Reconstruction of recurrent synaptic connectivity of thousands of neurons from simulated spiking activity
Yury V. Zaytsev, Abigail Morrison, Moritz Deger
备注：
This is the final version of the manuscript from the publisher which supersedes our original pre-print version. The spike data used in this paper and the code that implements our connectivity reconstruction method are publicly available for download at http://dx.doi.org/10.5281/zenodo.17662 and http://dx.doi.org/10.5281/zenodo.17663 respectively
Dynamics and function of neuronal networks are determined by their synaptic connectivity. Current experimental methods to analyze synaptic network structure on the cellular level, however, cover only small fractions of functional neuronal circuits, typically without a simultaneous record of neuronal spiking activity. Here we present a method for the reconstruction of large recurrent neuronal networks from thousands of parallel spike train recordings. We employ maximum likelihood estimation of a generalized linear model of the spiking activity in continuous time. For this model the point process likelihood is concave, such that a global optimum of the parameters can be obtained by gradient ascent. Previous methods, including those of the same class, did not allow recurrent networks of that order of magnitude to be reconstructed due to prohibitive computational cost and numerical instabilities. We describe a minimal model that is optimized for large networks and an efficient scheme for its parallelized numerical optimization on generic computing clusters. For a simulated balanced random network of 1000 neurons, synaptic connectivity is recovered with a misclassification error rate of less than 1% under ideal conditions. We show that the error rate remains low in a series of example cases under progressively less ideal conditions. Finally, we successfully reconstruct the connectivity of a hidden synfire chain that is embedded in a random network, which requires clustering of the network connectivity to reveal the synfire groups. Our results demonstrate how synaptic connectivity could potentially be inferred from large-scale parallel spike train recordings.
The effect of environmental temperature on neuronal spiking behaviors is investigated by numerically simulating the temperature dependence of spiking threshold of the Hodgkin-Huxley neuron subject to synaptic stimulus. We find that the spiking threshold exhibits a global minimum in a "comfortable temperature" range where spike initiation needs weakest synaptic strength, indicating the occurrence of optimal use of synaptic transmission in neural system. We further explore the biophysical origin of this phenomenon in ion channel gating kinetics and also discuss its possible biological relevance …
Learning in the brain requires complementary mechanisms: potentiation and activity-dependent homeostatic scaling. We introduce synaptic scaling to a biologically-realistic spiking model of neocortex which can learn changes in oscillatory rhythms using STDP, and show that scaling is necessary to balance both positive and negative changes in input from potentiation and atrophy. We discuss some of the issues that arise when considering synaptic scaling in such a model, and show that scaling regulates activity whilst allowing learning to remain unaltered.
Spiking networks that perform probabilistic inference have been proposed both as models of cortical computation and as candidates for solving problems in machine learning. However, the evidence for spike-based computation being in any way superior to non-spiking alternatives remains scarce. We propose that short-term plasticity can provide spiking networks with distinct computational advantages compared to their classical counterparts. In this work, we use networks of leaky integrate-and-fire neurons that are trained to perform both discriminative and generative tasks in their forward and back…
We examine the effects of stochastic input currents on the firing behavior of two excitable neurons coupled with fast excitatory synapses. In such cells (models), typified by the quadratic integrate and fire model, mutual synaptic coupling can cause sustained firing or oscillatory behavior which is necessarily antiphase. Additive Gaussian white noise can transiently terminate the oscillations, hence destroying the stable limit cycle. Further application of the noise may return the system to spiking activity. In a particular noise range, the transition times between the oscillating and the rest…
Coarse-graining microscopic models of biological neural networks to obtain mesoscopic models of neural activities is an essential step towards multi-scale models of the brain. Here, we extend a recent theory for mesoscopic population dynamics with static synapses to the case of dynamic synapses exhibiting short-term plasticity (STP). Under the assumption that spike arrivals at synapses have Poisson statistics, we derive analytically stochastic mean-field dynamics for the effective synaptic coupling between finite-size populations undergoing Tsodyks-Markram STP. The novel mean-field equations a…
Synapses change on multiple timescales, ranging from milliseconds to minutes, due to a combination of both short- and long-term plasticity. Here we develop an extension of the common Generalized Linear Model to infer both short- and long-term changes in the coupling between a pre- and post-synaptic neuron based on observed spiking activity. We model short-term synaptic plasticity using additive effects that depend on the presynaptic spike timing, and we model long-term changes in both synaptic weight and baseline firing rate using point process adaptive smoothing. Using simulations, we first s…
Message passing between components of a distributed physical system is non-instantaneous and contributes to determine the time scales of the emerging collective dynamics like an effective inertia. In biological neuron networks this inertia is due in part to local synaptic filtering of exchanged spikes, and in part to the distribution of the axonal transmission delays. How differently these two kinds of inertia affect the network dynamics is an open issue not yet addressed due to the difficulties in dealing with the non-Markovian nature of synaptic transmission. Here, we develop a mean-field di…
We have added a simplified neuromorphic model of Spike Time Dependent Plasticity (STDP) to the Synapto-dendritic Kernel Adapting Neuron (SKAN). The resulting neuron model is the first to show synaptic encoding of afferent signal to noise ratio in addition to the unsupervised learning of spatio temporal spike patterns. The neuron model is particularly suitable for implementation in digital neuromorphic hardware as it does not use any complex mathematical operations and uses a novel approach to achieve synaptic homeostasis. The neurons noise compensation properties are characterized and tested o…
Sparse coding algorithms trained on natural images can accurately predict the features that excite visual cortical neurons, but it is not known whether such codes can be learned using biologically realistic plasticity rules. We have developed a biophysically motivated spiking network, relying solely on synaptically local information, that can predict the full diversity of V1 simple cell receptive field shapes when trained on natural images. This represents the first demonstration that sparse coding principles, operating within the constraints imposed by cortical architecture, can successfully …
We consider a classical space-clamped Hodgkin-Huxley model neuron stimulated by synaptic excitation and inhibition with conductances represented by Ornstein-Uhlenbeck processes. Using numerical solutions of the stochastic model system obtained by an Euler method, it is found that with excitation only there is a critical value of the steady state excitatory conductance for repetitive spiking without noise and for values of the conductance near the critical value small noise has a powerfully inhibitory effect. For a given level of inhibition there is also a critical value of the steady state exc…
Low-dimensional descriptions of neural network dynamics are an effective tool for bridging different scales of organization of brain structure and function. Recent advances in deriving mean-field descriptions for networks of coupled oscillators have sparked the development of a new generation of neural mass models. Of notable interest are mean-field descriptions of all-to-all coupled quadratic integrate-and-fire (QIF) neurons, which have already seen numerous extensions and applications. These extensions include different forms of short-term adaptation (STA) considered to play an important rol…
Learning synaptic weights of spiking neural network (SNN) models that can reproduce target spike trains from provided neural firing data is a central problem in computational neuroscience and spike-based computing. The discovery of the optimal weight values can be posed as a supervised learning task wherein the weights of the model network are chosen to maximize the similarity between the target spike trains and the model outputs. It is still largely unknown whether optimizing spike train similarity of highly recurrent SNNs produces weight matrices similar to those of the ground truth model. T…
Artificial neural networks normally require precise weights to operate, despite their origins in biological systems, which can be highly variable and noisy. When implementing artificial networks which utilize analog 'synaptic' devices to encode weights, however, inherent limits are placed on the accuracy and precision with which these values can be encoded. In this work, we investigate the effects that inaccurate synapses have on spiking neurons and spiking neural networks. Starting with a mathematical analysis of integrate-and-fire (IF) neurons, including different non-idealities (such as lea…
Efficient path planning and navigation is critical for animals, robotics, logistics and transportation. We study a model in which spatial navigation problems can rapidly be solved in the brain by parallel mental exploration of alternative routes using propagating waves of neural activity. A wave of spiking activity propagates through a hippocampus-like network, altering the synaptic connectivity. The resulting vector field of synaptic change then guides a simulated animal to the appropriate selected target locations. We demonstrate that the navigation problem can be solved using realistic, loc…
We present a method of estimating the gradient of an objective function with respect to the synaptic weights of a spiking neural network. The method works by measuring the fluctuations in the objective function in response to dynamic perturbation of the membrane conductances of the neurons. It is compatible with recurrent networks of conductance-based model neurons with dynamic synapses. The method can be interpreted as a biologically plausible synaptic learning rule, if the dynamic perturbations are generated by a special class of ``empiric'' synapses driven by random spike trains from an ext…
To understand the behavior of a neural circuit it is a presupposition that we have a model of the dynamical system describing this circuit. This model is determined by several parameters, including not only the synaptic weights, but also the parameters of each neuron. Existing works mainly concentrate on either the synaptic weights or the neural parameters. In this paper we present an algorithm to reconstruct all parameters including the synaptic weights of a spiking neuron model. The model based on works of Eugene M. Izhikevich (Izhikevich 2007) consists of two differential equations and cove…
The timing of individual neuronal spikes is essential for biological brains to make fast responses to sensory stimuli. However, conventional artificial neural networks lack the intrinsic temporal coding ability present in biological networks. We propose a spiking neural network model that encodes information in the relative timing of individual neuron spikes. In classification tasks, the output of the network is indicated by the first neuron to spike in the output layer. This temporal coding scheme allows the supervised training of the network with backpropagation, using locally exact derivati…
Information in neural networks is represented as weighted connections, or synapses, between neurons. This poses a problem as the primary computational bottleneck for neural networks is the vector-matrix multiply when inputs are multiplied by the neural network weights. Conventional processing architectures are not well suited for simulating neural networks, often requiring large amounts of energy and time. Additionally, synapses in biological neural networks are not binary connections, but exhibit a nonlinear response function as neurotransmitters are emitted and diffuse between neurons. Inspi…
How can neural networks learn to efficiently represent complex and high-dimensional inputs via local plasticity mechanisms? Classical models of representation learning assume that input weights are learned via pairwise Hebbian-like plasticity. Here, we show that pairwise Hebbian-like plasticity only works under unrealistic requirements on neural dynamics and input statistics. To overcome these limitations, we derive from first principles a learning scheme based on voltage-dependent synaptic plasticity rules. Here, inhibition learns to locally balance excitatory input in individual dendritic co…
HetSyn: Versatile Timescale Integration in Spiking Neural Networks via Heterogeneous Synapses
College of Intelligence and Computing, Tianjin University（智能与计算学院，天津大学）；College of Computer and Information Engineering, Tianjin Normal University（计算机与信息工程学院，天津师范大学）
In many normative theories of synaptic plasticity, weight updates implicitly depend on the chosen parametrization of the weights. This problem relates, for example, to neuronal morphology: synapses which are functionally equivalent in terms of their impact on somatic firing can differ substantially in spine size due to their different positions along the dendritic tree. Classical theories based on Euclidean gradient descent can easily lead to inconsistencies due to such parametrization dependence. The issues are solved in the framework of Riemannian geometry, in which we propose that plasticit…
We analyze the collective dynamics of hierarchically structured networks of densely connected spiking neurons. These networks of sub-networks may represent interactions between cell assemblies or different nuclei in the brain. The dynamical activity pattern that results from these interactions depends on the strength of synaptic coupling between them. Importantly, the overall dynamics of a brain region in the absence of external input, so called ongoing brain activity, has been attributed to the dynamics of such interactions. In our study, two different network scenarios are considered: a syst…
The plasticity of the conduction delay between neurons plays a fundamental role in learning. However, the exact underlying mechanisms in the brain for this modulation is still an open problem. Understanding the precise adjustment of synaptic delays could help us in developing effective brain-inspired computational models in providing aligned insights with the experimental evidence. In this paper, we propose an unsupervised biologically plausible learning rule for adjusting the synaptic delays in spiking neural networks. Then, we provided some mathematical proofs to show that our learning rule …
Laboratory of Biological Modeling, NIDDK/NIH（美国国立糖尿病、消化系统疾病和肾病研究所（NIDDK）/美国国立卫生研究院（NIH）生物建模实验室）
Spiking activity of neurons engaged in learning and performing a task show complex spatiotemporal dynamics. While the output of recurrent network models can learn to perform various tasks, the possible range of recurrent dynamics that emerge after learning remains unknown. Here we show that modifying the recurrent connectivity with a recursive least squares algorithm provides sufficient flexibility for synaptic and spiking rate dynamics of spiking networks to produce a wide range of spatiotemporal activity. We apply the training method to learn arbitrary firing patterns, stabilize irregular sp…
When neural circuits learn to perform a task, it is often the case that there are many sets of synaptic connections that are consistent with the task. However, only a small number of possible solutions are robust to noise in the input and are capable of generalizing their performance of the task to new inputs. Finding such good solutions is an important goal of learning systems in general and neuronal circuits in particular. For systems operating with static inputs and outputs, a well known approach to the problem is the large margin methods such as Support Vector Machines (SVM). By maximizing…
In this paper we present a novel approach to automatically infer parameters of spiking neural networks. Neurons are modelled as timed automata waiting for inputs on a number of different channels (synapses), for a given amount of time (the accumulation period). When this period is over, the current potential value is computed considering current and past inputs. If this potential overcomes a given threshold, the automaton emits a broadcast signal over its output channel , otherwise it restarts another accumulation period. After each emission, the automaton remains inactive for a fixed refracto…
We investigate the efficient transmission and processing of weak, subthreshold signals in a realistic neural medium in the presence of different levels of the underlying noise. Assuming Hebbian weights for maximal synaptic conductances -- that naturally balances the network with excitatory and inhibitory synapses -- and considering short-term synaptic plasticity affecting such conductances, we found different dynamic phases in the system. This includes a memory phase where population of neurons remain synchronized, an oscillatory phase where transitions between different synchronized populatio…
The synaptic connectivity of cortical networks features an overrepresentation of certain wiring motifs compared to simple random-network models. This structure is shaped, in part, by synaptic plasticity that promotes or suppresses connections between neurons depending on their spiking activity. Frequently, theoretical studies focus on how feedforward inputs drive plasticity to create this network structure. We study the complementary scenario of self-organized structure in a recurrent network, with spike timing-dependent plasticity driven by spontaneous dynamics. We develop a self-consistent t…
The background activity of a cortical neural network is modeled by a homogeneous integrate-and-fire network with unreliable inhibitory synapses. Numerical and analytical calculations show that the network relaxes into a stationary state of high attention. The majority of the neurons has a membrane potential just below the threshold; as a consequence the network can react immediately - on the time scale of synaptic transmission- on external pulses. The neurons fire with a low rate and with a broad distribution of interspike intervals. Firing events of the total network are correlated over short…
Synaptic connections in neuronal circuits are modulated by pre- and post-synaptic spiking activity. Heuristic models of this process of synaptic plasticity can provide excellent fits to results from in-vitro experiments in which pre- and post-synaptic spiking is varied in a controlled fashion. However, the plasticity rules inferred from fitting such data are inevitably unstable, in that given constant pre- and post-synaptic activity the synapse will either fully potentiate or depress. This instability can be held in check by adding additional mechanisms, such as homeostasis. Here we consider a…
A Synapse-Threshold Synergistic Learning Approach for Spiking Neural Networks
University of Electronic Science and Technology of China（电子科技大学）；Sichuan Provincial People’s Hospital（四川省人民医院）；Chinese Academy of Medical Sciences（中国医学科学院）；Zhengzhou University（郑州大学）
In computer simulations of spiking neural networks, often it is assumed that every two neurons of the network are connected by a probability of 2\%, 20\% of neurons are inhibitory and 80\% are excitatory. These common values are based on experiments, observations, and trials and errors, but here, I take a different perspective, inspired by evolution, I systematically simulate many networks, each with a different set of parameters, and then I try to figure out what makes the common values desirable. I stimulate networks with pulses and then measure their: dynamic range, dominant frequency of po…
MPI for Intelligent Systems（马克斯·普朗克智能系统研究所）；ETH Zurich（苏黎世联邦理工学院）；MPI for Biological Cybernetics（马克斯·普朗克生物控制论研究所）
This paper suggests a learning-theoretic perspective on how synaptic plasticity benefits global brain functioning. We introduce a model, the selectron, that (i) arises as the fast time constant limit of leaky integrate-and-fire neurons equipped with spiking timing dependent plasticity (STDP) and (ii) is amenable to theoretical analysis. We show that the selectron encodes reward estimates into spikes and that an error bound on spikes is controlled by a spiking margin and the sum of synaptic weights. Moreover, the efficacy of spikes (their usefulness to other reward maximizing selectrons) also d…
Polychronous neural groups are effective structures for the recognition of precise spike-timing patterns but the detection method is an inefficient multi-stage brute force process that works off-line on pre-recorded simulation data. This work presents a new model of polychronous patterns that can capture precise sequences of spikes directly in the neural simulation. In this scheme, each neuron is assigned a randomized code that is used to tag the post-synaptic neurons whenever a spike is transmitted. This creates a polychronous code that preserves the order of pre-synaptic activity and can be …
We study finite-size fluctuations in a network of spiking deterministic neurons coupled with non-uniform synaptic coupling. We generalize a previously developed theory of finite size effects for uniform globally coupled neurons. In the uniform case, mean field theory is well defined by averaging over the network as the number of neurons in the network goes to infinity. However, for nonuniform coupling it is no longer possible to average over the entire network if we are interested in fluctuations at a particular location within the network. We show that if the coupling function approaches a co…
Computing Center（计算中心）；Far Eastern Branch（远东分部）；Russian Academy of Sciences（俄罗斯科学院）
Parallels between the signal processing tasks and biological neurons lead to an understanding of the principles of self-organized optimization of input signal recognition. In the present paper, we discuss such similarities among biological and technical systems. We propose adding the well-known STDP synaptic plasticity rule to direct the weight modification towards the state associated with the maximal difference between background noise and correlated signals. We use the principle of physically constrained weight growth as a basis for such weights' modification control. It is proposed that th…
We analyze a large system of heterogeneous quadratic integrate-and-fire (QIF) neurons with time delayed, all-to-all synaptic coupling. The model is exactly reduced to a system of firing rate equations that is exploited to investigate the existence, stability and bifurcations of fully synchronous, partially synchronous, and incoherent states. In conjunction with this analysis we perform extensive numerical simulations of the original network of QIF neurons, and determine the relation between the macroscopic and microscopic states for partially synchronous states. The results are summarized in t…
The influence of temperature on neuronal excitability is studied by numerical simulations on the spiking threshold characteristics of bushy cells in cochlear nucleus periodically stimulated by synaptic currents. The results reveal that there is a cut-off frequency for the spiking of bushy cell in a specific temperature environment, corresponding to the existence of a critical temperature for the neuron to respond with real spikes to the synaptic stimulus of a given frequency, due to the finiteness of spike width. An optimal temperature range for neuronal spiking is also found for a specific st…
We consider the Watts-Strogatz small-world network consisting of subthreshold neurons which exhibit noise-induced spikings. This neuronal network has adaptive dynamic synaptic strengths governed by the spike-timing-dependent plasticity (STDP). In previous works without STDP, stochastic spike synchronization (SSS) between noise-induced spikings of subthreshold neurons was found to occur in a range of intermediate noise intensities through competition between the constructive and the destructive roles of noise. Here, we investigate the effect of additive STDP on the SSS by varying the noise inte…
In network models of spiking neurons, the joint impact of network structure and synaptic parameters on activity propagation is still an open problem. Here we use an information-theoretical approach to investigate activity propagation in spiking networks with hierarchical modular topology. We observe that optimized pairwise information propagation emerges due to the increase of either (i) the global synaptic strength parameter or (ii) the number of modules in the network, while the network size remains constant. At the population level, information propagation of activity among adjacent modules…
We show that the local Spike Timing-Dependent Plasticity (STDP) rule has the effect of regulating the trans-synaptic weights of loops of any length within a simulated network of neurons. We show that depending on STDP's polarity, functional loops are formed or eliminated in networks driven to normal spiking conditions by random, partially correlated inputs, where functional loops comprise weights that exceed a non-zero threshold. We further prove that STDP is a form of loop-regulating plasticity for the case of a linear network comprising random weights drawn from certain distributions. Thus a…
In an all-to-all network of integrate-fire oscillators in which there is a disorder in the intrinsic firing rates of the neurons, we show that through spike timing-dependent plasticity the links which have the faster oscillators as presynaptic, tend to be strengthened while the links originated from the slow spiking neurons are weakened. The emergent effective flow of directed connections, introduces the faster neurons as the more influent elements in the network and facilitates synchronization by decreasing the synaptic cost for onset of synchronization.
Understanding how recurrent neural circuits can learn to implement dynamical systems is a fundamental challenge in neuroscience. The credit assignment problem, i.e. determining the local contribution of each synapse to the network's global output error, is a major obstacle in deriving biologically plausible local learning rules. Moreover, spiking recurrent networks implementing such tasks should not be hugely costly in terms of number of neurons and spikes, as they often are when adapted from rate models. Finally, these networks should be robust to noise and neural deaths in order to sustain t…
In neuroscience, learning and memory are usually associated to long-term changes of neuronal connectivity. In this context, synaptic plasticity refers to the set of mechanisms driving the dynamics of neuronal connections, called {\em synapses} and represented by a scalar value, the synaptic weight. Spike-Timing Dependent Plasticity (STDP) is a biologically-based model representing the time evolution of the synaptic weight as a functional of the past spiking activity of adjacent neurons. If numerous models of neuronal cells have been proposed in the mathematical literature, few of them include …
We consider the Watts-Strogatz small-world network (SWN) consisting of inhibitory fast spiking Izhikevich interneurons. This inhibitory neuronal population has adaptive dynamic synaptic strengths governed by the inhibitory spike-timing-dependent plasticity (iSTDP). In previous works without iSTDP, fast sparsely synchronized rhythms, associated with diverse cognitive functions, were found to appear in a range of large noise intensities for fixed strong synaptic inhibition strengths. Here, we investigate the effect of iSTDP on fast sparse synchronization (FSS) by varying the noise intensity $D$.…
Neuroscientific theory suggests that dopaminergic neurons broadcast global reward prediction errors to large areas of the brain influencing the synaptic plasticity of the neurons in those regions. We build on this theory to propose a multi-agent learning framework with spiking neurons in the generalized linear model (GLM) formulation as agents, to solve reinforcement learning (RL) tasks. We show that a network of GLM spiking agents connected in a hierarchical fashion, where each spiking agent modulates its firing policy based on local information and a global prediction error, can learn comple…
