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Publication# Topological exploration of artificial neuronal network dynamics

Abstract

One of the paramount challenges in neuroscience is to understand the dynamics of individual neurons and how they give rise to network dynamics when interconnected. Historically, researchers have resorted to graph theory, statistics, and statistical mechanics to describe the spatiotemporal structure of such network dynamics. Our novel approach employs tools from algebraic topology to characterize the global properties of network structure and dynamics.We propose a method based on persistent homology to automatically classify network dynamics using topological features of spaces built from various spike train distances. We investigate the efficacy of our method by simulating activity in three small artificial neural networks with different sets of parameters, giving rise to dynamics that can be classified into four regimes. We then compute three measures of spike train similarity and use persistent homology to extract topological features that are fundamentally different from those used in traditional methods. Our results show that a machine learning classifier trained on these features can accurately predict the regime of the network it was trained on and also generalize to other networks that were not presented during training. Moreover, we demonstrate that using features extracted from multiple spike train distances systematically improves the performance of our method.

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Related concepts (16)

Persistent homology

:See homology for an introduction to the notation.
Persistent homology is a method for computing topological features of a space at different spatial resolutions. More persistent features are detect

Algebraic topology

Algebraic topology is a branch of mathematics that uses tools from abstract algebra to study topological spaces. The basic goal is to find algebraic invariants that classify topological spaces up to

Graph theory

In mathematics, graph theory is the study of graphs, which are mathematical structures used to model pairwise relations between objects. A graph in this context is made up of vertices (also called no

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Wulfram Gerstner, Samuel Pavio Muscinelli, Tilo Schwalger

While most models of randomly connected neural networks assume single-neuron models with simple dynamics, neurons in the brain exhibit complex intrinsic dynamics over multiple timescales. We analyze how the dynamical properties of 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 neurons 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 neurons. For the case of two-dimensional rate neurons 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 neurons, 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 neurons, 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 neural networks. Author summary Biological neural networks are formed by a large number of neurons whose interactions can be extremely complex. Such systems have been successfully studied using random network models, in which the interactions among neurons are assumed to be random. However, the dynamics of single units are usually described using over-simplified models, which might not capture several salient features of real neurons. Here, we show how accounting for richer single-neuron dynamics results in shaping the network dynamics and determines which signals are better transmitted. We focus on adaptation, an important mechanism present in biological neurons that consists in the decrease of their firing rate in response to a sustained stimulus. Our mean-field approach reveals that the presence of adaptation shifts the network into a previously unreported dynamical regime, that we term resonant chaos, in which chaotic activity has a strong oscillatory component. Moreover, we show that this regime is advantageous for the transmission of low-frequency signals. Our work bridges the microscopic dynamics (single neurons) to the macroscopic dynamics (network), and shows how the global signal-transmission properties of the network can be controlled by acting on the single-neuron dynamics. These results paves the way for further developments that include more complex neural mechanisms, and considerably advance our understanding of realistic neural networks.

2019Humans and some other animals are able to perform tasks that require coordination of movements across multiple temporal scales, ranging from hundreds of milliseconds to several seconds. The fast timescale at which neurons naturally operate, on the order of tens of milliseconds, is well-suited to support motor control of rapid movements. In contrast, to coordinate movements on the order of seconds, a neural network should produce reliable dynamics on a similarly âslowâ timescale. Neurons and synapses exhibit biophysical mechanisms whose timescales range from tens of milliseconds to hours, which suggests a possible role of these mechanisms in producing slow reliable dynamics. However, how such mechanisms influence network dynamics is not yet understood. An alternative approach to achieve slow dynamics in a neural network consists in modifying its connectivity structure. Still, the limitations of this approach and in particular to what degree the weights require fine-tuning, remain unclear. Understanding how both the single neuron mechanisms and the connectivity structure might influence the network dynamics
to produce slow timescales is the main goal of this thesis.
We first consider the possibility of obtaining slow dynamics in binary networks by tuning their connectivity. It is known that binary networks can produce sequential dynamics. However, if the sequences consist of random patterns, the typical length of the longest sequence that can be produced grows linearly with the number of units. Here, we show that we can overcome this limitation by carefully designing the sequence structure. More precisely, we obtain a constructive proof that allows to obtain sequences whose length scales exponentially with the number of units. To achieve this however, one needs to exponentially fine-tune the connectivity matrix.
Next, we focus on the interaction between single neuron mechanisms and recurrent dynamics. Particular attention is dedicated to adaptation, which is known to have a broad range of timescales and is therefore particularly interesting for the subject of this thesis. We study the dynamics of a random network with adaptation using mean-field techniques, and we show that the network can enter a state of resonant chaos. Interestingly, the resonance frequency of this state is independent of the connectivity strength and depends only on the properties of the single neuron model. The approach used to study networks with adaptation can also be applied when considering linear rate units with an arbitrary number of auxiliary variables. Based on a qualitative analysis of the mean-field theory for a random network whose neurons are described by a D -dimensional rate model, we conclude that the statistics of the chaotic dynamics are strongly influenced by the single neuron model under investigation.
Using a reservoir computing approach, we show preliminary evidence that slow adaptation can be beneficial when performing tasks that require slow timescales. The positive impact of adaptation on the network performance is particularly strong in the presence of noise. Finally, we propose a network architecture in which the slowing-down effect due to adaptation is combined with a hierarchical structure, with the purpose of efficiently generate sequences that require multiple, hierarchically organized timescales.

The way our brain learns to disentangle complex signals into unambiguous concepts is fascinating but remains largely unknown. There is evidence, however, that hierarchical neural representations play a key role in the cortex. This thesis investigates biologically plausible models of unsupervised learning of hierarchical representations as found in the brain and modern computer vision models. We use computational modeling to address three main questions at the intersection of artificial intelligence (AI) and computational neuroscience.The first question is: What are useful neural representations and when are deep hierarchical representations needed? We approach this point with a systematic study of biologically plausible unsupervised feature learning in a shallow 2-layer networks on digit (MNIST) and object (CIFAR10) classification. Surprisingly, random features support high performance, especially for large hidden layers. When combined with localized receptive fields, random feature networks approach the performance of supervised backpropagation on MNIST, but not on CIFAR10. We suggest that future models of biologically plausible learning should outperform such random feature benchmarks on MNIST, or that such models should be evaluated in different ways.The second question is: How can hierarchical representations be learned with mechanisms supported by neuroscientific evidence? We cover this question by proposing a unifying Hebbian model, inspired by common models of V1 simple and complex cells based on unsupervised sparse coding and temporal invariance learning. In shallow 2-layer networks, our model reproduces learning of simple and complex cell receptive fields, as found in V1. In deeper networks, we stack multiple layers of Hebbian learning but find that it does not yield hierarchical representations of increasing usefulness. From this, we hypothesise that standard Hebbian rules are too constrained to build increasingly useful representations, as observed in higher areas of the visual cortex or deep artificial neural networks.The third question is: Can AI inspire learning models that build deep representations and are still biologically plausible? We address this question by proposing a learning rule that takes inspiration from neuroscience and recent advances in self-supervised deep learning. The proposed rule is Hebbian, i.e. only depends on pre- and post-synaptic neuronal activity, but includes additional local factors, namely predictive dendritic input and widely broadcasted modulation factors. Algorithmically, this rule applies self-supervised contrastive predictive learning to a causal, biological setting using saccades. We find that networks trained with this generalised Hebbian rule build deep hierarchical representations of images, speech and video.We see our modeling as a potential starting point for both, new hypotheses, that can be tested experimentally, and novel AI models that could benefit from added biological realism.