Jack D. Cowan

A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue

It is proposed that distinct anatomical regions of cerebral cortex and of thalamic nuclei are functionally two-dimensional. On this view, the third (radial) dimension of cortical and thalamic structures is associated with a redundancy of circuits and functions so that reliable signal processing obtains in the presence of noisy or ambiguous stimuli.A mathematical model of simple cortical and thalamic nervous tissue is consequently developed, comprising two types of neurons (excitatory and inhibitory), homogeneously distributed in planar sheets, and interacting by way of recurrent lateral connexions. Following a discussion of certain anatomical and physiological restrictions on such interactions, numerical solutions of the relevant non-linear integro-differential equations are obtained. The results fall conveniently into three categories, each of which is postulated to correspond to a distinct type of tissue: sensory neo-cortex, archior prefrontal cortex, and thalamus.The different categories of solution are referred to as dynamical modes. The mode appropriate to thalamus involves a variety of non-linear oscillatory phenomena. That appropriate to archior prefrontal cortex is defined by the existence of spatially inhomogeneous stable steady states which retain contour information about prior stimuli. Finally, the mode appropriate to sensory neo-cortex involves active transient responses. It is shown that this particular mode reproduces some of the phenomenology of visual psychophysics, including spatial modulation transfer function determinations, certain metacontrast effects, and the spatial hysteresis phenomenon found in stereopsis.

A mathematical theory of visual hallucination patterns

Neuronal activity in a two-dimensional net is analyzed in the neighborhood of an instability. Bifurcation theory and group theory are used to demonstrate the existence of a variety of doublyperiodic patterns, hexagons, rolls, etc., as solutions to the field equations for the net activity. It is suggested that these simple geometric patterns are the cortical concomitants of the “form constants” seen during visual hallucinosis.

What matters in neuronal locking

Exploiting local stability, we show what neuronal characteristics are essential to ensure that coherent oscillations are asymptotically stable in a spatially homogeneous network of spiking neurons. Under standard conditions, a necessary and, in the limit of a large number of interacting neighbors, also sufficient condition is that the postsynaptic potential is increasing in time as the neurons fire. If the postsynaptic potential is decreasing, oscillations are bound to be unstable. This is a kind of locking theorem and boils down to a subtle interplay of axonal delays, postsynaptic potentials, and refractory behavior. The theorem also allows for mixtures of excitatory and inhibitory interactions. On the basis of the locking theorem, we present a simple geometric method to verify the existence and local stability of a coherent oscillation.

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. Klver 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 retinocortical 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 V1s 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.

Temporal oscillations in neuronal nets

SummaryA model for the interactions of cortical neurons is derived and analyzed. It is shown that small amplitude spatially inhomogeneous standing oscillations can bifurcate from the rest state. In a periodic domain, traveling wave trains exist. Stability of these patterns is discussed in terms of biological parameters. Homoclinic and heteroclinic orbits are demonstrated for the space-clamped system.

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.

Outline of a theory for the ontogenesis of iso-orientation domains in visual cortex

The following statements are assumed as experimental facts: The majority of cells in visual cortex is selectively sensitive to stimuli in the form of lines or edges of a certain orientation. Optimal orientation varies smoothly from cell to cell over the cortical surface. This structure is present, in immature form, at the time of eye opening. The problem is to find a plausible mechanism for the ontogenesis of this structure. Published theories are reviewed and found to be insufficient in one or more respects. A new theory is proposed. It distinguishes two processes: A) In the previsual period, intracortical connections re-organize themselves such that they restrict activity to an appropriate family of patterns (e.g. stripes of different phases). B) Later, a one-to-one mapping is developed that couples each stimulus orientation to one of the cortical patterns. The coupling may take place in two stages: a) Still before eye opening, two sets of afferent pilot fibres serve to fix the mapping in two points. (The pilot fibres can be assigned to these two sets on the basis of correlated or anticorrelated spike activity. They have genetically programmed orientation preferences which fall into two groups. A fibre sorting mechanism analogous to the one producing ocularity domains concentrates the sets of fibres into complementary activity patterns.) b) After eye opening, a more precise mapping of orientations to cortical patterns develops with the help of visual stimulation and synaptic plasticity according to a well-known mechanism. Experimental evidence for the theory is discussed. The theory can be evaluated in terms of general principles of brain organization.

Faithful representation of separable distributions

A geometric approach to data representation incorporating information theoretic ideas is presented. The task of finding a faithful representation, where the input distribution is evenly partitioned into regions of equal mass, is addressed. For input consisting of mixtures of statistically independent sources, we treat independent component analysis (ICA) as a computational geometry problem. First, we consider the separation of sources with sharply peaked distribution functions, where the ICA problem becomes that of finding high-density directions in the input distribution. Second, we consider the more general problem for arbitrary input distributions, where ICA is transformed into the task of finding an aligned equipartition. By modifying the Kohonen self-organized feature maps, we arrive at neural networks with local interactions that optimize coding while simultaneously performing source separation. The local nature of our approach results in networks with nonlinear ICA capabilities.

Emergent Oscillations in Networks of Stochastic Spiking Neurons

Networks of neurons produce diverse patterns of oscillations, arising from the networks 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 networks 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.