Evolution of the Wilson-Cowan equations.

The Wilson-Cowan equations were developed to provide a simplified yet powerful description of neural network dynamics. As such, they embraced nonlinear dynamics, but in an interpretable form. Most importantly, it was the first mathematical formulation to emphasize the significance of interactions between excitatory and inhibitory neural populations, thereby incorporating both cooperation and competition. Subsequent research by many has documented the Wilson-Cowan significance in such diverse fields as visual hallucinations, memory, binocular rivalry, and epilepsy. The fact that these equations are still being used to elucidate a wide range of phenomena attests to their validity as a dynamical approximation to more detailed descriptions of complex neural computations.

Pattern forming mechanisms of color vision.

While our understanding of the way single neurons process chromatic stimuli in the early visual pathway has advanced significantly in recent years, we do not yet know how these cells interact to form stable representations of hue. Drawing on physiological studies, we offer a dynamical model of how the primary visual cortex tunes for color, hinged on intracortical interactions and emergent network effects. After detailing the evolution of network activity through analytical and numerical approaches, we discuss the effects of the model's cortical parameters on the selectivity of the tuning curves. In particular, we explore the role of the model's thresholding nonlinearity in enhancing hue selectivity by expanding the region of stability, allowing for the precise encoding of chromatic stimuli in early vision. Finally, in the absence of a stimulus, the model is capable of explaining hallucinatory color perception via a Turing-like mechanism of biological pattern formation.

Generalized spin models for coupled cortical feature maps obtained by coarse graining correlation based synaptic learning rules.

We derive generalized spin models for the development of feedforward cortical architecture from a Hebbian synaptic learning rule in a two layer neural network with nonlinear weight constraints. Our model takes into account the effects of lateral interactions in visual cortex combining local excitation and long range effective inhibition. Our approach allows the principled derivation of developmental rules for low-dimensional feature maps, starting from high-dimensional synaptic learning rules. We incorporate the effects of smooth nonlinear constraints on net synaptic weight projected from units in the thalamic layer (the fan-out) and on the net synaptic weight received by units in the cortical layer (the fan-in). These constraints naturally couple together multiple feature maps such as orientation preference and retinotopic organization. We give a detailed illustration of the method applied to the development of the orientation preference map as a special case, in addition to deriving a model for joint pattern formation in cortical maps of orientation preference, retinotopic location, and receptive field width. We show that the combination of Hebbian learning and center-surround cortical interaction naturally leads to an orientation map development model that is closely related to the XY magnetic lattice model from statistical physics. The results presented here provide justification for phenomenological models studied in Cowan and Friedman (Advances in neural information processing systems 3, 1991), Thomas and Cowan (Phys Rev Lett 92(18):e188101, 2004) and provide a developmental model realizing the synaptic weight constraints previously assumed in Thomas and Cowan (Math Med Biol 23(2):119-138, 2006).

Avalanches in a stochastic model of spiking neurons.

Neuronal avalanches are a form of spontaneous activity widely observed in cortical slices and other types of nervous tissue, both in vivo and in vitro. They are characterized by irregular, isolated population bursts when many neurons fire together, where the number of spikes per burst obeys a power law distribution. We simulate, using the Gillespie algorithm, a model of neuronal avalanches based on stochastic single neurons. The network consists of excitatory and inhibitory neurons, first with all-to-all connectivity and later with random sparse connectivity. Analyzing our model using the system size expansion, we show that the model obeys the standard Wilson-Cowan equations for large network sizes ( neurons). When excitation and inhibition are closely balanced, networks of thousands of neurons exhibit irregular synchronous activity, including the characteristic power law distribution of avalanche size. We show that these avalanches are due to the balanced network having weakly stable functionally feedforward dynamics, which amplifies some small fluctuations into the large population bursts. Balanced networks are thought to underlie a variety of observed network behaviours and have useful computational properties, such as responding quickly to changes in input. Thus, the appearance of avalanches in such functionally feedforward networks indicates that avalanches may be a simple consequence of a widely present network structure, when neuron dynamics are noisy. An important implication is that a network need not be "critical" for the production of avalanches, so experimentally observed power laws in burst size may be a signature of noisy functionally feedforward structure rather than of, for example, self-organized criticality.

Systematic fluctuation expansion for neural network activity equations.

Population rate or activity equations are the foundation of a common approach to modeling for neural networks. These equations provide mean field dynamics for the firing rate or activity of neurons within a network given some connectivity. The shortcoming of these equations is that they take into account only the average firing rate, while leaving out higher-order statistics like correlations between firing. A stochastic theory of neural networks that includes statistics at all orders was recently formulated. We describe how this theory yields a systematic extension to population rate equations by introducing equations for correlations and appropriate coupling terms. Each level of the approximation yields closed equations; they depend only on the mean and specific correlations of interest, without an ad hoc criterion for doing so. We show in an example of an all-to-all connected network how our system of generalized activity equations captures phenomena missed by the mean field rate equations alone.

Field-theoretic approach to fluctuation effects in neural networks.

A well-defined stochastic theory for neural activity, which permits the calculation of arbitrary statistical moments and equations governing them, is a potentially valuable tool for theoretical neuroscience. We produce such a theory by analyzing the dynamics of neural activity using field theoretic methods for nonequilibrium statistical processes. Assuming that neural network activity is Markovian, we construct the effective spike model, which describes both neural fluctuations and response. This analysis leads to a systematic expansion of corrections to mean field theory, which for the effective spike model is a simple version of the Wilson-Cowan equation. We argue that neural activity governed by this model exhibits a dynamical phase transition which is in the universality class of directed percolation. More general models (which may incorporate refractoriness) can exhibit other universality classes, such as dynamic isotropic percolation. Because of the extremely high connectivity in typical networks, it is expected that higher-order terms in the systematic expansion are small for experimentally accessible measurements, and thus, consistent with measurements in neocortical slice preparations, we expect mean field exponents for the transition. We provide a quantitative criterion for the relative magnitude of each term in the systematic expansion, analogous to the Ginsburg criterion. Experimental identification of dynamic universality classes in vivo is an outstanding and important question for neuroscience.

Simultaneous constraints on pre- and post-synaptic cells couple cortical feature maps in a 2D geometric model of orientation preference.

The most prominent feature of mammalian striate cortex (V1) is the spatial organization of response preferences for the position and orientation of elementary visual stimuli. Models for the formation of cortical maps of orientation and 'retinotopic' position typically rely on a combination of Hebbian or correlation-based synaptic plasticity, and constraints on the distribution of synaptic weights. We consider a simplified model of orientation and retinotopic specificity based on the geometry of the feed-forward synaptic weight distribution from an 'unoriented' layer of cells to a first weakly oriented layer. We model the feed-forward weight distribution as a system of planar Gaussian receptive fields each elongated in the direction matching the preferred orientation of the postsynaptic cell. Under the constraint of presynaptic weight normalization (each cell in the oriented layer receives the same net synaptic weight) and a uniform retinotopic map (displacement of centres of mass of receptive fields in the unoriented layer is strictly proportional to the displacement of the corresponding cells in the oriented layer), we find that imposing a pattern of orientation preference forces the system to violate postsynaptic weight normalization (each cell in the unoriented layer no longer sends forth the same net synaptic weight). We study this deviation from uniformity of the postsynaptic weight, and find that the deviation has a distinct form in the vicinity of the 'pinwheel' singularities of the orientation map. We show that uniform synaptic coverage of the unoriented layer can be restored by introducing a distortion in the retinotopic locations of the receptive fields. We calculate, to first order in the relative elongation of the receptive fields, the retinotopic distortion vector field. Both the pattern of postsynaptic weight non-uniformity and the corrective retinotopic distortion vector field fail to possess the reflection symmetry commonly assumed to relate orientation singularities with topological index +/- pi. Hence, we show that 'right-handed' and 'left-handed' orientation singularities are funda-mentally distinct anatomical structures when full 2D synaptic architecture is taken into account. Finally, we predict specific patterns of retinotopic distortion that should obtain in the vicinity of +/- pi-fold orientation singularities, if uniform pre- and post-synaptic weight constraints are strongly enforced.

Wilson-Cowan Equations for Neocortical Dynamics.

In 1972-1973 Wilson and Cowan introduced a mathematical model of the population dynamics of synaptically coupled excitatory and inhibitory neurons in the neocortex. The model dealt only with the mean numbers of activated and quiescent excitatory and inhibitory neurons, and said nothing about fluctuations and correlations of such activity. However, in 1997 Ohira and Cowan, and then in 2007-2009 Buice and Cowan introduced Markov models of such activity that included fluctuation and correlation effects. Here we show how both models can be used to provide a quantitative account of the population dynamics of neocortical activity.We first describe how the Markov models account for many recent measurements of the resting or spontaneous activity of the neocortex. In particular we show that the power spectrum of large-scale neocortical activity has a Brownian motion baseline, and that the statistical structure of the random bursts of spiking activity found near the resting state indicates that such a state can be represented as a percolation process on a random graph, called directed percolation.Other data indicate that resting cortex exhibits pair correlations between neighboring populations of cells, the amplitudes of which decay slowly with distance, whereas stimulated cortex exhibits pair correlations which decay rapidly with distance. Here we show how the Markov model can account for the behavior of the pair correlations.Finally we show how the 1972-1973 Wilson-Cowan equations can account for recent data which indicates that there are at least two distinct modes of cortical responses to stimuli. In mode 1 a low intensity stimulus triggers a wave that propagates at a velocity of about 0.3 m/s, with an amplitude that decays exponentially. In mode 2 a high intensity stimulus triggers a larger response that remains local and does not propagate to neighboring regions.

Modeling focal epileptic activity in the Wilson-cowan model with depolarization block.

UNLABELLED: Measurements of neuronal signals during human seizure activity and evoked epileptic activity in experimental models suggest that, in these pathological states, the individual nerve cells experience an activity driven depolarization block, i.e. they saturate. We examined the effect of such a saturation in the Wilson-Cowan formalism by adapting the nonlinear activation function; we substituted the commonly applied sigmoid for a Gaussian function. We discuss experimental recordings during a seizure that support this substitution. Next we perform a bifurcation analysis on the Wilson-Cowan model with a Gaussian activation function. The main effect is an additional stable equilibrium with high excitatory and low inhibitory activity. Analysis of coupled local networks then shows that such high activity can stay localized or spread. Specifically, in a spatial continuum we show a wavefront with inhibition leading followed by excitatory activity. We relate our model simulations to observations of spreading activity during seizures. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13408-015-0019-4) contains supplementary material 1.

The functional geometry of local and horizontal connections in a model of V1.

A mathematical model of interacting hypercolumns in primary visual cortex (V1) is presented that incorporates details concerning the geometry of local and long-range horizontal connections. Each hypercolumn is modeled as a network of interacting excitatory and inhibitory neural populations with orientation and spatial frequency preferences organized around a pair of pinwheels. The pinwheels are arranged on a planar lattice, reflecting the crystalline-like structure of cortex. Local interactions within a hypercolumn generate orientation and spatial frequency tuning curves, which are modulated by horizontal connections between different hypercolumns on the lattice. The symmetry properties of the local and long-range connections play an important role in determining the types of spontaneous activity patterns that can arise in cortex.

Emergent oscillations in networks of stochastic spiking neurons.

Networks of neurons produce diverse patterns of oscillations, arising from the network's global properties, the propensity of individual neurons to oscillate, or a mixture of the two. Here we describe noisy limit cycles and quasi-cycles, two related mechanisms underlying emergent oscillations in neuronal networks whose individual components, stochastic spiking neurons, do not themselves oscillate. Both mechanisms are shown to produce gamma band oscillations at the population level while individual neurons fire at a rate much lower than the population frequency. Spike trains in a network undergoing noisy limit cycles display a preferred period which is not found in the case of quasi-cycles, due to the even faster decay of phase information in quasi-cycles. These oscillations persist in sparsely connected networks, and variation of the network's connectivity results in variation of the oscillation frequency. A network of such neurons behaves as a stochastic perturbation of the deterministic Wilson-Cowan equations, and the network undergoes noisy limit cycles or quasi-cycles depending on whether these have limit cycles or a weakly stable focus. These mechanisms provide a new perspective on the emergence of rhythmic firing in neural networks, showing the coexistence of population-level oscillations with very irregular individual spike trains in a simple and general framework.

Implementing the Retinex algorithm with Wilson-Cowan equations.

It is shown that a form of the Wilson-Cowan equations representing large-scale activity in interacting neural populations can implement a form of the Retinex algorithm for color vision. It has also been shown recently that a color enhancement algorithm closely related to Retinex can be derived from a variational principle. It follows that a variational principle exists for equations of Wilson-Cowan type. Thus the Wilson-Cowan equations are the Euler-Lagrange solution of the minimization of an energy functional. This result suggests many interesting neural applications.

Spontaneous pattern formation and pinning in the primary visual cortex.

A mean field approach to the population activity of cortical neurons is used to provide a possible mechanism for the generation of geometric visual hallucinations. As was previously investigated, competition between short-range excitation and longer-range inhibition in the connectivity profile of neurons provides the difference of length scales necessary for spontaneous symmetry breaking in the form of the Turing mechanism to generate patterns of activity. This approach is expanded in order to be able to incorporate additional details of the cortical circuitry, namely that neurons are also weakly connected at long ranges to other neurons sharing a particular preference for a stimulus feature such as orientation, spatial frequency, motion, color or disparity. Since the layout of cortical feature maps is approximately crystalline, one can apply a study of nonlinear dynamics similar to the analysis of wave propagation in a crystalline lattice to demonstrate how the spatial pattern formed through the Turing instability can be pinned to the geometric layout of various feature preferences. The specific feature map used in the study presented here is that of orientation preference, although the model can be extended to include additional features. The perturbation analysis is analogous to solving the Schrödinger equation in a weak periodic potential. Competition between the local isotropic connections which produce patterns of activity via the Turing mechanism and the weaker patchy lateral connections that depend on a neuron's particular set of feature preferences create long wavelength affects analogous to commensurate-incommensurate transitions found in fluid systems under a spatially periodic driving force. Using the retinocortical map, spontaneously formed activity patterns generated by the model can then be overlayed on the feature maps to construct the corresponding image in the visual field. We thus describe a new approach that allows the incorporation of some of the above features into a comprehensive account of the origins of hallucinations.

Statistical mechanics of the neocortex.

We analyze neocortical dynamics using field theoretic methods for non-equilibrium statistical processes. Assuming the dynamics is Markovian, we introduce a model that describes both neural fluctuations and responses to stimuli. We show that at low spiking rates, neocortical activity exhibits a dynamical phase transition which is in the universality class of directed percolation (DP). Because of the high density and large spatial extent of neural interactions, there is a "mean field" region in which the effects of fluctuations are negligible. However as the generation and decay of spiking activity becomes balanced, there is a crossover into the critical fluctuation driven DP region, consistent with measurements in neocortical slice preparations. From the perspective of theoretical neuroscience, the principal contribution of this work is the formulation of a theory of neural activity that goes beyond the mean-field approximation and incorporates the effects of fluctuations and correlations in the critical region. This theory shows that the scaling laws found in many measurements of neocortical activity, in anesthetized, normal and epileptic neocortex, are consistent with the existence of DP and related phase transitions at a critical point. It also shows how such properties lead to a model of the origins of both random and rhythmic brain activity.

A spherical model for orientation and spatial-frequency tuning in a cortical hypercolumn.

A theory is presented of the way in which the hypercolumns in primary visual cortex (V1) are organized to detect important features of visual images, namely local orientation and spatial-frequency. Given the existence in V1 of dual maps for these features, both organized around orientation pinwheels, we constructed a model of a hypercolumn in which orientation and spatial-frequency preferences are represented by the two angular coordinates of a sphere. The two poles of this sphere are taken to correspond, respectively, to high and low spatial-frequency preferences. In Part I of the paper, we use mean-field methods to derive exact solutions for localized activity states on the sphere. We show how cortical amplification through recurrent interactions generates a sharply tuned, contrast-invariant population response to both local orientation and local spatial frequency, even in the case of a weakly biased input from the lateral geniculate nucleus (LGN). A major prediction of our model is that this response is non-separable with respect to the local orientation and spatial frequency of a stimulus. That is, orientation tuning is weaker around the pinwheels, and there is a shift in spatial-frequency tuning towards that of the closest pinwheel at non-optimal orientations. In Part II of the paper, we demonstrate that a simple feed-forward model of spatial-frequency preference, unlike that for orientation preference, does not generate a faithful representation when amplified by recurrent interactions in V1. We then introduce the idea that cortico-geniculate feedback modulates LGN activity to generate a faithful representation, thus providing a new functional interpretation of the role of this feedback pathway. Using linear filter theory, we show that if the feedback from a cortical cell is taken to be approximately equal to the reciprocal of the corresponding feed-forward receptive field (in the two-dimensional Fourier domain), then the mismatch between the feed-forward and cortical frequency representations is eliminated. We therefore predict that cortico-geniculate feedback connections innervate the LGN in a pattern determined by the orientation and spatial-frequency biases of feed-forward receptive fields. Finally, we show how recurrent cortical interactions can generate cross-orientation suppression.

Symmetry induced coupling of cortical feature maps.

The mammalian visual cortex maps retinal position (retinotopy) and orientation preference (OP) across its surface. Simultaneous measurements in vivo suggest that positive correlation exists between the location of dislocations in these two maps, contradicting the predictions of classical dimension reduction models. Model symmetries exert a significant influence on pattern development. However, classical models for cortical map formation have inappropriate symmetry properties. By applying equivariant bifurcation theory we derive symmetry induced, model independent coupling of the OP and retinotopic maps and show that this coupling replicates observations.

An amplitude equation approach to contextual effects in visual cortex.

A mathematical theory of interacting hypercolumns in primary visual cortex (V1) is presented that incorporates details concerning the anisotropic nature of long-range lateral connections. Each hypercolumn is modeled as a ring of interacting excitatory and inhibitory neural populations with orientation preferences over the range 0 to 180 degrees. Analytical methods from bifurcation theory are used to derive nonlinear equations for the amplitude and phase of the population tuning curves in which the effective lateral interactions are linear in the amplitudes. These amplitude equations describe how mutual interactions between hypercolumns via lateral connections modify the response of each hypercolumn to modulated inputs from the lateral geniculate nucleus; such interactions form the basis of contextual effects. The coupled ring model is shown to reproduce a number of orientation-dependent and contrast-dependent features observed in center-surround experiments. A major prediction of the model is that the anisotropy in lateral connections results in a nonuniform modulatory effect of the surround that is correlated with the orientation of the center.

SO3 symmetry breaking mechanism for orientation and spatial frequency tuning in the visual cortex.

A dynamical model of orientation and spatial frequency tuning in a cortical hypercolumn is presented. The network topology is taken to be a sphere whose poles correspond to orientation pinwheels associated with high and low spatial frequency domains, respectively. Recurrent interactions within the sphere generate a tuned response via an SO3 symmetry breaking mechanism.

What geometric visual hallucinations tell us about the visual cortex.

Many observers see geometric visual hallucinations after taking hallucinogens such as LSD, cannabis, mescaline or psilocybin; on viewing bright flickering lights; on waking up or falling asleep; in "near-death" experiences; and in many other syndromes. Klüver organized the images into four groups called form constants: (I) tunnels and funnels, (II) spirals, (III) lattices, including honeycombs and triangles, and (IV) cobwebs. In most cases, the images are seen in both eyes and move with them. We interpret this to mean that they are generated in the brain. Here, we summarize a theory of their origin in visual cortex (area V1), based on the assumption that the form of the retino-cortical map and the architecture of V1 determine their geometry. (A much longer and more detailed mathematical version has been published in Philosophical Transactions of the Royal Society B, 356 [2001].) We model V1 as the continuum limit of a lattice of interconnected hypercolumns, each comprising a number of interconnected iso-orientation columns. Based on anatomical evidence, we assume that the lateral connectivity between hypercolumns exhibits symmetries, rendering it invariant under the action of the Euclidean group E(2), composed of reflections and translations in the plane, and a (novel) shift-twist action. Using this symmetry, we show that the various patterns of activity that spontaneously emerge when V1's spatially uniform resting state becomes unstable correspond to the form constants when transformed to the visual field using the retino-cortical map. The results are sensitive to the detailed specification of the lateral connectivity and suggest that the cortical mechanisms that generate geometric visual hallucinations are closely related to those used to process edges, contours, surfaces, and textures.