Maximum entropy models are the least structured probability distributions that exactly reproduce a chosen set of statistics measured in an interacting network. Here we use this principle to construct probabilistic models which describe the correlated spiking activity of populations of up to 120 neurons in the salamander retina as it responds to natural movies. Already in groups as small as 10 neurons, interactions between spikes can no longer be regarded as small perturbations in an otherwise independent system; for 40 or more neurons pairwise interactions need to be supplemented by a global interaction that controls the distribution of synchrony in the population. Here we show that such "K-pairwise" models--being systematic extensions of the previously used pairwise Ising models--provide an excellent account of the data. We explore the properties of the neural vocabulary by: 1) estimating its entropy, which constrains the population's capacity to represent visual information; 2) classifying activity patterns into a small set of metastable collective modes; 3) showing that the neural codeword ensembles are extremely inhomogenous; 4) demonstrating that the state of individual neurons is highly predictable from the rest of the population, allowing the capacity for error correction.

Sensory information about the outside world is encoded by neurons in sequences of discrete, identical pulses termed action potentials or spikes. There is persistent controversy about the extent to which the precise timing of these spikes is relevant to the function of the brain. We revisit this issue, using the motion-sensitive neurons of the fly visual system as a test case. Our experimental methods allow us to deliver more nearly natural visual stimuli, comparable to those which flies encounter in free, acrobatic flight. New mathematical methods allow us to draw more reliable conclusions about the information content of neural responses even when the set of possible responses is very large. We find that significant amounts of visual information are represented by details of the spike train at millisecond and sub-millisecond precision, even though the sensory input has a correlation time of approximately 55 ms; different patterns of spike timing represent distinct motion trajectories, and the absolute timing of spikes points to particular features of these trajectories with high precision. Finally, the efficiency of our entropy estimator makes it possible to uncover features of neural coding relevant for natural visual stimuli: first, the system's information transmission rate varies with natural fluctuations in light intensity, resulting from varying cloud cover, such that marginal increases in information rate thus occur even when the individual photoreceptors are counting on the order of one million photons per second. Secondly, we see that the system exploits the relatively slow dynamics of the stimulus to remove coding redundancy and so generate a more efficient neural code.

A major challenge in analyzing animal behavior is to discover some underlying simplicity in complex motor actions. Here, we show that the space of shapes adopted by the nematode Caenorhabditis elegans is low dimensional, with just four dimensions accounting for 95% of the shape variance. These dimensions provide a quantitative description of worm behavior, and we partially reconstruct "equations of motion" for the dynamics in this space. These dynamics have multiple attractors, and we find that the worm visits these in a rapid and almost completely deterministic response to weak thermal stimuli. Stimulus-dependent correlations among the different modes suggest that one can generate more reliable behaviors by synchronizing stimuli to the state of the worm in shape space. We confirm this prediction, effectively "steering" the worm in real time.

Does the brain construct an efficient representation of the sensory world? We review progress on this question, focusing on a series of experiments in the last decade which use fly vision as a model system in which theory and experiment can confront each other. Although the idea of efficient representation has been productive, clearly it is incomplete since it doesn't tell us which bits of sensory information are most valuable to the organism. We argue that, in fact, an organism which maximizes the (biologically meaningful) adaptive value of its actions given fixed resources must have internal representations of the outside world that are optimal in a very specific information theoretic sense: they maximize the information about the future of sensory inputs at a fixed value of the information about their past. This principle contains as special cases computations which the brain seems to carry out, and it should be possible to test this optimization directly. We return to the fly visual system and report the results of preliminary experiments that are in very suggestive agreement with theory

We propose a method that allows for a rigorous statistical analysis of neural responses to natural stimuli that are nongaussian and exhibit strong correlations. We have in mind a model in which neurons are selective for a small number of stimulus dimensions out of a high-dimensional stimulus space, but within this subspace the responses can be arbitrarily nonlinear. Existing analysis methods are based on correlation functions between stimuli and responses, but these methods are guaranteed to work only in the case of gaussian stimulus ensembles. As an alternative to correlation functions, we maximize the mutual information between the neural responses and projections of the stimulus onto low-dimensional subspaces. The procedure can be done iteratively by increasing the dimensionality of this subspace. Those dimensions that allow the recovery of all of the information between spikes and the full unprojected stimuli describe the relevant subspace. If the dimensionality of the relevant subspace indeed is small, it becomes feasible to map the neuron's input-output function even under fully natural stimulus conditions. These ideas are illustrated in simulations on model visual and auditory neurons responding to natural scenes and sounds, respectively.

Clustering provides a common means of identifying structure in complex data, and there is renewed interest in clustering as a tool for the analysis of large data sets in many fields. A natural question is how many clusters are appropriate for the description of a given system. Traditional approaches to this problem are based on either a framework in which clusters of a particular shape are assumed as a model of the system or on a two-step procedure in which a clustering criterion determines the optimal assignments for a given number of clusters and a separate criterion measures the goodness of the classification to determine the number of clusters. In a statistical mechanics approach, clustering can be seen as a trade-off between energy- and entropy-like terms, with lower temperature driving the proliferation of clusters to provide a more detailed description of the data. For finite data sets, we expect that there is a limit to the meaningful structure that can be resolved and therefore a minimum temperature beyond which we will capture sampling noise. This suggests that correcting the clustering criterion for the bias that arises due to sampling errors will allow us to find a clustering solution at a temperature that is optimal in the sense that we capture maximal meaningful structure--without having to define an external criterion for the goodness or stability of the clustering. We show that in a general information-theoretic framework, the finite size of a data set determines an optimal temperature, and we introduce a method for finding the maximal number of clusters that can be resolved from the data in the hard clustering limit.

What happens to the optimal interpretation of noisy data when there exists more than one equally plausible interpretation of the data? In a Bayesian model-learning framework the answer depends on the prior ex- pectations of the dynamics of the model parameter that is to be inferred from the data. Local time constraints on the priors are insufficient to pick one interpretation over another. On the other hand, nonlocal time constraints, induced by a 1/f noise spectrum of the priors, is shown to permit learning of a specific model parameter even when there are in- finitely many equally plausible interpretations of the data. This transition is inferred by a remarkable mapping of the model estimation problem to a dissipative physical system, allowing the use of powerful statisti- cal mechanical methods to uncover the transition from indeterminate to determinate model learning.

We introduce an information theoretic method for nonparametric, non- linear dimensionality reduction, based on the infinite cluster limit of rate distortion theory. By constraining the information available to manifold coordinates, a natural probabilistic map emerges that assigns original data to corresponding points on a lower dimensional manifold. With only the information-distortion trade off as a parameter, our method de- termines the shape of the manifold, its dimensionality, the probabilistic map and the prior that provide optimal description of the data. 1 A simple example Some data sets may not be as complicated as they appear. Consider the set of points on a plane in Figure 1. As a two dimensional set, it requires a two dimensional density ρ(x, y) for its description. Since the data are sparse the density will be almost singular. We may use a smoothing kernel, but then the data set will be described by a complicated combina- tion of troughs and peaks with no obvious pattern and hence no ability to generalize. We intuitively, however, see a strong one dimensional structure (a curve) underlying the data. In this paper we attempt to capture this intuition formally, through the use of the infinite cluster limit of rate distortion theory. Any set of points can be embedded in a hypersurface of any intrinsic dimensionality if we allow that hypersurface to be highly “folded.” For example, in Figure 1, any curve that goes through all the points gives a one dimensional representation. We would like to avoid such solutions, since they do not help us discover structure in the data. Looking for a simpler description one may choose to penalize the curvature term [1]. The problem with this approach is that it is not easily generalized to multiple dimensions, and requires the dimensionality of the solution as an input. An alternative approach is to allow curves of all shapes and sizes, but to send the reduced coordinates through an information bottleneck. With a fixed number of bits, position along a highly convoluted curve becomes uncertain. This will penalize curves that follow the data too closely (see Figure 1). There are several advantages to this approach. First, it removes the artificiality introduced by Hastie [2] of adding to the cost function only orthogonal er- rors. If we believe that data points fall out of the manifold due to noise, there is no reason to treat the projection onto the manifold as exact. Second, it does not require the dimension- Figure 1: Rate distortion curve for a data set of 25 points (red). We used 1000 points to represent the curve which where initialized by scattering them uni- formly on the plane. Note that the pro- duced curve is well defined, one dimen- sional and smooth. ality of the solution manifold as an input. By adding extra dimensions, one quickly looses the precision with which manifold points are specified (due to the fixed information bottle- neck). Hence, the optimal dimension emerges naturally. This also means that the method works well in many dimensions with no adjustments. Third, the method handles sparse data well. This is important since in high dimensional spaces all data sets are sparse, i.e. they look like points in Figure 1, and the density estimation becomes impossible. Luckily, if the data are truly generated by a lower dimensional process, then density estimation in the data space is not important (from the viewpoint of prediction or any other). What is critical is the density of the data along the manifold (known in latent variable modeling as a prior), and our algorithm finds it naturally. 2 Latent variable models and dimensionality reduction Recently, the problem of reducing the dimensionality of a data set has received renewed attention [3,4]. The underlying idea, due to Hotelling [5], is that most of the variation in many high dimensional data sets can often be explained by a few latent variables. Alterna- tively, we say that rather than filling the whole space, the data lie on a lower dimensional manifold. The dimensionality of this manifold is the dimensionality of the latent space and the coordinate system on this manifold provides the latent variables. Traditional tools of principal component analysis (PCA) and factor analysis (FA) are still the most widely used methods in data analysis. They project the data onto a hyperplane, so the reduced coordinates are easy to interpret. However, these methods are unable to deal with nonlinear correlations in a data set. To accommodate nonlinearity in a data set, one has to relax the assumption that the data is modeled by a hyperplane, and allow a general low dimensional manifold of unknown shape and dimensionality. The same questions that we asked in the previous section apply here. What do we mean by requiring that “the manifold models the data well”? In the next section, we formalize this notion by defining the manifold description of data as a doublet (the shape of the manifold and the projection map). Note that we do not require the probability distribution over the manifold (known for generative models [6,7] as a prior distribution over the latent variables and postulated a priori). It is completely determined by the doublet. Nonlinear correlations in data can also be accommodated implicitly, without constructing an actual low dimensional manifold. By mapping the data from the original space to an even higher dimensional feature space, we may hope that the correlations will become linearized and PCA will apply. Kernel methods [8] allow us to do this without actually constructing an explicit map to feature space. They introduce nonlinearity through an a priori nonlinear kernel. Alternatively, autoassociative neural networks [9] force the data through a bottleneck (with an internal layer of desired dimensionality) to produce a reduced 024681012123456789 description. One of the disadvantages of these methods is that the results are not easy to interpret. Recent attempts to describe a data set with a low dimensional representation generally fol- low into two categories: spectral methods and density modeling methods. Spectral methods (LLE [3], ISOMAP [4], Laplacian eigenmaps [10]) give reduced coordinates of an a pri- ori dimensionality by introducing a quadratic cost function in reduced coordinates (hence eigenvectors are solutions) that mimics the relationships between points in the original data space (geodesic distance for ISOMAP, linear reconstruction for LLE). Density modeling methods (GTM [6], GMM [7]) are generative models that try to reproduce the data with fewer variables. They require a prior and a parametric generative model to be introduced a priori and then find optimal parameters via maximum likelihood. The approach that we will take is inspired by the work of Kramer [9] and others who tried to formulate dimensionality reduction as a compression problem. They tried to solve the problem by building an explicit neural network encoder-decoder system which restricted the information implicitly by limiting the number of nodes in the bottleneck layer. Extend- ing their intuition with the tools of information theory, we recast dimensionality reduction as a compression problem where the bottleneck is the information available to manifold coordinates. This allows us to define the optimal manifold description as that which pro- duces the best reconstruction of the original data set, given that the coordinates can only be transmitted through a channel of fixed capacity. 3 Dimensionality reduction as compression Suppose that we have a data set X in a high dimensional state space RD described by a density function ρ(x). We would like to find a “simplified” description of this data set. One may do so by visualizing a lower dimensional manifold M that “almost” describes the data. If we have a manifold M and a stochastic map PM : x → PM(µ|x) to points µ on the manifold, we will say that they provide a manifold description of the data set X. Note that the stochastic map here is well justified: if a data point does not lie exactly on the manifold then we should expect some uncertainty in the estimation of the value of its latent variables. Also note that we do not need to specify the inverse (generative) map: M → RD; it can be obtained by Bayes’ rule. The manifold description (M, PM) is a less than faithful representation of the data. To formalize this notion we will introduce the distortion measure D(M, PM, ρ):

We argue that K–means and deterministic annealing algorithms for geo- metric clustering can be derived from the more general Information Bot- tleneck approach. If we cluster the identities of data points to preserve information about their location, the set of optimal solutions is massively degenerate. But if we treat the equations that define the optimal solution as an iterative algorithm, then a set of “smooth” initial conditions selects solutions with the desired geometrical properties. In addition to concep- tual unification, we argue that this approach can be more efficient and robust than classic algorithms.

A spiking neuron "computes" by transforming a complex dynamical input into a train of action potentials, or spikes. The computation performed by the neuron can be formulated as dimensional reduction, or feature detection, followed by a nonlinear decision function over the low-dimensional space. Generalizations of the reverse correlation technique with white noise input provide a numerical strategy for extracting the relevant low-dimensional features from experimental data, and information theory can be used to evaluate the quality of the low-dimensional approximation. We apply these methods to analyze the simplest biophysically realistic model neuron, the Hodgkin-Huxley (HH) model, using this system to illustrate the general methodological issues. We focus on the features in the stimulus that trigger a spike, explicitly eliminating the effects of interactions between spikes. One can approximate this triggering "feature space" as a two-dimensional linear subspace in the high-dimensional space of input histories, capturing in this way a substantial fraction of the mutual information between inputs and spike time. We find that an even better approximation, however, is to describe the relevant subspace as two dimensional but curved; in this way, we can capture 90% of the mutual information even at high time resolution. Our analysis provides a new understanding of the computational properties of the HH model. While it is common to approximate neural behavior as "integrate and fire," the HH model is not an integrator nor is it well described by a single threshold.

A population of neurons typically exhibits a broad diversity of responses to sensory inputs. The intuitive notion of functional classification is that cells can be clustered so that most of the diversity is captured by the iden- tity of the clusters rather than by individuals within clusters. We show how this intuition can be made precise using information theory, with- out any need to introduce a metric on the space of stimuli or responses. Applied to the retinal ganglion cells of the salamander, this approach re- covers classical results, but also provides clear evidence for subclasses beyond those identified previously. Further, we find that each of the gan- glion cells is functionally unique, and that even within the same subclass only a few spikes are needed to reliably distinguish between cells.

We study properties of popular near–uniform (Dirichlet) priors for learn- ing undersampled probability distributions on discrete nonmetric spaces and show that they lead to disastrous results. However, an Occam–style phase space argument expands the priors into their infinite mixture and resolves most of the observed problems. This leads to a surprisingly good estimator of entropies of discrete distributions. Learning a probability distribution from examples is one of the basic problems in data analysis. Common practical approaches introduce a family of parametric models, leading to questions about model selection. In Bayesian inference, computing the total probability of the data arising from a model involves an integration over parameter space, and the resulting “phase space volume” automatically discriminates against models with larger numbers of parameters—hence the description of these volume terms as Occam factors [1, 2]. As we move from finite parameterizations to models that are described by smooth functions, the integrals over parameter space become functional integrals and methods from quantum field theory allow us to do these integrals asymptotically; again the volume in model space consistent with the data is larger for models that are smoother and hence less complex [3]. Further, at least under some conditions the relevant degree of smoothness can be determined self–consistently from the data, so that we approach something like a model independent method for learning a distribution [4]. describe as the number of times ni each possibility is observed in a set of N =PK The results emphasizing the importance of phase space factors in learning prompt us to look back at a seemingly much simpler problem, namely learning a distribution on a dis- crete, nonmetric space. Here the probability distribution is just a list of numbers fqig, i = 1; 2;(cid:1)(cid:1)(cid:1) ; K, where K is the number of bins or possibilities. We do not assume any metric on the space, so that a priori there is no reason to believe that any qi and qj should be similar. The task is to learn this distribution from a set of examples, which we can i=1 ni samples. This problem arises in the context of language, where the index i might label words or phrases, so that there is no natural way to place a metric on the space, nor is it even clear that our intuitions about similarity are consistent with the constraints of a met- ric space. Similarly, in bioinformatics the index i might label n–mers of the the DNA or amino acid sequence, and although most work in the field is based on metrics for sequence comparison one might like an alternative approach that does not rest on such assumptions. In the analysis of neural responses, once we fix our time resolution the response becomes a set of discrete “words,” and estimates of the information content in the response are de- termined by the probability distribution on this discrete space. What all of these examples have in common is that we often need to draw some conclusions with data sets that are not in the asymptotic limit N (cid:29) K. Thus, while we might use a large corpus to sample the distribution of words in English by brute force (reaching N (cid:29) K with K the size of the vocabulary), we can hardly do the same for three or four word phrases. In models described by continuous functions, the infinite number of “possibilities” can never be overwhelmed by examples; one is saved by the notion of smoothness. Is there some nonmetric analog of this notion that we can apply in the discrete case? Our intuition is that information theoretic quantities may play this role. If we have a joint distribution of two variables, the analog of a smooth distribution would be one which does not have too much mutual information between these variables. Even more simply, we might say that smooth distributions have large entropy. While the idea of “maximum entropy inference” is common [5], the interplay between constraints on the entropy and the volume in the space of models seems not to have been considered. As we shall explain, phase space factors alone imply that seemingly sensible, more or less uniform priors on the space of discrete probability distributions correspond to disastrously singular prior hypotheses about the entropy of the underlying distribution. We argue that reliable inference outside the asymptotic regime N (cid:29) K requires a more uniform prior on the entropy, and we offer one way of doing this. While many distributions are consistent with the data when N (cid:20) K, we provide empirical evidence that this flattening of the entropic prior allows us to make surprisingly reliable statements about the entropy itself in this regime. At the risk of being pedantic, we state very explicitly what we mean by uniform or nearly uniform priors on the space of distributions. The natural “uniform” prior is given by

In nature, animals encounter high dimensional sensory stimuli that have complex statistical and dynamical structure. Attempts to study the neu- ral coding of these natural signals face challenges both in the selection of the signal ensemble and in the analysis of the resulting neural responses. For zebra finches, naturalistic stimuli can be defined as sounds that they encounter in a colony of conspecific birds. We assembled an ensemble of these sounds by recording groups of 10-40 zebra finches, and then ana- lyzed the response of single neurons in the songbird central auditory area (field L) to continuous playback of long segments from this ensemble. Following methods developed in the fly visual system, we measured the information that spike trains provide about the acoustic stimulus with- out any assumptions about which features of the stimulus are relevant. Preliminary results indicate that large amounts of information are carried by spike timing, with roughly half of the information accessible only at time resolutions better than 10 ms; additional information is still be- ing revealed as time resolution is improved to 2 ms. Information can be decomposed into that carried by the locking of individual spikes to the stimulus (or modulations of spike rate) vs. that carried by timing in spike patterns. Initial results show that in field L, temporal patterns give at least  % extra information. Thus, single central auditory neurons can pro- vide an informative representation of naturalistic sounds, in which spike timing may play a significant role.

We define predictive information I(pred)(T) as the mutual information between the past and the future of a time series. Three qualitatively different behaviors are found in the limit of large observation times T:I(pred)(T) can remain finite, grow logarithmically, or grow as a fractional power law. If the time series allows us to learn a model with a finite number of parameters, then I(pred)(T) grows logarithmically with a coefficient that counts the dimensionality of the model space. In contrast, power-law growth is associated, for example, with the learning of infinite parameter (or nonparametric) models such as continuous functions with smoothness constraints. There are connections between the predictive information and measures of complexity that have been defined both in learning theory and the analysis of physical systems through statistical mechanics and dynamical systems theory. Furthermore, in the same way that entropy provides the unique measure of available information consistent with some simple and plausible conditions, we argue that the divergent part of I(pred)(T) provides the unique measure for the complexity of dynamics underlying a time series. Finally, we discuss how these ideas may be useful in problems in physics, statistics, and biology.

In this paper we formulate a description of the computation per(cid:173) formed by a neuron as a combination of dimensional reduction and nonlinearity. We implement this description for the Hodgkin(cid:173) Huxley model, identify the most relevant dimensions and find the nonlinearity. A two dimensional description already captures a significant fraction of the information that spikes carry about dy(cid:173) namic inputs. This description also shows that computation in the Hodgkin-Huxley model is more complex than a simple integrate(cid:173) and-fire or perceptron model.

Many processes in biology, from the regulation of gene expression in bacteria to memory in the brain, involve switches constructed from networks of biochemical reactions. Crucial molecules are present in small numbers, raising questions about noise and stability. Analysis of noise in simple reaction schemes indicates that switches stable for years and switchable in milliseconds can be built from fewer than one hundred molecules. Prospects for direct tests of this prediction, as well as implications, are discussed.

Many neural systems extend their dynamic range by adaptation. We ex(cid:173) amine the timescales of adaptation in the context of dynamically mod(cid:173) ulated rapidly-varying stimuli, and demonstrate in the fly visual system that adaptation to the statistical ensemble of the stimulus dynamically maximizes information transmission about the time-dependent stimulus. Further, while the rate response has long transients, the adaptation takes place on timescales consistent with optimal variance estimation.

Learning of a smooth but nonparametric probability density can be reg(cid:173) ularized using methods of Quantum Field Theory. We implement a field theoretic prior numerically, test its efficacy, and show that the free pa(cid:173) rameter of the theory (,smoothness scale') can be determined self con(cid:173) sistently by the data; this forms an infinite dimensional generalization of the MDL principle. Finally, we study the implications of one's choice of the prior and the parameterization and conclude that the smoothness scale determination makes density estimation very weakly sensitive to the choice of the prior, and that even wrong choices can be advantageous for small data sets. One of the central problems in learning is to balance 'goodness of fit' criteria against the complexity of models. An important development in the Bayesian approach was thus the realization that there does not need to be any extra penalty for model complexity: if we compute the total probability that data are generated by a model, there is a factor from the volume in parameter space-the 'Occam factor' -that discriminates against models with more parameters [1, 2]. This works remarkably welJ for systems with a finite number of parameters and creates a complexity 'razor' (after 'Occam's razor') that is almost equiv(cid:173) alent to the celebrated Minimal Description Length (MDL) principle [3]. In addition, if the a priori distributions involved are strictly Gaussian, the ideas have also been proven to apply to some infinite-dimensional (nonparametric) problems [4]. It is not clear, however, what happens if we leave the finite dimensional setting to consider nonparametric prob(cid:173) lems which are not Gaussian, such as the estimation of a smooth probability density. A possible route to progress on the nonparametric problem was opened by noticing [5] that a Bayesian prior for density estimation is equivalent to a quantum field theory (QFT). In particular, there are field theoretic methods for computing the infinite dimensional analog of the Occam factor, at least asymptotically for large numbers of examples. These obser(cid:173) vations have led to a number of papers [6, 7, 8, 9] exploring alternative formulations and their implications for the speed of learning. Here we return to the original formulation of Ref. [5] and use numerical methods to address some of the questions left open by the analytic work [10]: What is the result of balancing the infinite dimensional Occam factor against the goodness of fit? Is the QFT inference optimal in using alJ of the information relevant for learning [II]? What happens if our learning problem is strongly atypical of the prior distribution? Following Ref. [5], if N i. i. d. samples {Xi}, i = 1 ... N, are observed, then the probability that a particular density Q(x) gave rise to these data is given by P[Q(x)] rr~1 Q(Xi)

The problem of neural coding is to understand how sequences of action potentials (spikes) are related to sensory stimuli, motor out(cid:173) puts, or (ultimately) thoughts and intentions. One clear question is whether the same coding rules are used by different neurons, or by corresponding neurons in different individuals. We present a quantitative formulation of this problem using ideas from informa(cid:173) tion theory, and apply this approach to the analysis of experiments in the fly visual system. We find significant individual differences in the structure of the code, particularly in the way that tempo(cid:173) ral patterns of spikes are used to convey information beyond that available from variations in spike rate. On the other hand, all the flies in our ensemble exhibit a high coding efficiency, so that every spike carries the same amount of information in all the individuals. Thus the neural code has a quantifiable mixture of individuality and universality.

We show that the information carried by compound events in neural spike trains-patterns of spikes across time or across a population of cells-can be measured, independent of assumptions about what these patterns might represent. By comparing the information carried by a compound pattern with the information carried independently by its parts, we directly measure the synergy among these parts. We illustrate the use of these methods by applying them to experiments on the motion-sensitive neuron H1 of the fly's visual system, where we confirm that two spikes close together in time carry far more than twice the information carried by a single spike. We analyze the sources of this synergy and provide evidence that pairs of spikes close together in time may be especially important patterns in the code of H1.

We show that a simple statistical mechanics model can capture the collective behavior of large networks of spiking neurons. Qualitative arguments suggest that regularly firing neurons should be described by a planar "spin" of unit length. We extract these spins from spike trains and then measure the interaction Hamiltonian using simulations of small clusters of cells. Correlations among spike trains obtained from simulations of large arrays of cells are in quantitative agreement with the predictions from these Hamiltonians. We comment on the novel computational abilities of these "XY networks."

In many biological systems the primary transduction of sensory stimuli occurs in a regular array of receptors. Because of this discrete sampling it is usually assumed that the organism has no knowledge of signals beyond the Nyquist frequency. In fact, higher frequency signals are expected to mask the available lower frequency information as a result of aliasing. It has been suggested that these considerations are important in understanding, for example, the design of the receptor lattice in the mammalian fovea. We show that if the organism has knowledge of the probability distribution from which the signals are drawn, outputs from a discrete receptor array can be used to estimate signals beyond the Nyquist limit. In effect, a priori knowledge can be used to de-alias the image, and the estimated signal above the Nyquist cutoff is in fact coherent with the real signal at these high frequencies. We address initially the problem of stimulus reconstruction from a noisy receptor array responding to a Gaussian stimulus ensemble. In this case, the best reconstruction strategy is a simple linear transformation. In the more interesting (and natural) case of nongaussian stimuli, optimal reconstruction requires nonlinear operations, but the higher order correlations in the stimulus ensemble can be used to improve the estimate of super-Nyquist signals.