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Ilya Nemenman

Publications and source records attributed to Ilya Nemenman.

At least 37 records · Page 2Linked to original sources

Extrinsic vs Intrinsic Criticality in Systems with Many Components

Biological systems with many components often exhibit seemingly critical behaviors, characterized by atypically large correlated fluctuations. Yet the underlying causes remain unclear. Here we define and examine two types of criticality. Intrinsic criticality arises from interactions within the system which are fine-tuned to a critical point. Extrinsic criticality, in contrast, emerges without fine tuning when observable degrees of freedom are coupled to unobserved fluctuating variables. We unify both types of criticality using the language of learning and information theory. We show that critical correlations, intrinsic or extrinsic, lead to diverging mutual information between two halves of the system, and are a feature of learning problems, in which the unobserved fluctuations are inferred from the observable degrees of freedom. We argue that extrinsic criticality is equivalent to standard inference, whereas intrinsic criticality describes fractional learning, in which the amount to be learned depends on the system size. We show further that both types of criticality are on the same continuum, connected by a smooth crossover. In addition, we investigate the observability of Zipf's law, a power-law rank-frequency distribution often used as an empirical signature of criticality. We find that Zipf's law is a robust feature of extrinsic criticality but can be nontrivial to observe for some intrinsically critical systems, including critical mean-field models. We further demonstrate that models with global dynamics, such as oscillatory models, can produce observable Zipf's law without relying on either external fluctuations or fine tuning. Our findings suggest that while possible in theory, fine tuning is not the only, nor the most likely, explanation for the apparent ubiquity of criticality in biological systems with many components.

physics.bio-ph↗

Bayesian estimation of the Kullback-Leibler divergence for categorical sytems using mixtures of Dirichlet priors

In many applications in biology, engineering and economics, identifying similarities and differences between distributions of data from complex processes requires comparing finite categorical samples of discrete counts. Statistical divergences quantify the difference between two distributions. However, their estimation is very difficult and empirical methods often fail, especially when the samples are small. We develop a Bayesian estimator of the Kullback-Leibler divergence between two probability distributions that makes use of a mixture of Dirichlet priors on the distributions being compared. We study the properties of the estimator on two examples: probabilities drawn from Dirichlet distributions, and random strings of letters drawn from Markov chains. We extend the approach to the squared Hellinger divergence. Both estimators outperform other estimation techniques, with better results for data with a large number of categories and for higher values of divergences.

stat.ME↗

Intrinsic Motivation in Dynamical Control Systems

Biological systems often choose actions without an explicit reward signal, a phenomenon known as intrinsic motivation. The computational principles underlying this behavior remain poorly understood. In this study, we investigate an information-theoretic approach to intrinsic motivation, based on maximizing an agent's empowerment (the mutual information between its past actions and future states). We show that this approach generalizes previous attempts to formalize intrinsic motivation, and we provide a computationally efficient algorithm for computing the necessary quantities. We test our approach on several benchmark control problems, and we explain its success in guiding intrinsically motivated behaviors by relating our information-theoretic control function to fundamental properties of the dynamical system representing the combined agent-environment system. This opens the door for designing practical artificial, intrinsically motivated controllers and for linking animal behaviors to their dynamical properties.

cs.AI↗

Low probability states, data statistics, and entropy estimation

A fundamental problem in analysis of complex systems is getting a reliable estimate of entropy of their probability distributions over the state space. This is difficult because unsampled states can contribute substantially to the entropy, while they do not contribute to the Maximum Likelihood estimator of entropy, which replaces probabilities by the observed frequencies. Bayesian estimators overcome this obstacle by introducing a model of the low-probability tail of the probability distribution. Which statistical features of the observed data determine the model of the tail, and hence the output of such estimators, remains unclear. Here we show that well-known entropy estimators for probability distributions on discrete state spaces model the structure of the low probability tail based largely on few statistics of the data: the sample size, the Maximum Likelihood estimate, the number of coincidences among the samples, the dispersion of the coincidences. We derive approximate analytical entropy estimators for undersampled distributions based on these statistics, and we use the results to propose an intuitive understanding of how the Bayesian entropy estimators work.

physics.data-an↗

Multi-dimensional structure of C. elegans thermal learning

Quantitative models of associative learning that explain the behavior of real animals with high precision have turned out very difficult to construct. We do this in the context of the dynamics of the thermal preference of C. elegans. For this, we quantify C. elegans thermotaxis in response to various conditioning parameters, genetic perturbations, and operant behavior using a fast, high-throughput microfluidic droplet assay. We then model this data comprehensively, within a new, biologically interpretable, multi-modal framework. We discover that the dynamics of thermal preference are described by two independent contributions and require a model with at least four dynamical variables. One pathway positively associates the experienced temperature independently of food and the other negatively associates to the temperature when food is absent.

physics.bio-ph↗

Ballistic deposition with memory: a new universality class of surface growth with a new scaling law

Motivated by recent experimental studies in microbiology, we suggest a modification of the classic ballistic deposition model of surface growth, where the memory of a deposition at a site induces more depositions at that site or its neighbors. By studying the statistics of surfaces in this model, we obtain three independent critical exponents: the growth exponent $β=5/4$, the roughening exponent $α= 2$, and the new (size) exponent $γ= 1/2$. The model requires a modification to the Family-Vicsek scaling, resulting in the dynamical exponent $z = \frac{α+γ}β = 2$. This modified scaling collapses the surface width vs time curves for various lattice sizes. This is a previously unobserved universality class of surface growth that could describe surface properties of a wide range of natural systems.

nlin.CG↗

Statistical properties of large data sets with linear latent features

Analytical understanding of how low-dimensional latent features reveal themselves in large-dimensional data is still lacking. We study this by defining a linear latent feature model with additive noise constructed from probabilistic matrices, and analytically and numerically computing the statistical distributions of pairwise correlations and eigenvalues of the correlation matrix. This allows us to resolve the latent feature structure across a wide range of data regimes set by the number of recorded variables, observations, latent features and the signal-to-noise ratio. We find a characteristic imprint of latent features in the distribution of correlations and eigenvalues and provide an analytic estimate for the boundary between signal and noise even in the absence of a clear spectral gap.

cond-mat.dis-nn↗

Inferring phenomenological models of first passage processes

Biochemical processes in cells are governed by complex networks of many chemical species interacting stochastically in diverse ways and on different time scales. Constructing microscopically accurate models of such networks is often infeasible. Instead, here we propose a systematic framework for building phenomenological models of such networks from experimental data, focusing on accurately approximating the time it takes to complete the process, the First Passage (FP) time. Our phenomenological models are mixtures of Gamma distributions, which have a natural biophysical interpretation. The complexity of the models is adapted automatically to account for the amount of available data and its temporal resolution. The framework can be used for predicting the behavior of various FP systems under varying external conditions. To demonstrate the utility of the approach, we build models for the distribution of inter-spike intervals of a morphologically complex neuron, a Purkinje cell, from experimental and simulated data. We demonstrate that the developed models can not only fit the data but also make nontrivial predictions. We demonstrate that our coarse-grained models provide constraints on more mechanistically accurate models of the involved phenomena.

q-bio.QM↗

Latent dynamical variables produce signatures of spatiotemporal criticality in large biological systems

Understanding the activity of large populations of neurons is difficult due to the combinatorial complexity of possible cell-cell interactions. To reduce the complexity, coarse-graining had been previously applied to experimental neural recordings, which showed over two decades of scaling in free energy, activity variance, eigenvalue spectra, and correlation time, hinting that the mouse hippocampus operates in a critical regime. We model the experiment by simulating conditionally independent binary neurons coupled to a small number of long-timescale stochastic fields and then replicating the coarse-graining procedure and analysis. This reproduces the experimentally-observed scalings, suggesting that they may arise from coupling the neural population activity to latent dynamic stimuli. Further, parameter sweeps for our model suggest that emergence of scaling requires most of the cells in a population to couple to the latent stimuli, predicting that even the celebrated place cells must also respond to non-place stimuli.

q-bio.NC↗

Unsupervised Bayesian Ising Approximation for revealing the neural dictionary in songbirds

The problem of deciphering how low-level patterns (action potentials in the brain, amino acids in a protein, etc.) drive high-level biological features (sensorimotor behavior, enzymatic function) represents the central challenge of quantitative biology. The lack of general methods for doing so from the size of datasets that can be collected experimentally severely limits our understanding of the biological world. For example, in neuroscience, some sensory and motor codes have been shown to consist of precisely timed multi-spike patterns. However, the combinatorial complexity of such pattern codes have precluded development of methods for their comprehensive analysis. Thus, just as it is hard to predict a protein's function based on its sequence, we still do not understand how to accurately predict an organism's behavior based on neural activity. Here we derive a method for solving this class of problems. We demonstrate its utility in an application to neural data, detecting precisely timed spike patterns that code for specific motor behaviors in a songbird vocal system. Our method detects such codewords with an arbitrary number of spikes, does so from small data sets, and accounts for dependencies in occurrences of codewords. Detecting such dictionaries of important spike patterns --- rather than merely identifying the timescale on which such patterns exist, as in some prior approaches --- opens the door for understanding fine motor control and the neural bases of sensorimotor learning in animals. For example, for the first time, we identify differences in encoding motor exploration versus typical behavior. Crucially, our method can be used not only for analysis of neural systems, but also for understanding the structure of correlations in other biological and nonbiological datasets.

q-bio.QM↗

Precise Spatial Memory in Local Random Networks

Self-sustained, elevated neuronal activity persisting on time scales of ten seconds or longer is thought to be vital for aspects of working memory, including brain representations of real space. Continuous-attractor neural networks, one of the most well-known modeling frameworks for persistent activity, have been able to model crucial aspects of such spatial memory. These models tend to require highly structured or regular synaptic architectures. In contrast, we elaborate a geometrically-embedded model with a local but otherwise random connectivity profile which, combined with a global regulation of the mean firing rate, produces localized, finely spaced discrete attractors that effectively span a 2D manifold. We demonstrate how the set of attracting states can reliably encode a representation of the spatial locations at which the system receives external input, thereby accomplishing spatial memory via attractor dynamics without synaptic fine-tuning or regular structure. We measure the network's storage capacity and find that the statistics of retrievable positions are also equivalent to a full tiling of the plane, something hitherto achievable only with (approximately) translationally invariant synapses, and which may be of interest in modeling such biological phenomena as visuospatial working memory in two dimensions.

q-bio.NC↗

Thermodynamic Computing

The hardware and software foundations laid in the first half of the 20th Century enabled the computing technologies that have transformed the world, but these foundations are now under siege. The current computing paradigm, which is the foundation of much of the current standards of living that we now enjoy, faces fundamental limitations that are evident from several perspectives. In terms of hardware, devices have become so small that we are struggling to eliminate the effects of thermodynamic fluctuations, which are unavoidable at the nanometer scale. In terms of software, our ability to imagine and program effective computational abstractions and implementations are clearly challenged in complex domains. In terms of systems, currently five percent of the power generated in the US is used to run computing systems - this astonishing figure is neither ecologically sustainable nor economically scalable. Economically, the cost of building next-generation semiconductor fabrication plants has soared past $10 billion. All of these difficulties - device scaling, software complexity, adaptability, energy consumption, and fabrication economics - indicate that the current computing paradigm has matured and that continued improvements along this path will be limited. If technological progress is to continue and corresponding social and economic benefits are to continue to accrue, computing must become much more capable, energy efficient, and affordable. We propose that progress in computing can continue under a united, physically grounded, computational paradigm centered on thermodynamics. Herein we propose a research agenda to extend these thermodynamic foundations into complex, non-equilibrium, self-organizing systems and apply them holistically to future computing systems that will harness nature's innate computational capacity. We call this type of computing "Thermodynamic Computing" or TC.

cs.CY↗

Randomly connected networks generate emergent selectivity and predict decoding properties of large populations of neurons

Advances in neural recording methods enable sampling from populations of thousands of neurons during the performance of behavioral tasks, raising the question of how recorded activity relates to the theoretical models of computations underlying performance. In the context of decision making in rodents, patterns of functional connectivity between choice-selective cortical neurons, as well as broadly distributed choice information in both excitatory and inhibitory populations, were recently reported [1]. The straightforward interpretation of these data suggests a mechanism relying on specific patterns of anatomical connectivity to achieve selective pools of inhibitory as well as excitatory neurons. We investigate an alternative mechanism for the emergence of these experimental observations using a computational approach. We find that a randomly connected network of excitatory and inhibitory neurons generates single-cell selectivity, patterns of pairwise correlations, and indistinguishable excitatory and inhibitory readout weight distributions, as observed in recorded neural populations. Further, we make the readily verifiable experimental predictions that, for this type of evidence accumulation task, there are no anatomically defined sub-populations of neurons representing choice, and that choice preference of a particular neuron changes with the details of the task. This work suggests that distributed stimulus selectivity and patterns of functional organization in population codes could be emergent properties of randomly connected networks.

q-bio.NC↗

Physical limit to concentration sensing in a changing environment

Cells adapt to changing environments by sensing ligand concentrations using specific receptors. The accuracy of sensing is ultimately limited by the finite number of ligand molecules bound by receptors. Previously derived physical limits to sensing accuracy have assumed that the concentration was constant and ignored its temporal fluctuations. We formulate the problem of concentration sensing in a strongly fluctuating environment as a non-linear field-theoretic problem, for which we find an excellent approximate Gaussian solution. We derive a new physical bound on the relative error in concentration $c$ which scales as $δc/c \sim (Dacτ)^{-1/4}$ with ligand diffusivity $D$, receptor cross-section $a$, and characteristic fluctuation time scale $τ$, in stark contrast with the usual Berg and Purcell bound $δc/c \sim (DacT)^{-1/2}$ for a perfect receptor sensing concentration during time $T$. We show how the bound can be achieved by a simple biochemical network downstream the receptor that adapts the kinetics of signaling as a function of the square root of the sensed concentration.

q-bio.SC↗

Universal properties of concentration sensing in large ligand-receptor networks

Cells estimate concentrations of chemical ligands in their environment using a limited set of receptors. Recent work has shown that the temporal sequence of binding and unbinding events on just a single receptor can be used to estimate the concentrations of multiple ligands. Here, for a network of many ligands and many receptors, we show that such temporal sequences can be used to estimate the concentration of a few times as many ligand species as there are receptors. Crucially, we show that the spectrum of the inverse covariance matrix of these estimates has several universal properties, which we trace to properties of Vandermonde matrices. We argue that this can be used by cells in realistic biochemical decoding networks.

q-bio.MN↗

Estimation of mutual information for real-valued data with error bars and controlled bias

Estimation of mutual information between (multidimensional) real-valued variables is used in analysis of complex systems, biological systems, and recently also quantum systems. This estimation is a hard problem, and universally good estimators provably do not exist. Kraskov et al. (PRE, 2004) introduced a successful mutual information estimation approach based on the statistics of distances between neighboring data points, which empirically works for a wide class of underlying probability distributions. Here we improve this estimator by (i) expanding its range of applicability, and by providing (ii) a self-consistent way of verifying the absence of bias, (iii) a method for estimation of its variance, and (iv) a criterion for choosing the values of the free parameter of the estimator. We demonstrate the performance of our estimator on synthetic data sets, as well as on neurophysiological and systems biology data sets.

q-bio.QM↗

Receptor crosstalk improves concentration sensing of multiple ligands

Cells need to reliably sense external ligand concentrations to achieve various biological functions such as chemotaxis or signaling. The molecular recognition of ligands by surface receptors is degenerate in many systems leading to crosstalk between different receptors. Crosstalk is often thought of as a deviation from optimal specific recognition, as the binding of non-cognate ligands can interfere with the detection of the receptor's cognate ligand, possibly leading to a false triggering of a downstream signaling pathway. Here we quantify the optimal precision of sensing the concentrations of multiple ligands by a collection of promiscuous receptors. We demonstrate that crosstalk can improve precision in concentration sensing and discrimination tasks. To achieve superior precision, the additional information about ligand concentrations contained in short binding events of the non-cognate ligand should be exploited. We present a proofreading scheme to realize an approximate estimation of multiple ligand concentrations that reaches a precision close to the derived optimal bounds. Our results help rationalize the observed ubiquity of receptor crosstalk in molecular sensing.

q-bio.SC↗

Automated, predictive, and interpretable inference of C. elegans escape dynamics

The roundworm C. elegans exhibits robust escape behavior in response to rapidly rising temperature. The behavior lasts for a few seconds, shows history dependence, involves both sensory and motor systems, and is too complicated to model mechanistically using currently available knowledge. Instead we model the process phenomenologically, and we use the Sir Isaac dynamical inference platform to infer the model in a fully automated fashion directly from experimental data. The inferred model requires incorporation of an unobserved dynamical variable, and is biologically interpretable. The model makes accurate predictions about the dynamics of the worm behavior, and it can be used to characterize the functional logic of the dynamical system underlying the escape response. This work illustrates the power of modern artificial intelligence to aid in discovery of accurate and interpretable models of complex natural systems.

q-bio.NC↗