Learning spiking neuronal networks with artificial neural networks: neural oscillations.

First-principles-based modelings have been extremely successful in providing crucial insights and predictions for complex biological functions and phenomena. However, they can be hard to build and expensive to simulate for complex living systems. On the other hand, modern data-driven methods thrive at modeling many types of high-dimensional and noisy data. Still, the training and interpretation of these data-driven models remain challenging. Here, we combine the two types of methods to model stochastic neuronal network oscillations. Specifically, we develop a class of artificial neural networks to provide faithful surrogates to the high-dimensional, nonlinear oscillatory dynamics produced by a spiking neuronal network model. Furthermore, when the training data set is enlarged within a range of parameter choices, the artificial neural networks become generalizable to these parameters, covering cases in distinctly different dynamical regimes. In all, our work opens a new avenue for modeling complex neuronal network dynamics with artificial neural networks.

Stress relief as a natural resilience mechanism against depression-like behaviors.

Relief, the appetitive state after the termination of aversive stimuli, is evolutionarily conserved. Understanding the behavioral role of this well-conserved phenomenon and its underlying neurobiological mechanisms are open and important questions. Here, we discover that the magnitude of relief from physical stress strongly correlates with individual resilience to depression-like behaviors in chronic stressed mice. Notably, blocking stress relief causes vulnerability to depression-like behaviors, whereas natural rewards supplied shortly after stress promotes resilience. Stress relief is mediated by reward-related mesolimbic dopamine neurons, which show minute-long, persistent activation after stress termination. Circuitry-wise, activation or inhibition of circuits downstream of the ventral tegmental area during the transient relief period bi-directionally regulates depression resilience. These results reveal an evolutionary function of stress relief in depression resilience and identify the neural substrate mediating this effect. Importantly, our data suggest a behavioral strategy of augmenting positive valence of stress relief with natural rewards to prevent depression.

Multi-band oscillations emerge from a simple spiking network.

In the brain, coherent neuronal activities often appear simultaneously in multiple frequency bands, e.g., as combinations of alpha (8-12 Hz), beta (12.5-30 Hz), and gamma (30-120 Hz) oscillations, among others. These rhythms are believed to underlie information processing and cognitive functions and have been subjected to intense experimental and theoretical scrutiny. Computational modeling has provided a framework for the emergence of network-level oscillatory behavior from the interaction of spiking neurons. However, due to the strong nonlinear interactions between highly recurrent spiking populations, the interplay between cortical rhythms in multiple frequency bands has rarely been theoretically investigated. Many studies invoke multiple physiological timescales (e.g., various ion channels or multiple types of inhibitory neurons) or oscillatory inputs to produce rhythms in multi-bands. Here, we demonstrate the emergence of multi-band oscillations in a simple network consisting of one excitatory and one inhibitory neuronal population driven by constant input. First, we construct a data-driven, Poincaré section theory for robust numerical observations of single-frequency oscillations bifurcating into multiple bands. Then, we develop model reductions of the stochastic, nonlinear, high-dimensional neuronal network to capture the appearance of multi-band dynamics and the underlying bifurcations theoretically. Furthermore, when viewed within the reduced state space, our analysis reveals conserved geometrical features of the bifurcations on low-dimensional dynamical manifolds. These results suggest a simple geometric mechanism behind the emergence of multi-band oscillations without appealing to oscillatory inputs or multiple synaptic or neuronal timescales. Thus, our work points to unexplored regimes of stochastic competition between excitation and inhibition behind the generation of dynamic, patterned neuronal activities.

Multilevel monte carlo for cortical circuit models.

Multilevel Monte Carlo (MLMC) methods aim to speed up computation of statistics from dynamical simulations. MLMC is easy to implement and is sometimes very effective, but its efficacy may depend on the underlying dynamics. We apply MLMC to networks of spiking neurons and assess its effectiveness on prototypical models of cortical circuitry under different conditions. We find that MLMC can be very efficient for computing reliable features, i.e., features of network dynamics that are reproducible upon repeated presentation of the same external forcing. In contrast, MLMC is less effective for complex, internally generated activity. Qualitative explanations are given using concepts from random dynamical systems theory.

A data-informed mean-field approach to mapping of cortical parameter landscapes.

Constraining the many biological parameters that govern cortical dynamics is computationally and conceptually difficult because of the curse of dimensionality. This paper addresses these challenges by proposing (1) a novel data-informed mean-field (MF) approach to efficiently map the parameter space of network models; and (2) an organizing principle for studying parameter space that enables the extraction biologically meaningful relations from this high-dimensional data. We illustrate these ideas using a large-scale network model of the Macaque primary visual cortex. Of the 10-20 model parameters, we identify 7 that are especially poorly constrained, and use the MF algorithm in (1) to discover the firing rate contours in this 7D parameter cube. Defining a "biologically plausible" region to consist of parameters that exhibit spontaneous Excitatory and Inhibitory firing rates compatible with experimental values, we find that this region is a slightly thickened codimension-1 submanifold. An implication of this finding is that while plausible regimes depend sensitively on parameters, they are also robust and flexible provided one compensates appropriately when parameters are varied. Our organizing principle for conceptualizing parameter dependence is to focus on certain 2D parameter planes that govern lateral inhibition: Intersecting these planes with the biologically plausible region leads to very simple geometric structures which, when suitably scaled, have a universal character independent of where the intersections are taken. In addition to elucidating the geometry of the plausible region, this invariance suggests useful approximate scaling relations. Our study offers, for the first time, a complete characterization of the set of all biologically plausible parameters for a detailed cortical model, which has been out of reach due to the high dimensionality of parameter space.

Model Reduction Captures Stochastic Gamma Oscillations on Low-Dimensional Manifolds.

Gamma frequency oscillations (25-140 Hz), observed in the neural activities within many brain regions, have long been regarded as a physiological basis underlying many brain functions, such as memory and attention. Among numerous theoretical and computational modeling studies, gamma oscillations have been found in biologically realistic spiking network models of the primary visual cortex. However, due to its high dimensionality and strong non-linearity, it is generally difficult to perform detailed theoretical analysis of the emergent gamma dynamics. Here we propose a suite of Markovian model reduction methods with varying levels of complexity and apply it to spiking network models exhibiting heterogeneous dynamical regimes, ranging from nearly homogeneous firing to strong synchrony in the gamma band. The reduced models not only successfully reproduce gamma oscillations in the full model, but also exhibit the same dynamical features as we vary parameters. Most remarkably, the invariant measure of the coarse-grained Markov process reveals a two-dimensional surface in state space upon which the gamma dynamics mainly resides. Our results suggest that the statistical features of gamma oscillations strongly depend on the subthreshold neuronal distributions. Because of the generality of the Markovian assumptions, our dimensional reduction methods offer a powerful toolbox for theoretical examinations of other complex cortical spatio-temporal behaviors observed in both neurophysiological experiments and numerical simulations.