Exact finite-dimensional description for networks of globally coupled spiking neurons.

We consider large networks of globally coupled spiking neurons and derive an exact low-dimensional description of their collective dynamics in the thermodynamic limit. Individual neurons are described by the Ermentrout-Kopell canonical model that can be excitable or tonically spiking and interact with other neurons via pulses. Utilizing the equivalence of the quadratic integrate-and-fire and the theta-neuron formulations, we first derive the dynamical equations in terms of the Kuramoto-Daido order parameters (Fourier modes of the phase distribution) and relate them to two biophysically relevant macroscopic observables, the firing rate and the mean voltage. For neurons driven by Cauchy white noise or for Cauchy-Lorentz distributed input currents, we adapt the results by Cestnik and Pikovsky [Chaos 32, 113126 (2022)1054-150010.1063/5.0106171] and show that for arbitrary initial conditions the collective dynamics reduces to six dimensions. We also prove that in this case the dynamics asymptotically converges to a two-dimensional invariant manifold first discovered by Ott and Antonsen. For identical, noise-free neurons, the dynamics reduces to three dimensions, becoming equivalent to the Watanabe-Strogatz description. We illustrate the exact six-dimensional dynamics outside the invariant manifold by calculating nontrivial basins of different asymptotic regimes in a bistable situation.

Mesoscopic description of hippocampal replay and metastability in spiking neural networks with short-term plasticity.

Bottom-up models of functionally relevant patterns of neural activity provide an explicit link between neuronal dynamics and computation. A prime example of functional activity patterns are propagating bursts of place-cell activities called hippocampal replay, which is critical for memory consolidation. The sudden and repeated occurrences of these burst states during ongoing neural activity suggest metastable neural circuit dynamics. As metastability has been attributed to noise and/or slow fatigue mechanisms, we propose a concise mesoscopic model which accounts for both. Crucially, our model is bottom-up: it is analytically derived from the dynamics of finite-size networks of Linear-Nonlinear Poisson neurons with short-term synaptic depression. As such, noise is explicitly linked to stochastic spiking and network size, and fatigue is explicitly linked to synaptic dynamics. To derive the mesoscopic model, we first consider a homogeneous spiking neural network and follow the temporal coarse-graining approach of Gillespie to obtain a "chemical Langevin equation", which can be naturally interpreted as a stochastic neural mass model. The Langevin equation is computationally inexpensive to simulate and enables a thorough study of metastable dynamics in classical setups (population spikes and Up-Down-states dynamics) by means of phase-plane analysis. An extension of the Langevin equation for small network sizes is also presented. The stochastic neural mass model constitutes the basic component of our mesoscopic model for replay. We show that the mesoscopic model faithfully captures the statistical structure of individual replayed trajectories in microscopic simulations and in previously reported experimental data. Moreover, compared to the deterministic Romani-Tsodyks model of place-cell dynamics, it exhibits a higher level of variability regarding order, direction and timing of replayed trajectories, which seems biologically more plausible and could be functionally desirable. This variability is the product of a new dynamical regime where metastability emerges from a complex interplay between finite-size fluctuations and local fatigue.

Kuramoto model for populations of quadratic integrate-and-fire neurons with chemical and electrical coupling.

We derive the Kuramoto model (KM) corresponding to a population of weakly coupled, nearly identical quadratic integrate-and-fire (QIF) neurons with both electrical and chemical coupling. The ratio of chemical to electrical coupling determines the phase lag of the characteristic sine coupling function of the KM and critically determines the synchronization properties of the network. We apply our results to uncover the presence of chimera states in two coupled populations of identical QIF neurons. We find that the presence of both electrical and chemical coupling is a necessary condition for chimera states to exist. Finally, we numerically demonstrate that chimera states gradually disappear as coupling strengths cease to be weak.

Low-dimensional firing-rate dynamics for populations of renewal-type spiking neurons.

The macroscopic dynamics of large populations of neurons can be mathematically analyzed using low-dimensional firing-rate or neural-mass models. However, these models fail to capture spike synchronization effects and nonstationary responses of the population activity to rapidly changing stimuli. Here we derive low-dimensional firing-rate models for homogeneous populations of neurons modeled as time-dependent renewal processes. The class of renewal neurons includes integrate-and-fire models driven by white noise and has been frequently used to model neuronal refractoriness and spike synchronization dynamics. The derivation is based on an eigenmode expansion of the associated refractory density equation, which generalizes previous spectral methods for Fokker-Planck equations to arbitrary renewal models. We find a simple relation between the eigenvalues characterizing the timescales of the firing rate dynamics and the Laplace transform of the interspike interval density, for which explicit expressions are available for many renewal models. Retaining only the first eigenmode already yields a reliable low-dimensional approximation of the firing-rate dynamics that captures spike synchronization effects and fast transient dynamics at stimulus onset. We explicitly demonstrate the validity of our model for a large homogeneous population of Poisson neurons with absolute refractoriness and other renewal models that admit an explicit analytical calculation of the eigenvalues. The eigenmode expansion presented here provides a systematic framework for alternative firing-rate models in computational neuroscience based on spiking neuron dynamics with refractoriness.

Exact firing rate model reveals the differential effects of chemical versus electrical synapses in spiking networks.

Chemical and electrical synapses shape the dynamics of neuronal networks. Numerous theoretical studies have investigated how each of these types of synapses contributes to the generation of neuronal oscillations, but their combined effect is less understood. This limitation is further magnified by the impossibility of traditional neuronal mean-field models-also known as firing rate models or firing rate equations-to account for electrical synapses. Here, we introduce a firing rate model that exactly describes the mean-field dynamics of heterogeneous populations of quadratic integrate-and-fire (QIF) neurons with both chemical and electrical synapses. The mathematical analysis of the firing rate model reveals a well-established bifurcation scenario for networks with chemical synapses, characterized by a codimension-2 cusp point and persistent states for strong recurrent excitatory coupling. The inclusion of electrical coupling generally implies neuronal synchrony by virtue of a supercritical Hopf bifurcation. This transforms the cusp scenario into a bifurcation scenario characterized by three codimension-2 points (cusp, Takens-Bogdanov, and saddle-node separatrix loop), which greatly reduces the possibility for persistent states. This is generic for heterogeneous QIF networks with both chemical and electrical couplings. Our results agree with several numerical studies on the dynamics of large networks of heterogeneous spiking neurons with electrical and chemical couplings.

Scale-freeness or partial synchronization in neural mass phase oscillator networks: Pick one of two?

Modeling and interpreting (partial) synchronous neural activity can be a challenge. We illustrate this by deriving the phase dynamics of two seminal neural mass models: the Wilson-Cowan firing rate model and the voltage-based Freeman model. We established that the phase dynamics of these models differed qualitatively due to an attractive coupling in the first and a repulsive coupling in the latter. Using empirical structural connectivity matrices, we determined that the two dynamics cover the functional connectivity observed in resting state activity. We further searched for two pivotal dynamical features that have been reported in many experimental studies: (1) a partial phase synchrony with a possibility of a transition towards either a desynchronized or a (fully) synchronized state; (2) long-term autocorrelations indicative of a scale-free temporal dynamics of phase synchronization. Only the Freeman phase model exhibited scale-free behavior. Its repulsive coupling, however, let the individual phases disperse and did not allow for a transition into a synchronized state. The Wilson-Cowan phase model, by contrast, could switch into a (partially) synchronized state, but it did not generate long-term correlations although being located close to the onset of synchronization, i.e. in its critical regime. That is, the phase-reduced models can display one of the two dynamical features, but not both.

Equivalence of coupled networks and networks with multimodal frequency distributions: Conditions for the bimodal and trimodal case.

Populations of oscillators can display a variety of synchronization patterns depending on the oscillators' intrinsic coupling and the coupling between them. We consider two coupled symmetric (sub)populations with unimodal frequency distributions. If internal and external coupling strengths are identical, a change of variables transforms the system into a single population of oscillators whose natural frequencies are bimodally distributed. Otherwise an additional bifurcation parameter κ enters the dynamics. By using the Ott-Antonsen ansatz, we rigorously prove that κ does not lead to new bifurcations, but that a symmetric two-coupled-population network and a network with a symmetric bimodal frequency distribution are topologically equivalent. Seeking for generalizations, we further analyze a symmetric trimodal network vis-à-vis three coupled symmetric unimodal populations. Here, however, the equivalence with respect to stability, dynamics, and bifurcations of the two systems no longer holds.

Ott-Antonsen attractiveness for parameter-dependent oscillatory systems.

The Ott-Antonsen (OA) ansatz [Ott and Antonsen, Chaos 18, 037113 (2008); Chaos 19, 023117 (2009)] has been widely used to describe large systems of coupled phase oscillators. If the coupling is sinusoidal and if the phase dynamics does not depend on the specific oscillator, then the macroscopic behavior of the systems can be fully described by a low-dimensional dynamics. Does the corresponding manifold remain attractive when introducing an intrinsic dependence between an oscillator's phase and its dynamics by additional, oscillator specific parameters? To answer this, we extended the OA ansatz and proved that parameter-dependent oscillatory systems converge to the OA manifold given certain conditions. Our proof confirms recent numerical findings that already hinted at this convergence. Furthermore, we offer a thorough mathematical underpinning for networks of so-called theta neurons, where the OA ansatz has just been applied. In a final step, we extend our proof by allowing for time-dependent and multi-dimensional parameters as well as for network topologies other than global coupling. This renders the OA ansatz an excellent starting point for the analysis of a broad class of realistic settings.