks observed during the interictal period, structureless activity during the preictal period when the two networks have different properties, and bursting dynamics driven by the network corresponding to the epileptic focus. Based on this result, we hypothesize that the beginning of the preictal period marks the beginning of the transition of the epileptic network from normal activity toward seizing