How single neuron properties shape chaotic dynamics and signal transmission in random neural networks

While most models of randomly connected networks assume nodes with simple dynamics, nodes in realistic highly connected networks, such as neurons in the brain, exhibit intrinsic dynamics over multiple timescales. We analyze how the dynamical properties of nodes (such as single neurons) and recurrent connections interact to shape the effective dynamics in large randomly connected networks. A novel dynamical mean-field theory for strongly connected networks of multi-dimensional rate units shows that the power spectrum of the network activity in the chaotic phase emerges from a nonlinear sharpening of the frequency response function of single units. For the case of two-dimensional rate units with strong adaptation, we find that the network exhibits a state of "resonant chaos", characterized by robust, narrow-band stochastic oscillations. The coherence of stochastic oscillations is maximal at the onset of chaos and their correlation time scales with the adaptation timescale of single units. Surprisingly, the resonance frequency can be predicted from the properties of isolated units, even in the presence of heterogeneity in the adaptation parameters. In the presence of these internally-generated chaotic fluctuations, the transmission of weak, low-frequency signals is strongly enhanced by adaptation, whereas signal transmission is not influenced by adaptation in the non-chaotic regime. Our theoretical framework can be applied to other mechanisms at the level of single nodes, such as synaptic filtering, refractoriness or spike synchronization. These results advance our understanding of the interaction between the dynamics of single units and recurrent connectivity, which is a fundamental step toward the description of biologically realistic network models in the brain, or, more generally, networks of other physical or man-made complex dynamical units

Fluctuations and information filtering in coupled populations of spiking neurons with adaptation

Finite-sized populations of spiking elements are fundamental to brain function, but also used in many areas of physics. Here we present a theory of the dynamics of finite-sized populations of spiking units, based on a quasi-renewal description of neurons with adaptation. We derive an integral equation with colored noise that governs the stochastic dynamics of the population activity in response to time-dependent stimulation and calculate the spectral density in the asynchronous state. We show that systems of coupled populations with adaptation can generate a frequency band in which sensory information is preferentially encoded. The theory is applicable to fully as well as randomly connected networks, and to leaky integrate-and-fire as well as to generalized spiking neurons with adaptation on multiple time scales

Mapping input noise to escape noise in integrate-and-fire neurons: a level-crossing approach

Noise in spiking neurons is commonly modeled by a noisy input current or by generating output spikes stochastically with a voltage-dependent hazard rate (“escape noise”). While input noise lends itself to modeling biophysical noise processes, the phenomenological escape noise is mathematically more tractable. Using the level-crossing theory for differentiable Gaussian processes, we derive an approximate mapping between colored input noise and escape noise in leaky integrate-and-fire neurons. This mapping requires the first-passage-time (FPT) density of an overdamped Brownian particle driven by colored noise with respect to an arbitrarily moving boundary. Starting from the Wiener–Rice series for the FPT density, we apply the second-order decoupling approximation of Stratonovich to the case of moving boundaries and derive a simplified hazard-rate representation that is local in time and numerically efficient. This simplification requires the calculation of the non-stationary auto-correlation function of the level-crossing process: For exponentially correlated input noise (Ornstein–Uhlenbeck process), we obtain an exact formula for the zero-lag auto-correlation as a function of noise parameters, mean membrane potential and its speed, as well as an exponential approximation of the full auto-correlation function. The theory well predicts the FPT and interspike interval densities as well as the population activities obtained from simulations with colored input noise and time-dependent stimulus or boundary. The agreement with simulations is strongly enhanced across the sub- and suprathreshold firing regime compared to a first-order decoupling approximation that neglects correlations between level crossings. The second-order approximation also improves upon a previously proposed theory in the subthreshold regime. Depending on a simplicity-accuracy trade-off, all considered approximations represent useful mappings from colored input noise to escape noise, enabling progress in the theory of neuronal population dynamics.TU Berlin, Open-Access-Mittel – 202

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 of stochastic spiking neurons such as the non-stationary population response to rapidly changing stimuli. Here, we derive low-dimensional firing-rate models for homogeneous populations of general renewal-type neurons, including integrate-and-fire models driven by white noise. Renewal models account for 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, which determine the characteristic time scales of the firing rate dynamics, and the Laplace transform of the interspike interval density or the survival function of the renewal process. Analytical expressions for the Laplace transforms are readily available for many renewal models including the leaky integrate-and-fire model. Retaining only the first eigenmode yields already an adequate 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 here presented eigenmode expansion provides a systematic framework for novel firing-rate models in computational neuroscience based on spiking neuron dynamics with refractoriness.Comment: 24 pages, 7 figure

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 pattern is hippocampal replay, which is critical for memory consolidation. The switchings between replay events and a low-activity state in neural recordings suggests 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 spike noise and network size, and fatigue is explicitly linked to synaptic dynamics. To derive the mesosocpic model, we first consider a homogeneous spiking neural network and follow the temporal coarse-graining approach of Gillespie ("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. This stochastic neural mass model is the basic component of our mesoscopic model for replay. We show that our model faithfully captures the stochastic nature of individual replayed trajectories. Moreover, compared to the deterministic Romani-Tsodyks model of place cell dynamics, it exhibits a higher level of variability in terms of content, direction and timing of replay events, compatible with biological evidence 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.Comment: 43 pages, 8 figure

Patterns of interval correlations in neural oscillators with adaptation

Neural firing is often subject to negative feedback by adaptation currents. These currents can induce strong correlations among the time intervals between spikes. Here we study analytically the interval correlations of a broad class of noisy neural oscillators with spike-triggered adaptation of arbitrary strength and time scale. Our weak-noise theory provides a general relation between the correlations and the phase-response curve (PRC) of the oscillator, proves anti-correlations between neighboring intervals for adapting neurons with type I PRC and identifies a single order parameter that determines the qualitative pattern of correlations. Monotonically decaying or oscillating correlation structures can be related to qualitatively different voltage traces after spiking, which can be explained by the phase plane geometry. A thigh firing rates, the long-term variability of the spike train associated with the cumulative interval correlations becomes small, independent of model details. Our results are verified by comparison with stochastic simulations of the exponential, leaky, and generalized integrate-and-fire models with adaptation