Exact low-dimensional description for fast neural oscillations with low firing rates.

Recently, low-dimensional models of neuronal activity have been exactly derived for large networks of deterministic, quadratic integrate-and-fire (QIF) neurons. Such firing rate models (FRM) describe the emergence of fast collective oscillations (>30 Hz) via the frequency locking of a subset of neurons to the global oscillation frequency. However, the suitability of such models to describe realistic neuronal states is seriously challenged by the fact that during episodes of fast collective oscillations, neuronal discharges are often very irregular and have low firing rates compared to the global oscillation frequency. Here we extend the theory to derive exact FRM for QIF neurons to include noise and show that networks of stochastic neurons displaying irregular discharges at low firing rates during episodes of fast oscillations are governed by exactly the same evolution equations as deterministic networks. Our results reconcile two traditionally confronted views on neuronal synchronization and upgrade the applicability of exact FRM to describe a broad range of biologically realistic neuronal states.

The impact of regional heterogeneity in whole-brain dynamics in the presence of oscillations.

Large variability exists across brain regions in health and disease, considering their cellular and molecular composition, connectivity, and function. Large-scale whole-brain models comprising coupled brain regions provide insights into the underlying dynamics that shape complex patterns of spontaneous brain activity. In particular, biophysically grounded mean-field whole-brain models in the asynchronous regime were used to demonstrate the dynamical consequences of including regional variability. Nevertheless, the role of heterogeneities when brain dynamics are supported by synchronous oscillating state, which is a ubiquitous phenomenon in brain, remains poorly understood. Here, we implemented two models capable of presenting oscillatory behavior with different levels of abstraction: a phenomenological Stuart-Landau model and an exact mean-field model. The fit of these models informed by structural- to functional-weighted MRI signal (T1w/T2w) allowed us to explore the implication of the inclusion of heterogeneities for modeling resting-state fMRI recordings from healthy participants. We found that disease-specific regional functional heterogeneity imposed dynamical consequences within the oscillatory regime in fMRI recordings from neurodegeneration with specific impacts on brain atrophy/structure (Alzheimer's patients). Overall, we found that models with oscillations perform better when structural and functional regional heterogeneities are considered, showing that phenomenological and biophysical models behave similarly at the brink of the Hopf bifurcation.

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.

Exact Mean-Field Theory Explains the Dual Role of Electrical Synapses in Collective Synchronization.

Electrical synapses play a major role in setting up neuronal synchronization, but the precise mechanisms whereby these synapses contribute to synchrony are subtle and remain elusive. To investigate these mechanisms mean-field theories for quadratic integrate-and-fire neurons with electrical synapses have been recently put forward. Still, the validity of these theories is controversial since they assume that the neurons produce unrealistic, symmetric spikes, ignoring the well-known impact of spike shape on synchronization. Here, we show that the assumption of symmetric spikes can be relaxed in such theories. The resulting mean-field equations reveal a dual role of electrical synapses: First, they equalize membrane potentials favoring the emergence of synchrony. Second, electrical synapses act as "virtual chemical synapses," which can be either excitatory or inhibitory depending upon the spike shape. Our results offer a precise mathematical explanation of the intricate effect of electrical synapses in collective synchronization. This reconciles previous theoretical and numerical works, and confirms the suitability of recent low-dimensional mean-field theories to investigate electrically coupled neuronal networks.

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.

Network mechanisms underlying the role of oscillations in cognitive tasks.

Oscillatory activity robustly correlates with task demands during many cognitive tasks. However, not only are the network mechanisms underlying the generation of these rhythms poorly understood, but it is also still unknown to what extent they may play a functional role, as opposed to being a mere epiphenomenon. Here we study the mechanisms underlying the influence of oscillatory drive on network dynamics related to cognitive processing in simple working memory (WM), and memory recall tasks. Specifically, we investigate how the frequency of oscillatory input interacts with the intrinsic dynamics in networks of recurrently coupled spiking neurons to cause changes of state: the neuronal correlates of the corresponding cognitive process. We find that slow oscillations, in the delta and theta band, are effective in activating network states associated with memory recall. On the other hand, faster oscillations, in the beta range, can serve to clear memory states by resonantly driving transient bouts of spike synchrony which destabilize the activity. We leverage a recently derived set of exact mean-field equations for networks of quadratic integrate-and-fire neurons to systematically study the bifurcation structure in the periodically forced spiking network. Interestingly, we find that the oscillatory signals which are most effective in allowing flexible switching between network states are not smooth, pure sinusoids, but rather burst-like, with a sharp onset. We show that such periodic bursts themselves readily arise spontaneously in networks of excitatory and inhibitory neurons, and that the burst frequency can be tuned via changes in tonic drive. Finally, we show that oscillations in the gamma range can actually stabilize WM states which otherwise would not persist.

Kuramoto Model for Excitation-Inhibition-Based Oscillations.

The Kuramoto model (KM) is a theoretical paradigm for investigating the emergence of rhythmic activity in large populations of oscillators. A remarkable example of rhythmogenesis is the feedback loop between excitatory (E) and inhibitory (I) cells in large neuronal networks. Yet, although the EI-feedback mechanism plays a central role in the generation of brain oscillations, it remains unexplored whether the KM has enough biological realism to describe it. Here we derive a two-population KM that fully accounts for the onset of EI-based neuronal rhythms and that, as the original KM, is analytically solvable to a large extent. Our results provide a powerful theoretical tool for the analysis of large-scale neuronal oscillations.

Firing rate equations require a spike synchrony mechanism to correctly describe fast oscillations in inhibitory networks.

Recurrently coupled networks of inhibitory neurons robustly generate oscillations in the gamma band. Nonetheless, the corresponding Wilson-Cowan type firing rate equation for such an inhibitory population does not generate such oscillations without an explicit time delay. We show that this discrepancy is due to a voltage-dependent spike-synchronization mechanism inherent in networks of spiking neurons which is not captured by standard firing rate equations. Here we investigate an exact low-dimensional description for a network of heterogeneous canonical Class 1 inhibitory neurons which includes the sub-threshold dynamics crucial for generating synchronous states. In the limit of slow synaptic kinetics the spike-synchrony mechanism is suppressed and the standard Wilson-Cowan equations are formally recovered as long as external inputs are also slow. However, even in this limit synchronous spiking can be elicited by inputs which fluctuate on a time-scale of the membrane time-constant of the neurons. Our meanfield equations therefore represent an extension of the standard Wilson-Cowan equations in which spike synchrony is also correctly described.

Synchronization scenarios in the Winfree model of coupled oscillators.

Fifty years ago Arthur Winfree proposed a deeply influential mean-field model for the collective synchronization of large populations of phase oscillators. Here we provide a detailed analysis of the model for some special, analytically tractable cases. Adopting the thermodynamic limit, we derive an ordinary differential equation that exactly describes the temporal evolution of the macroscopic variables in the Ott-Antonsen invariant manifold. The low-dimensional model is then thoroughly investigated for a variety of pulse types and sinusoidal phase response curves (PRCs). Two structurally different synchronization scenarios are found, which are linked via the mutation of a Bogdanov-Takens point. From our results, we infer a general rule of thumb relating pulse shape and PRC offset with each scenario. Finally, we compare the exact synchronization threshold with the prediction of the averaging approximation given by the Kuramoto-Sakaguchi model. At the leading order, the discrepancy appears to behave as an odd function of the PRC offset.

Synchrony-induced modes of oscillation of a neural field model.

We investigate the modes of oscillation of heterogeneous ring networks of quadratic integrate-and-fire (QIF) neurons with nonlocal, space-dependent coupling. Perturbations of the equilibrium state with a particular wave number produce transient standing waves with a specific temporal frequency, analogously to those in a tense string. In the neuronal network, the equilibrium corresponds to a spatially homogeneous, asynchronous state. Perturbations of this state excite the network's oscillatory modes, which reflect the interplay of episodes of synchronous spiking with the excitatory-inhibitory spatial interactions. In the thermodynamic limit, an exact low-dimensional neural field model describing the macroscopic dynamics of the network is derived. This allows us to obtain formulas for the Turing eigenvalues of the spatially homogeneous state and hence to obtain its stability boundary. We find that the frequency of each Turing mode depends on the corresponding Fourier coefficient of the synaptic pattern of connectivity. The decay rate instead is identical for all oscillation modes as a consequence of the heterogeneity-induced desynchronization of the neurons. Finally, we numerically compute the spectrum of spatially inhomogeneous solutions branching from the Turing bifurcation, showing that similar oscillatory modes operate in neural bump states and are maintained away from onset.

From Quasiperiodic Partial Synchronization to Collective Chaos in Populations of Inhibitory Neurons with Delay.

Collective chaos is shown to emerge, via a period-doubling cascade, from quasiperiodic partial synchronization in a population of identical inhibitory neurons with delayed global coupling. This system is thoroughly investigated by means of an exact model of the macroscopic dynamics, valid in the thermodynamic limit. The collective chaotic state is reproduced numerically with a finite population, and persists in the presence of weak heterogeneities. Finally, the relationship of the model's dynamics with fast neuronal oscillations is discussed.

Collective synchronization in the presence of reactive coupling and shear diversity.

We analyze the synchronization dynamics of a model obtained from the phase reduction of the mean-field complex Ginzburg-Landau equation with heterogeneity. We present exact results that uncover the role of dissipative and reactive couplings on the synchronization transition when shears and natural frequencies are independently distributed. As it occurs in the purely dissipative case, an excess of shear diversity prevents the onset of synchronization, but this does not hold true if coupling is purely reactive. In this case, the synchronization threshold turns out to depend on the mean of the shear distribution, but not on all the other distribution's moments.

Shear diversity prevents collective synchronization.

Large ensembles of heterogeneous oscillators often exhibit collective synchronization as a result of mutual interactions. If the oscillators have distributed natural frequencies and common shear (or nonisochronicity), the transition from incoherence to collective synchronization is known to occur at large enough values of the coupling strength. However, here we demonstrate that shear diversity cannot be counterbalanced by diffusive coupling leading to synchronization. We present the first analytical results for the Kuramoto model with distributed shear and show that the onset of collective synchronization is impossible if the width of the shear distribution exceeds a precise threshold.

Existence of hysteresis in the Kuramoto model with bimodal frequency distributions.

We investigate the transition to synchronization in the Kuramoto model with bimodal distributions of the natural frequencies. Previous studies have concluded that the model exhibits a hysteretic phase transition if the bimodal distribution is close to a unimodal one due to the shallowness of the central dip. Here we show that proximity to the unimodal-bimodal border does not necessarily imply hysteresis when the width, but not the depth, of the central dip tends to zero. We draw this conclusion from a detailed study of the Kuramoto model with a suitable family of bimodal distributions.

Universal behavior in populations composed of excitable and self-oscillatory elements.

We study the robustness of self-sustained oscillatory activity in a globally coupled ensemble of excitable and oscillatory units. The critical balance to achieve collective self-sustained oscillations is analytically established. We also report a universal scaling function for the ensemble's mean frequency. Our results extend the framework of the "aging transition" [Phys. Rev. Lett. 93, 104101 (2004)] including a broad class of dynamical systems potentially relevant in biology.

Time delay in the Kuramoto model with bimodal frequency distribution.

We investigate the effects of a time-delayed all-to-all coupling scheme in a large population of oscillators with natural frequencies following a bimodal distribution. The regions of parameter space corresponding to synchronized and incoherent solutions are obtained both numerically and analytically for particular frequency distributions. In particular, we find that bimodality introduces a new time scale that results in a quasiperiodic disposition of the regions of incoherence.

Synchronization of two interacting populations of oscillators.

We analyze synchronization between two interacting populations of different phase oscillators. For the important case of asymmetric coupling functions, we find a much richer dynamical behavior compared to that of symmetrically coupled populations of identical oscillators. It includes three types of bistabilities, higher order entrainment, and the existence of states with unusual stability properties. All possible routes to synchronization of the populations are presented and some stability boundaries are obtained analytically. The impact of these findings for neuroscience is discussed.

Anomalous phase synchronization in populations of nonidentical oscillators.

We report the phenomenon of anomalous phase synchronization in interacting oscillator systems with randomly distributed parameters. We show that coupling is first able to enlarge the frequency disorder leading to maximal decoherence for intermediate levels of coupling strength before reaching synchronization. Anomalous synchronization arises when the natural frequency covaries with nonisochronicity and allows for synchronization control by adjustment of system parameters.

Using nonisochronicity to control synchronization in ensembles of nonidentical oscillators.

We investigate the transition to synchronization in ensembles of coupled oscillators with quenched disorder. We find that small coupling is able to increase the frequency disorder and to induce a spread of oscillator frequencies. This new effect of anomalous desynchronization is studied with numerical and analytical means in a large class of systems including Rössler, Lotka-Volterra, Landau-Stuart, and Van-der-Pol oscillators. We show that anomalous effects arise due to an interplay between nonisochronicity and natural frequency of each oscillator and can either increase or inhibit synchronization in the ensemble. This provides a novel possibility to control the synchronization transition in nonidentical systems by suitably distributing the disorder among system parameters. We conjecture that our results are of relevance for biological systems.