Alpha rhythm emerges from large-scale networks of realistically coupled multicompartmental model cortical neurons.

Conical pyramidal and stellate neurons were simulated using the GENESIS simulation package. Model neurons were leaky integrate-and-fire and consisted of from four to nine passive compartments. Neurophysiological measurements, based on single-cell recordings and patch-clamp experiments, provided estimations for the simulation of cortical neurons: transmitter-activated conductances, passive membrane time constants and axonal delays. Network connectivity was generated using a previously described probabilistic scheme based on known cortical histology, in which the probability of connections forming between one neuron and another fell off monotonically with increasing inter-cellular separation. Simulations of up to 6400 cortical neurons, approaching the scale of an individual cortical column, confirmed previous findings with smaller networks. Limit-cycle behaviour emerged in the network, in the frequency in the range of the mammalian alpha and beta rhythms (8-20 Hz). Contrary to expectation, near-linear relationships were found between the mean soma membrane potential and and neuronal firing probability. Some of the implications for cortical information processing, in particular the dynamical interactions between the neuronal and larger scales, are discussed.     

Burst synchrony patterns in hippocampal pyramidal cell model networks

Types of. mechanisms for and stability of synchrony are discussed in the context of two-compartment CA3 pyramidal cell and interneuron model networks. We show how the strength and timing of inhibitory and excitatory synaptic inputs work together to produce either perfectly synchronized or nearly synchronized oscillations, across different burst or spiking modes of firing. The analysis shows how excitatory inputs tend to desynchronize cells, and how common, slowly decaying inhibition can be used to synchronize them. We also introduce the concept of 'equivalent networks' in which networks with different architectures and synaptic connections display identical firing patterns.     

Computing and stability in cortical networks

Cortical neurons are predominantly excitatory and highly interconnected. In spite of this, the cortex is remarkably stable: normal brains do not exhibit the kind of runaway excitation one might expect of such a system. How does the cortex maintain stability in the face of this massive excitatory feedback? More importantly, how does it do so during computations, which necessarily involve elevated firing rates? Here we address these questions in the context of attractor networks-networks that exhibit multiple stable states, or memories. We find that such networks can be stabilized at the relatively low firing rates observed in vivo if two conditions are met: (1) the background state, where all neurons are firing at low rates, is inhibition dominated, and (2) the fraction of neurons involved in a memory is above some threshold, so that there is sufficient coupling between the memory neurons and the background. This allows "dynamical stabilization" of the attractors, meaning feedback from the pool of background neurons stabilizes what would otherwise be an unstable state. We suggest that dynamical stabilization may be a strategy used for a broad range of computations, not just those involving attractors.     

Center-crossing recurrent neural networks for the evolution of rhythmic behavior

A center-crossing recurrent neural network is one in which the null-(hyper)surfaces of each neuron intersect at their exact centers of symmetry, ensuring that each neuron's activation function is centered over the range of net inputs that it receives. We demonstrate that relative to a random initial population, seeding the initial population of an evolutionary search with center-crossing networks significantly improves both the frequency and the speed with which high-fitness oscillatory circuits evolve on a simple walking task. The improvement is especially striking at low mutation variances. Our results suggest that seeding with center-crossing networks may often be beneficial, since a wider range of dynamics is more likely to be easily accessible from a population of center-crossing networks than from a population of random networks.     

The high-conductance state of cortical networks

We studied the dynamics of large networks of spiking neurons with conductance-based (nonlinear) synapses and compared them to networks with current-based (linear) synapses. For systems with sparse and inhibition-dominated recurrent connectivity, weak external inputs induced asynchronous irregular firing at low rates. Membrane potentials fluctuated a few millivolts below threshold, and membrane conductances were increased by a factor 2 to 5 with respect to the resting state. This combination of parameters characterizes the ongoing spiking activity typically recorded in the cortex in vivo. Many aspects of the asynchronous irregular state in conductance-based networks could be sufficiently well characterized with a simple numerical mean field approach. In particular, it correctly predicted an intriguing property of conductance-based networks that does not appear to be shared by current-based models: they exhibit states of low-rate asynchronous irregular activity that persist for some period of time even in the absence of external inputs and without cortical pacemakers. Simulations of larger networks (up to 350,000 neurons) demonstrated that the survival time of self-sustained activity increases exponentially with network size.     

Correlations and population dynamics in cortical networks

The function of cortical networks depends on the collective interplay between neurons and neuronal populations, which is reflected in the correlation of signals that can be recorded at different levels. To correctly interpret these observations it is important to understand the origin of neuronal correlations. Here we study how cells in large recurrent networks of excitatory and inhibitory neurons interact and how the associated correlations affect stationary states of idle network activity. We demonstrate that the structure of the connectivity matrix of such networks induces considerable correlations between synaptic currents as well as between subthreshold membrane potentials, provided Dale's principle is respected. If, in contrast, synaptic weights are randomly distributed, input correlations can vanish, even for densely connected networks. Although correlations are strongly attenuated when proceeding from membrane potentials to action potentials (spikes), the resulting weak correlations in the spike output can cause substantial fluctuations in the population activity, even in highly diluted networks. We show that simple mean-field models that take the structure of the coupling matrix into account can adequately describe the power spectra of the population activity. The consequences of Dale's principle on correlations and rate fluctuations are discussed in the light of recent experimental findings.     

Differences in spiking patterns among cortical neurons

Spike sequences recorded from four cortical areas of an awake behaving monkey were examined to explore characteristics that vary among neurons. We found that a measure of the local variation of interspike intervals, L(V), is nearly the same for every spike sequence for any given neuron, while it varies significantly among neurons. The distributions of L(V) values for neuron ensembles in three of the four areas were found to be distinctly bimodal. Two groups of neurons classified according to the spiking irregularity exhibit different responses to the same stimulus. This suggests that neurons in each area can be classified into different groups possessing unique spiking statistics and corresponding functional properties.     

Influences of synaptic location on the synchronization of rhythmic bursting neurons

We study how the location of synaptic input influences the stablex firing states in coupled model neurons bursting rhythmically at the gamma frequencies (20-70 Hz). The model neuron consists of two compartments and generates one, two, three or four spikes in each burst depending on the intensity of input current and the maximum conductance of M-type potassium current. If the somata are connected by reciprocal excitatory synapses, we find strong correlations between the changes in the bursting mode and those in the stable phase-locked states of the coupled neurons. The stability of the in-phase phase-locked state (synchronously firing state) tends to change when the individual neurons change their bursting patterns. If, however, the synaptic connections are terminated on the dendritic compartments, no such correlated changes occur. In this case, the coupled bursting neurons do not show the in-phase phase-locked state in any bursting mode. These results indicate that synchronization behaviour of bursting neurons significantly depends on the synaptic location, unlike a coupled system of regular spiking neurons.     

Local asymptotic coherence of time-varying discrete ecological networks

The study of coherence of population dynamics is extremely important for predicting and evaluating the risk of global extinctions. The migration in a network of patch populations (metapopulation) inevitably involves various environmental noises or outside disturbances, which make the migration model time evolving and spatially extended. Thus time-invariant discrete ecological networks are often insufficient to capture the key features of real-world dynamical networks. Here, a time-varying discrete ecological network is proposed to characterize the practical metapopulation for the first time. Based on this model, several novel local coherence criteria are then attained, which provide some new insights into ecological conservation and biological diversity. Moreover, these coherence criteria are also applicable to the synchronization of complex networks in other biological and engineering systems.     

Synchrony in heterogeneous networks of spiking neurons

The emergence of synchrony in the activity of large, heterogeneous networks of spiking neurons is investigated. We define the robustness of synchrony by the critical disorder at which the asynchronous state becomes linearly unstable. We show that at low firing rates, synchrony is more robust in excitatory networks than in inhibitory networks, but excitatory networks cannot display any synchrony when the average firing rate becomes too high. We introduce a new regime where all inputs, external and internal, are strong and have opposite effects that cancel each other when averaged. In this regime, the robustness of synchrony is strongly enhanced, and robust synchrony can be achieved at a high firing rate in inhibitory networks. On the other hand, in excitatory networks, synchrony remains limited in frequency due to the intrinsic instability of strong recurrent excitation.     

Stationary bumps in networks of spiking neurons.

We examine the existence and stability of spatially localized "bumps" of neuronal activity in a network of spiking neurons. Bumps have been proposed in mechanisms of visual orientation tuning, the rat head direction system, and working memory. We show that a bump solution can exist in a spiking network provided the neurons fire asynchronously within the bump. We consider a parameter regime where the bump solution is bistable with an all-off state and can be initiated with a transient excitatory stimulus. We show that the activity profile matches that of a corresponding population rate model. The bump in a spiking network can lose stability through partial synchronization to either a traveling wave or the all-off state. This can occur if the synaptic timescale is too fast through a dynamical effect or if a transient excitatory pulse is applied to the network. A bump can thus be activated and deactivated with excitatory inputs that may have physiological relevance.     

Gamma oscillations in a nonlinear regime: a minimal model approach using heterogeneous integrate-and-fire networks

Fast oscillations and in particular gamma-band oscillation (20-80 Hz) are commonly observed during brain function and are at the center of several neural processing theories. In many cases, mathematical analysis of fast oscillations in neural networks has been focused on the transition between irregular and oscillatory firing viewed as an instability of the asynchronous activity. But in fact, brain slice experiments as well as detailed simulations of biological neural networks have produced a large corpus of results concerning the properties of fully developed oscillations that are far from this transition point. We propose here a mathematical approach to deal with nonlinear oscillations in a network of heterogeneous or noisy integrate-and-fire neurons connected by strong inhibition. This approach involves limited mathematical complexity and gives a good sense of the oscillation mechanism, making it an interesting tool to understand fast rhythmic activity in simulated or biological neural networks. A surprising result of our approach is that under some conditions, a change of the strength of inhibition only weakly influences the period of the oscillation. This is in contrast to standard theoretical and experimental models of interneuron network gamma oscillations (ING), where frequency tightly depends on inhibition strength, but it is similar to observations made in some in vitro preparations in the hippocampus and the olfactory bulb and in some detailed network models. This result is explained by the phenomenon of suppression that is known to occur in strongly coupled oscillating inhibitory networks but had not yet been related to the behavior of oscillation frequency.     

The complexity of latching transitions in large scale cortical networks

We study latching dynamics, i.e. the ability of a network to hop spontaneously from one discrete attractor state to another, which has been proposed as a model of an infinitely recursive process in large scale cortical networks, perhaps associated with higher cortical functions, such as language. We show that latching dynamics can span the range from deterministic to random under the control of a threshold parameter U. In particular, the interesting intermediate case is characterized by an asymmetric and complex set of transitions. We also indicate how finite latching sequences can become infinite, depending on the properties of the transition probability matrix and of its eigenvalues.     

Precision of pulse-coupled networks of integrate-and-fire neurons

Some sensory tasks in the nervous system require highly precise spike trains to be generated in the presence of intrinsic neuronal noise. Collective enhancement of precision (CEP) can occur when spike trains of many neurons are pooled together into a more precise population discharge. We study CEP in a network of N model neurons connected by recurrent excitation. Each neuron is driven by a periodic inhibitory spike train with independent jitter in the spike arrival time. The network discharge is characterized by sigmaW, the dispersion in the spike times within one cycle, and sigmaB, the jitter in the network-averaged spike time between cycles. In an uncoupled network sigmaB approximately = 1/square root(N) and sigmaW is independent of N. In a strongly coupled network sigmaB approximately = 1/square root(log N) and sigmaW is close to zero. At intermediate coupling strengths, sigmaW is reduced, while sigmaB remains close to its uncoupled value. The population discharge then has optimal biophysical properties compared with the uncoupled network.     

Image segmentation by networks of spiking neurons

A network of leaky integrate-and-fire (IAF) neurons is proposed to segment gray-scale images. The network architecture with local competition between neurons that encode segment assignments of image blocks is motivated by a histogram clustering approach to image segmentation. Lateral excitatory connections between neighboring image sites yield a local smoothing of segments. The mean firing rate of class membership neurons encodes the image segmentation. A weight modification scheme is proposed that estimates segment-specific prototypical histograms. The robustness properties of the network implementation make it amenable to an analog VLSI realization. Results on synthetic and real-world images demonstrate the effectiveness of the architecture.     

Short term memory in recurrent networks of spiking neurons

We present in this paper a general model of recurrent networks of spiking neurons, composed of several populations, and whose interaction pattern is set with a random draw. We use for simplicity discrete time neuron updating, and the emitted spikes are transmitted through randomly delayed lines. In excitatory-inhibitory networks, we show that inhomogeneous delays may favour synchronization provided that the inhibitory delays distribution is significantly stronger than the excitatory one. In that case, slow waves of synchronous activity appear (this synchronous activity is stronger in inhibitory population). This synchrony allows for a fast ada ptivity of the network to various input stimuli. In networks observing the constraint of short range excitation and long range inhibition, we show that under some parameter settings, this model displays properties of –1– dynamic retention –2– input normalization –3– target tracking. Those properties are of interest for modelling biological topologically organized structures, and for robotic applications taking place in noisy environments where targets vary in size, speed and duration. This revised version was published online in June 2006 with corrections to the Cover Date.     

Temporal correlations in stochastic networks of spiking neurons.

The determination of temporal and spatial correlations in neuronal activity is one of the most important neurophysiological tools to gain insight into the mechanisms of information processing in the brain. Its interpretation is complicated by the difficulty of disambiguating the effects of architecture, single-neuron properties, and network dynamics. We present a theory that describes the contribution of the network dynamics in a network of "spiking" neurons. For a simple neuron model including refractory properties, we calculate the temporal cross-correlations in a completely homogeneous, excitatory, fully connected network in a stable, stationary state, for stochastic dynamics in both discrete and continuous time. We show that even for this simple network architecture, the cross-correlations exhibit a large variety of qualitatively different properties, strongly dependent on the level of noise, the decay constant of the refractory function, and the network activity. At the critical point, the cross-correlations oscillate with a frequency that depends on the refractory properties or decay exponentially with a diverging damping constant (for "weak" refractory properties). We also investigate the effect of the synaptic time constants. It is shown that these time constants may, apart from their influence on the asymmetric peak arising from the direct synaptic connection, also affect the long-term properties of the cross-correlations.     

Selectively grouping neurons in recurrent networks of lateral inhibition

Winner-take-all networks have been proposed to underlie many of the brain's fundamental computational abilities. However, not much is known about how to extend the grouping of potential winners in these networks beyond single neuron or uniformly arranged groups of neurons. We show that competition between arbitrary groups of neurons can be realized by organizing lateral inhibition in linear threshold networks. Given a collection of potentially overlapping groups (with the exception of some degenerate cases), the lateral inhibition results in network dynamics such that any permitted set of neurons that can be coactivated by some input at a stable steady state is contained in one of the groups. The information about the input is preserved in this operation. The activity level of a neuron in a permitted set corresponds to its stimulus strength, amplified by some constant. Sets of neurons that are not part of a group cannot be coactivated by any input at a stable steady state. We analyze the storage capacity of such a network for random groups--the number of random groups the network can store as permitted sets without creating too many spurious ones. In this framework, we calculate the optimal sparsity of the groups (maximizing group entropy). We find that for dense inputs, the optimal sparsity is unphysiologically small. However, when the inputs and the groups are equally sparse, we derive a more plausible optimal sparsity. We believe our results are the first steps toward attractor theories in hybrid analog-digital networks.