Recurrent Networks Of Spiking Neurons Research Articles

Efficient coding in biophysically realistic excitatory-inhibitory spiking networks.

The principle of efficient coding posits that sensory cortical networks are designed to encode maximal sensory information with minimal metabolic cost. Despite the major influence of efficient coding in neuroscience, it has remained unclear whether fundamental empirical properties of neural network activity can be explained solely based on this normative principle. Here, we derive the structural, coding, and biophysical properties of excitatory-inhibitory recurrent networks of spiking neurons that emerge directly from imposing that the network minimizes an instantaneous loss function and a time-averaged performance measure enacting efficient coding. We assumed that the network encodes a number of independent stimulus features varying with a time scale equal to the membrane time constant of excitatory and inhibitory neurons. The optimal network has biologically-plausible biophysical features, including realistic integrate-and-fire spiking dynamics, spike-triggered adaptation, and a non-specific excitatory external input. The excitatory-inhibitory recurrent connectivity between neurons with similar stimulus tuning implements feature-specific competition, similar to that recently found in visual cortex. Networks with unstructured connectivity cannot reach comparable levels of coding efficiency. The optimal ratio of excitatory vs inhibitory neurons and the ratio of mean inhibitory-to-inhibitory vs excitatory-to-inhibitory connectivity are comparable to those of cortical sensory networks. The efficient network solution exhibits an instantaneous balance between excitation and inhibition. The network can perform efficient coding even when external stimuli vary over multiple time scales. Together, these results suggest that key properties of biological neural networks may be accounted for by efficient coding.

Co-existence of synaptic plasticity and metastable dynamics in a spiking model of cortical circuits.

Evidence for metastable dynamics and its role in brain function is emerging at a fast pace and is changing our understanding of neural coding by putting an emphasis on hidden states of transient activity. Clustered networks of spiking neurons have enhanced synaptic connections among groups of neurons forming structures called cell assemblies; such networks are capable of producing metastable dynamics that is in agreement with many experimental results. However, it is unclear how a clustered network structure producing metastable dynamics may emerge from a fully local plasticity rule, i.e., a plasticity rule where each synapse has only access to the activity of the neurons it connects (as opposed to the activity of other neurons or other synapses). Here, we propose a local plasticity rule producing ongoing metastable dynamics in a deterministic, recurrent network of spiking neurons. The metastable dynamics co-exists with ongoing plasticity and is the consequence of a self-tuning mechanism that keeps the synaptic weights close to the instability line where memories are spontaneously reactivated. In turn, the synaptic structure is stable to ongoing dynamics and random perturbations, yet it remains sufficiently plastic to remap sensory representations to encode new sets of stimuli. Both the plasticity rule and the metastable dynamics scale well with network size, with synaptic stability increasing with the number of neurons. Overall, our results show that it is possible to generate metastable dynamics over meaningful hidden states using a simple but biologically plausible plasticity rule which co-exists with ongoing neural dynamics.

Fast learning without synaptic plasticity in spiking neural networks

Spiking neural networks are of high current interest, both from the perspective of modelling neural networks of the brain and for porting their fast learning capability and energy efficiency into neuromorphic hardware. But so far we have not been able to reproduce fast learning capabilities of the brain in spiking neural networks. Biological data suggest that a synergy of synaptic plasticity on a slow time scale with network dynamics on a faster time scale is responsible for fast learning capabilities of the brain. We show here that a suitable orchestration of this synergy between synaptic plasticity and network dynamics does in fact reproduce fast learning capabilities of generic recurrent networks of spiking neurons. This points to the important role of recurrent connections in spiking networks, since these are necessary for enabling salient network dynamics. We show more specifically that the proposed synergy enables synaptic weights to encode more general information such as priors and task structures, since moment-to-moment processing of new information can be delegated to the network dynamics.

Accurate online training of dynamical spiking neural networks through Forward Propagation Through Time

With recent advances in learning algorithms, recurrent networks of spiking neurons are achieving performance that is competitive with vanilla recurrent neural networks. However, these algorithms are limited to small networks of simple spiking neurons and modest-length temporal sequences, as they impose high memory requirements, have difficulty training complex neuron models and are incompatible with online learning. Here, we show how the recently developed Forward-Propagation Through Time (FPTT) learning combined with novel liquid time-constant spiking neurons resolves these limitations. Applying FPTT to networks of such complex spiking neurons, we demonstrate online learning of exceedingly long sequences while outperforming current online methods and approaching or outperforming offline methods on temporal classification tasks. The efficiency and robustness of FPTT enable us to directly train a deep and performant spiking neural network for joint object localization and recognition, demonstrating the ability to train large-scale dynamic and complex spiking neural network architectures. Memory efficient online training of recurrent spiking neural networks without compromising accuracy is an open challenge in neuromorphic computing. Yin and colleagues demonstrate that training a recurrent neural network consisting of so-called liquid time-constant spiking neurons using an algorithm called Forward-Propagation Through Time allows for online learning and state-of-the-art performance at a reduced computational cost compared with existing approaches.

Organization and Priming of Long-term Memory Representations with Two-phase Plasticity

Background / IntroductionIn recurrent neural networks in the brain, memories are represented by so-called Hebbian cell assemblies. Such assemblies are groups of neurons with particularly strong synaptic connections formed by synaptic plasticity and consolidated by synaptic tagging and capture (STC). To link these synaptic mechanisms to long-term memory on the level of cognition and behavior, their functional implications on the level of neural networks have to be understood.MethodsWe employ a biologically detailed recurrent network of spiking neurons featuring synaptic plasticity and STC to model the learning and consolidation of long-term memory representations. Using this, we investigate the effects of different organizational paradigms, and of priming stimulation, on the functionality of multiple memory representations. We quantify these effects by the spontaneous activation of memory representations driven by background noise.ResultsWe find that the learning order of the memory representations significantly biases the likelihood of activation towards more recently learned representations, and that hub-like overlap structure counters this effect. We identify long-term depression as the mechanism underlying these findings. Finally, we demonstrate that STC has functional consequences for the interaction of long-term memory representations: 1. intermediate consolidation in between learning the individual representations strongly alters the previously described effects, and 2. STC enables the priming of a long-term memory representation on a timescale of minutes to hours.ConclusionOur findings show how synaptic and neuronal mechanisms can provide an explanatory basis for known cognitive effects.

Sequence learning, prediction, and replay in networks of spiking neurons

Sequence learning, prediction and replay have been proposed to constitute the universal computations performed by the neocortex. The Hierarchical Temporal Memory (HTM) algorithm realizes these forms of computation. It learns sequences in an unsupervised and continuous manner using local learning rules, permits a context specific prediction of future sequence elements, and generates mismatch signals in case the predictions are not met. While the HTM algorithm accounts for a number of biological features such as topographic receptive fields, nonlinear dendritic processing, and sparse connectivity, it is based on abstract discrete-time neuron and synapse dynamics, as well as on plasticity mechanisms that can only partly be related to known biological mechanisms. Here, we devise a continuous-time implementation of the temporal-memory (TM) component of the HTM algorithm, which is based on a recurrent network of spiking neurons with biophysically interpretable variables and parameters. The model learns high-order sequences by means of a structural Hebbian synaptic plasticity mechanism supplemented with a rate-based homeostatic control. In combination with nonlinear dendritic input integration and local inhibitory feedback, this type of plasticity leads to the dynamic self-organization of narrow sequence-specific subnetworks. These subnetworks provide the substrate for a faithful propagation of sparse, synchronous activity, and, thereby, for a robust, context specific prediction of future sequence elements as well as for the autonomous replay of previously learned sequences. By strengthening the link to biology, our implementation facilitates the evaluation of the TM hypothesis based on experimentally accessible quantities. The continuous-time implementation of the TM algorithm permits, in particular, an investigation of the role of sequence timing for sequence learning, prediction and replay. We demonstrate this aspect by studying the effect of the sequence speed on the sequence learning performance and on the speed of autonomous sequence replay.

A robust model of Stimulus-Specific Adaptation validated on neuromorphic hardware

Stimulus-Specific Adaptation (SSA) to repetitive stimulation is a phenomenon that has been observed across many different species and in several brain sensory areas. It has been proposed as a computational mechanism, responsible for separating behaviorally relevant information from the continuous stream of sensory information. Although SSA can be induced and measured reliably in a wide variety of conditions, the network details and intracellular mechanisms giving rise to SSA still remain unclear. Recent computational studies proposed that SSA could be associated with a fast and synchronous neuronal firing phenomenon called Population Spikes (PS). Here, we test this hypothesis using a mean-field rate model and corroborate it using a neuromorphic hardware. As the neuromorphic circuits used in this study operate in real-time with biologically realistic time constants, they can reproduce the same dynamics observed in biological systems, together with the exploration of different connectivity schemes, with complete control of the system parameter settings. Besides, the hardware permits the iteration of multiple experiments over many trials, for extended amounts of time and without losing the networks and individual neural processes being studied. Following this “neuromorphic engineering” approach, we therefore study the PS hypothesis in a biophysically inspired recurrent networks of spiking neurons and evaluate the role of different linear and non-linear dynamic computational primitives such as spike-frequency adaptation or short-term depression (STD). We compare both the theoretical mean-field model of SSA and PS to previously obtained experimental results in the area of novelty detection and observe its behavior on its neuromorphic physical equivalent model. We show how the approach proposed can be extended to other computational neuroscience modelling efforts for understanding high-level phenomena in mechanistic models.

Efficient and robust coding in heterogeneous recurrent networks.

Cortical networks show a large heterogeneity of neuronal properties. However, traditional coding models have focused on homogeneous populations of excitatory and inhibitory neurons. Here, we analytically derive a class of recurrent networks of spiking neurons that close to optimally track a continuously varying input online, based on two assumptions: 1) every spike is decoded linearly and 2) the network aims to reduce the mean-squared error between the input and the estimate. From this we derive a class of predictive coding networks, that unifies encoding and decoding and in which we can investigate the difference between homogeneous networks and heterogeneous networks, in which each neurons represents different features and has different spike-generating properties. We find that in this framework, 'type 1' and 'type 2' neurons arise naturally and networks consisting of a heterogeneous population of different neuron types are both more efficient and more robust against correlated noise. We make two experimental predictions: 1) we predict that integrators show strong correlations with other integrators and resonators are correlated with resonators, whereas the correlations are much weaker between neurons with different coding properties and 2) that 'type 2' neurons are more coherent with the overall network activity than 'type 1' neurons.

Characteristics of sequential activity in networks with temporally asymmetric Hebbian learning

Sequential activity has been observed in multiple neuronal circuits across species, neural structures, and behaviors. It has been hypothesized that sequences could arise from learning processes. However, it is still unclear whether biologically plausible synaptic plasticity rules can organize neuronal activity to form sequences whose statistics match experimental observations. Here, we investigate temporally asymmetric Hebbian rules in sparsely connected recurrent rate networks and develop a theory of the transient sequential activity observed after learning. These rules transform a sequence of random input patterns into synaptic weight updates. After learning, recalled sequential activity is reflected in the transient correlation of network activity with each of the stored input patterns. Using mean-field theory, we derive a low-dimensional description of the network dynamics and compute the storage capacity of these networks. Multiple temporal characteristics of the recalled sequential activity are consistent with experimental observations. We find that the degree of sparseness of the recalled sequences can be controlled by nonlinearities in the learning rule. Furthermore, sequences maintain robust decoding, but display highly labile dynamics, when synaptic connectivity is continuously modified due to noise or storage of other patterns, similar to recent observations in hippocampus and parietal cortex. Finally, we demonstrate that our results also hold in recurrent networks of spiking neurons with separate excitatory and inhibitory populations.

A solution to the learning dilemma for recurrent networks of spiking neurons

Recurrently connected networks of spiking neurons underlie the astounding information processing capabilities of the brain. Yet in spite of extensive research, how they can learn through synaptic plasticity to carry out complex network computations remains unclear. We argue that two pieces of this puzzle were provided by experimental data from neuroscience. A mathematical result tells us how these pieces need to be combined to enable biologically plausible online network learning through gradient descent, in particular deep reinforcement learning. This learning method–called e-prop–approaches the performance of backpropagation through time (BPTT), the best-known method for training recurrent neural networks in machine learning. In addition, it suggests a method for powerful on-chip learning in energy-efficient spike-based hardware for artificial intelligence.

STDP Forms Associations between Memory Traces in Networks of Spiking Neurons.

Memory traces and associations between them are fundamental for cognitive brain function. Neuron recordings suggest that distributed assemblies of neurons in the brain serve as memory traces for spatial information, real-world items, and concepts. However, there is conflicting evidence regarding neural codes for associated memory traces. Some studies suggest the emergence of overlaps between assemblies during an association, while others suggest that the assemblies themselves remain largely unchanged and new assemblies emerge as neural codes for associated memory items. Here we study the emergence of neural codes for associated memory items in a generic computational model of recurrent networks of spiking neurons with a data-constrained rule for spike-timing-dependent plasticity. The model depends critically on 2 parameters, which control the excitability of neurons and the scale of initial synaptic weights. By modifying these 2 parameters, the model can reproduce both experimental data from the human brain on the fast formation of associations through emergent overlaps between assemblies, and rodent data where new neurons are recruited to encode the associated memories. Hence, our findings suggest that the brain can use both of these 2 neural codes for associations, and dynamically switch between them during consolidation.

Self-Consistent Scheme for Spike-Train Power Spectra in Heterogeneous Sparse Networks.

Recurrent networks of spiking neurons can be in an asynchronous state characterized by low or absent cross-correlations and spike statistics which resemble those of cortical neurons. Although spatial correlations are negligible in this state, neurons can show pronounced temporal correlations in their spike trains that can be quantified by the autocorrelation function or the spike-train power spectrum. Depending on cellular and network parameters, correlations display diverse patterns (ranging from simple refractory-period effects and stochastic oscillations to slow fluctuations) and it is generally not well-understood how these dependencies come about. Previous work has explored how the single-cell correlations in a homogeneous network (excitatory and inhibitory integrate-and-fire neurons with nearly balanced mean recurrent input) can be determined numerically from an iterative single-neuron simulation. Such a scheme is based on the fact that every neuron is driven by the network noise (i.e., the input currents from all its presynaptic partners) but also contributes to the network noise, leading to a self-consistency condition for the input and output spectra. Here we first extend this scheme to homogeneous networks with strong recurrent inhibition and a synaptic filter, in which instabilities of the previous scheme are avoided by an averaging procedure. We then extend the scheme to heterogeneous networks in which (i) different neural subpopulations (e.g., excitatory and inhibitory neurons) have different cellular or connectivity parameters; (ii) the number and strength of the input connections are random (Erdős-Rényi topology) and thus different among neurons. In all heterogeneous cases, neurons are lumped in different classes each of which is represented by a single neuron in the iterative scheme; in addition, we make a Gaussian approximation of the input current to the neuron. These approximations seem to be justified over a broad range of parameters as indicated by comparison with simulation results of large recurrent networks. Our method can help to elucidate how network heterogeneity shapes the asynchronous state in recurrent neural networks.

An Online Structural Plasticity Rule for Generating Better Reservoirs.

In this letter, we propose a novel neuro-inspired low-resolution online unsupervised learning rule to train the reservoir or liquid of liquid state machines. The liquid is a sparsely interconnected huge recurrent network of spiking neurons. The proposed learning rule is inspired from structural plasticity and trains the liquid through formating and eliminating synaptic connections. Hence, the learning involves rewiring of the reservoir connections similar to structural plasticity observed in biological neural networks. The network connections can be stored as a connection matrix and updated in memory by using address event representation (AER) protocols, which are generally employed in neuromorphic systems. On investigating the pairwise separation property, we find that trained liquids provide 1.36 0.18times more interclass separation while retaining similar intraclass separation as compared to random liquids. Moreover, analysis of the linear separation property reveals that trained liquids are 2.05 0.27times better than random liquids. Furthermore, we show that our liquids are able to retain the generalization ability and generality of random liquids. A memory analysis shows that trained liquids have 83.67 5.79ms longer fading memory than random liquids, which have shown 92.8 5.03ms fading memory for a particular type of spike train inputs. We also throw some light on the dynamics of the evolution of recurrent connections within the liquid. Moreover, compared to separation-driven synaptic modification', a recently proposed algorithm for iteratively refining reservoirs, our learning rule provides 9.30%, 15.21%, and 12.52% more liquid separations and 2.8%, 9.1%, and 7.9% better classification accuracies for 4, 8, and 12 class pattern recognition tasks, respectively.

Real time unsupervised learning of visual stimuli in neuromorphic VLSI systems.

Neuromorphic chips embody computational principles operating in the nervous system, into microelectronic devices. In this domain it is important to identify computational primitives that theory and experiments suggest as generic and reusable cognitive elements. One such element is provided by attractor dynamics in recurrent networks. Point attractors are equilibrium states of the dynamics (up to fluctuations), determined by the synaptic structure of the network; a ‘basin’ of attraction comprises all initial states leading to a given attractor upon relaxation, hence making attractor dynamics suitable to implement robust associative memory. The initial network state is dictated by the stimulus, and relaxation to the attractor state implements the retrieval of the corresponding memorized prototypical pattern. In a previous work we demonstrated that a neuromorphic recurrent network of spiking neurons and suitably chosen, fixed synapses supports attractor dynamics. Here we focus on learning: activating on-chip synaptic plasticity and using a theory-driven strategy for choosing network parameters, we show that autonomous learning, following repeated presentation of simple visual stimuli, shapes a synaptic connectivity supporting stimulus-selective attractors. Associative memory develops on chip as the result of the coupled stimulus-driven neural activity and ensuing synaptic dynamics, with no artificial separation between learning and retrieval phases.

Slow fluctuations in recurrent networks of spiking neurons.

Networks of fast nonlinear elements may display slow fluctuations if interactions are strong. We find a transition in the long-term variability of a sparse recurrent network of perfect integrate-and-fire neurons at which the Fano factor switches from zero to infinity and the correlation time is minimized. This corresponds to a bifurcation in a linear map arising from the self-consistency of temporal input and output statistics. More realistic neural dynamics with a leak current and refractory period lead to smoothed transitions and modified critical couplings that can be theoretically predicted.

Distribution of orientation selectivity in recurrent networks of spiking neurons with different random topologies.

Neurons in the primary visual cortex are more or less selective for the orientation of a light bar used for stimulation. A broad distribution of individual grades of orientation selectivity has in fact been reported in all species. A possible reason for emergence of broad distributions is the recurrent network within which the stimulus is being processed. Here we compute the distribution of orientation selectivity in randomly connected model networks that are equipped with different spatial patterns of connectivity. We show that, for a wide variety of connectivity patterns, a linear theory based on firing rates accurately approximates the outcome of direct numerical simulations of networks of spiking neurons. Distance dependent connectivity in networks with a more biologically realistic structure does not compromise our linear analysis, as long as the linearized dynamics, and hence the uniform asynchronous irregular activity state, remain stable. We conclude that linear mechanisms of stimulus processing are indeed responsible for the emergence of orientation selectivity and its distribution in recurrent networks with functionally heterogeneous synaptic connectivity.

Structured chaos shapes spike-response noise entropy in balanced neural networks.

Large networks of sparsely coupled, excitatory and inhibitory cells occur throughout the brain. For many models of these networks, a striking feature is that their dynamics are chaotic and thus, are sensitive to small perturbations. How does this chaos manifest in the neural code? Specifically, how variable are the spike patterns that such a network produces in response to an input signal? To answer this, we derive a bound for a general measure of variability—spike-train entropy. This leads to important insights on the variability of multi-cell spike pattern distributions in large recurrent networks of spiking neurons responding to fluctuating inputs. The analysis is based on results from random dynamical systems theory and is complemented by detailed numerical simulations. We find that the spike pattern entropy is an order of magnitude lower than what would be extrapolated from single cells. This holds despite the fact that network coupling becomes vanishingly sparse as network size grows—a phenomenon that depends on “extensive chaos,” as previously discovered for balanced networks without stimulus drive. Moreover, we show how spike pattern entropy is controlled by temporal features of the inputs. Our findings provide insight into how neural networks may encode stimuli in the presence of inherently chaotic dynamics.

Alternation of up and down states at a dynamical phase-transition of a neural network with spatiotemporal attractors

Complex collective activity emerges spontaneously in cortical circuits in vivo and in vitro, such as alternation of up and down states, precise spatiotemporal patterns replay, and power law scaling of neural avalanches. We focus on such critical features observed in cortical slices. We study spontaneous dynamics emerging in noisy recurrent networks of spiking neurons with sparse structured connectivity. The emerging spontaneous dynamics is studied, in presence of noise, with fixed connections. Note that no short-term synaptic depression is used. Two different regimes of spontaneous activity emerge changing the connection strength or noise intensity: a low activity regime, characterized by a nearly exponential distribution of firing rates with a maximum at rate zero, and a high activity regime, characterized by a nearly Gaussian distribution peaked at a high rate for high activity, with long-lasting replay of stored patterns. Between this two regimes, a transition region is observed, where firing rates show a bimodal distribution, with alternation of up and down states. In this region, one observes neuronal avalanches exhibiting power laws in size and duration, and a waiting time distribution between successive avalanches which shows a non-monotonic behavior. During periods of high activity (up states) consecutive avalanches are correlated, since they are part of a short transient replay initiated by noise focusing, and waiting times show a power law distribution. One can think at this critical dynamics as a reservoire of dynamical patterns for memory functions.

Stochastic variational learning in recurrent spiking networks.

The ability to learn and perform statistical inference with biologically plausible recurrent networks of spiking neurons is an important step toward understanding perception and reasoning. Here we derive and investigate a new learning rule for recurrent spiking networks with hidden neurons, combining principles from variational learning and reinforcement learning. Our network defines a generative model over spike train histories and the derived learning rule has the form of a local Spike Timing Dependent Plasticity rule modulated by global factors (neuromodulators) conveying information about “novelty” on a statistically rigorous ground. Simulations show that our model is able to learn both stationary and non-stationary patterns of spike trains. We also propose one experiment that could potentially be performed with animals in order to test the dynamics of the predicted novelty signal.

Emergence of Connectivity Motifs in Networks of Model Neurons with Short- and Long-Term Plastic Synapses

Recent experimental data from the rodent cerebral cortex and olfactory bulb indicate that specific connectivity motifs are correlated with short-term dynamics of excitatory synaptic transmission. It was observed that neurons with short-term facilitating synapses form predominantly reciprocal pairwise connections, while neurons with short-term depressing synapses form predominantly unidirectional pairwise connections. The cause of these structural differences in excitatory synaptic microcircuits is unknown. We show that these connectivity motifs emerge in networks of model neurons, from the interactions between short-term synaptic dynamics (SD) and long-term spike-timing dependent plasticity (STDP). While the impact of STDP on SD was shown in simultaneous neuronal pair recordings in vitro, the mutual interactions between STDP and SD in large networks are still the subject of intense research. Our approach combines an SD phenomenological model with an STDP model that faithfully captures long-term plasticity dependence on both spike times and frequency. As a proof of concept, we first simulate and analyze recurrent networks of spiking neurons with random initial connection efficacies and where synapses are either all short-term facilitating or all depressing. For identical external inputs to the network, and as a direct consequence of internally generated activity, we find that networks with depressing synapses evolve unidirectional connectivity motifs, while networks with facilitating synapses evolve reciprocal connectivity motifs. We then show that the same results hold for heterogeneous networks, including both facilitating and depressing synapses. This does not contradict a recent theory that proposes that motifs are shaped by external inputs, but rather complements it by examining the role of both the external inputs and the internally generated network activity. Our study highlights the conditions under which SD-STDP might explain the correlation between facilitation and reciprocal connectivity motifs, as well as between depression and unidirectional motifs.