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Animal locomotion is often subject to constraints arising from anatomical/physiological asymmetries. We use the nematode C.~elegans as a minimal model system to ask whether such constraints might shape locomotion patterns optimized during evolution. We focus on turning behaviours in two contrasting environmental contexts: (i) random exploration in the absence of strong stimuli and (ii) acute avoidance (escape) navigation upon encountering a strong aversive stimulus. We characterise the full repertoire of reorientation behaviours, including gradual reorientations and various posturally distinct sharp turns. During exploration, our measurements and theoretical modelling indicate that orientation fluctuations on short timescales are, on average, optimized to compensate the constraining gradual turn bias on long timescales. During escape, our data suggests that the reorientation is controlled not by an analog logic of continuous turn-amplitude modulations, but rather through the digital logic of selecting discrete turn types, leading to a symmetric escape performance despite strongly asymmetric turning biases., Comment: 32 pages, 17 figures

How do we capture the breadth of behavior in animal movement, from rapid body twitches to aging? Using high-resolution videos of the nematode worm $C. elegans$, we show that a single dynamics connects posture-scale fluctuations with trajectory diffusion, and longer-lived behavioral states. We take short posture sequences as an instantaneous behavioral measure, fixing the sequence length for maximal prediction. Within the space of posture sequences we construct a fine-scale, maximum entropy partition so that transitions among microstates define a high-fidelity Markov model, which we also use as a means of principled coarse-graining. We translate these dynamics into movement using resistive force theory, capturing the statistical properties of foraging trajectories. Predictive across scales, we leverage the longest-lived eigenvectors of the inferred Markov chain to perform a top-down subdivision of the worm's foraging behavior, revealing both "runs-and-pirouettes" as well as previously uncharacterized finer-scale behaviors. We use our model to investigate the relevance of these fine-scale behaviors for foraging success, recovering a trade-off between local and global search strategies., Comment: 28 pages, 15 figures

Isolating slower dynamics from fast fluctuations has proven remarkably powerful, but how do we proceed from partial observations of dynamical systems for which we lack underlying equations? Here, we construct maximally-predictive states by concatenating measurements in time, partitioning the resulting sequences using maximum entropy, and choosing the sequence length to maximize short-time predictive information. Transitions between these states yield a simple approximation of the transfer operator, which we use to reveal timescale separation and long-lived collective modes through the operator spectrum. Applicable to both deterministic and stochastic processes, we illustrate our approach through partial observations of the Lorenz system and the stochastic dynamics of a particle in a double-well potential. We use our transfer operator approach to provide a new estimator of the Kolmogorov-Sinai entropy, which we demonstrate in discrete and continuous-time systems, as well as the movement behavior of the nematode worm $C. elegans$., Comment: 22 pages, 14 figures

While measurement advances now allow extensive surveys of gene activity (large numbers of genes across many samples), interpretation of these data is often confounded by noise -- expression counts can differ strongly across samples due to variation of both biological and experimental origin. Complimentary to perturbation approaches, we extract functionally related groups of genes by analyzing the standing variation within a sampled population. To distinguish biologically meaningful patterns from uninterpretable noise, we focus on correlated variation and develop a novel density-based clustering approach that takes advantage of a percolation transition generically arising in random, uncorrelated data. We apply our approach to two contrasting RNA sequencing data sets that sample individual variation -- across single cells of fission yeast and whole animals of C. elegans worms -- and demonstrate robust applicability and versatility in revealing correlated gene clusters of diverse biological origin, including cell cycle phase, development/reproduction, tissue-specific functions, and feeding history. Our technique exploits generic features of noisy high-dimensional data and is applicable, beyond gene expression, to feature-rich data that sample population-level variability in the presence of noise., Comment: 13 pages, 8 figures

Animal behavior is often quantified through subjective, incomplete variables that may mask essential dynamics. Here, we develop a behavioral state space in which the full instantaneous state is smoothly unfolded as a combination of short-time posture dynamics. Our technique is tailored to multivariate observations and extends previous reconstructions through the use of maximal prediction. Applied to high-resolution video recordings of the roundworm \textit{C. elegans}, we discover a low-dimensional state space dominated by three sets of cyclic trajectories corresponding to the worm's basic stereotyped motifs: forward, backward, and turning locomotion. In contrast to this broad stereotypy, we find variability in the presence of locally-unstable dynamics, and this unpredictability shows signatures of deterministic chaos: a collection of unstable periodic orbits together with a positive maximal Lyapunov exponent. The full Lyapunov spectrum is symmetric with positive, chaotic exponents driving variability balanced by negative, dissipative exponents driving stereotypy. The symmetry is indicative of damped, driven Hamiltonian dynamics underlying the worm's movement control., Comment: 26 pages, 14 figures

Tracking large numbers of densely-arranged, interacting objects is challenging due to occlusions and the resulting complexity of possible trajectory combinations, as well as the sparsity of relevant, labeled datasets. Here we describe a novel technique of collective tracking in the model environment of a 2D honeybee hive in which sample colonies consist of $N\sim10^3$ highly similar individuals, tightly packed, and in rapid, irregular motion. Such a system offers universal challenges for multi-object tracking, while being conveniently accessible for image recording. We first apply an accurate, segmentation-based object detection method to build initial short trajectory segments by matching object configurations based on class, position and orientation. We then join these tracks into full single object trajectories by creating an object recognition model which is adaptively trained to recognize honeybee individuals through their visual appearance across multiple frames, an attribute we denote as pixel personality. Overall, we reconstruct ~46% of the trajectories in 5 min recordings from two different hives and over 71% of the tracks for at least 2 min. We provide validated trajectories spanning 3000 video frames of 876 unmarked moving bees in two distinct colonies in different locations and filmed with different pixel resolutions, which we expect to be useful in the further development of general-purpose tracking solutions., Comment: 13 pages, 4 main and 9 supplementary figures as well as a link to supplementary movies

The reliable detection of environmental molecules in the presence of noise is an important cellular function, yet the underlying computational mechanisms are not well understood. We introduce a model of two interacting sensors which allows for the principled exploration of signal statistics, cooperation strategies and the role of energy consumption in optimal sensing, quantified through the mutual information between the signal and the sensors. Here we report that in general the optimal sensing strategy depends both on the noise level and the statistics of the signals. For joint, correlated signals, energy consuming (nonequilibrium), asymmetric couplings result in maximum information gain in the low-noise, high-signal-correlation limit. Surprisingly we also find that energy consumption is not always required for optimal sensing. We generalise our model to incorporate time integration of the sensor state by a population of readout molecules, and demonstrate that sensor interaction and energy consumption remain important for optimal sensing., Comment: 9 pages, 5 figures, Forthcoming in Nature Communications

The dynamics of complex systems generally include high-dimensional, non-stationary and non-linear behavior, all of which pose fundamental challenges to quantitative understanding. To address these difficulties we detail a new approach based on local linear models within windows determined adaptively from the data. While the dynamics within each window are simple, consisting of exponential decay, growth and oscillations, the collection of local parameters across all windows provides a principled characterization of the full time series. To explore the resulting model space, we develop a novel likelihood-based hierarchical clustering and we examine the eigenvalues of the linear dynamics. We demonstrate our analysis with the Lorenz system undergoing stable spiral dynamics and in the standard chaotic regime. Applied to the posture dynamics of the nematode $C. elegans$ our approach identifies fine-grained behavioral states and model dynamics which fluctuate close to an instability boundary, and we detail a bifurcation in a transition from forward to backward crawling. Finally, we analyze whole-brain imaging in $C. elegans$ and show that the stability of global brain states changes with oxygen concentration., Comment: 25 pages, 16 figures

A deterministic population dynamics model involving birth and death for a two-species system, comprising a wild-type and more resistant species competing via logistic growth, is subjected to two distinct stress environments designed to mimic those that would typically be induced by temporal variation in the concentration of a drug (antibiotic or chemotherapeutic) as it permeates through the population and is progressively degraded. Different treatment regimes, involving single or periodical doses, are evaluated in terms of the minimal population size (a measure of the extinction probability), and the population composition (a measure of the selection pressure for resistance or tolerance during the treatment). We show that there exist timescales over which the low-stress regime is as effective as the high-stress regime, due to the competition between the two species. For multiple periodic treatments, competition can ensure that the minimal population size is attained during the first pulse when the high-stress regime is short, which implies that a single short pulse can be more effective than a more protracted regime. Our results suggest that when the duration of the high-stress environment is restricted, a treatment with one or multiple shorter pulses can produce better outcomes than a single long treatment. If ecological competition is to be exploited for treatments, it is crucial to determine these timescales, and estimate for the minimal population threshold that suffices for extinction. These parameters can be quantified by experiment.

From human crowds to cells in tissue, the detection and efficient tracking of multiple objects in dense configurations is an important and unsolved problem. In the past, limitations of image analysis have restricted studies of dense groups to tracking a single or subset of marked individuals, or to coarse-grained group-level dynamics, all of which yield incomplete information. Here, we combine convolutional neural networks (CNNs) with the model environment of a honeybee hive to automatically recognize all individuals in a dense group from raw image data. We create new, adapted individual labeling and use the segmentation architecture U-Net with a loss function dependent on both object identity and orientation. We additionally exploit temporal regularities of the video recording in a recurrent manner and achieve near human-level performance while reducing the network size by 94% compared to the original U-Net architecture. Given our novel application of CNNs, we generate extensive problem-specific image data in which labeled examples are produced through a custom interface with Amazon Mechanical Turk. This dataset contains over 375,000 labeled bee instances across 720 video frames at 2 FPS, representing an extensive resource for the development and testing of tracking methods. We correctly detect 96% of individuals with a location error of ~7% of a typical body dimension, and orientation error of 12 degrees, approximating the variability of human raters. Our results provide an important step towards efficient image-based dense object tracking by allowing for the accurate determination of object location and orientation across time-series image data efficiently within one network architecture., Comment: 15 pages, including supplementary figures. 1 supplemental movie available as an ancillary file

We exploit the reduced space of C. elegans postures to develop a novel tracking algorithm which captures both simple shapes and also self-occluding coils, an important, yet unexplored, component of worm behavior. We apply our algorithm to show that visually complex, coiled sequences are a superposition of two simpler patterns: the body wave dynamics and a head-curvature pulse. We demonstrate the precise coiled dynamics of an escape response and uncover new behaviors in spontaneous, large amplitude coils; deep reorientations occur through classical Omega-shaped postures and also through larger, new postural excitations which we label here as delta-turns. We find that omega and delta turns occur independently, the serpentine analog of a random left-right step, suggesting a distinct triggering mechanism. We also show that omega and delta turns display approximately equal rates and adapt to food-free conditions on a similar timescale, a simple strategy to avoid navigational bias., Comment: 14 pages and 8 figures, including supplementary information

With the advent of online networks, societies are substantially more connected with individual members able to easily modify and maintain their own social links. Here, we show that active network maintenance exposes agents to confirmation bias, the tendency to confirm one's beliefs, and we explore how this affects collective opinion formation. We introduce a model of binary opinion dynamics on a complex network with fast, stochastic rewiring and show that confirmation bias induces a segregation of individuals with different opinions. We use the dynamics of global opinion to generally categorize opinion update rules and find that confirmation bias always stabilizes the consensus state. Finally, we show that the time to reach consensus has a non-monotonic dependence on the magnitude of the bias, suggesting a novel avenue for large-scale opinion engineering., Comment: 6 pages, 4 figures

A quantitative understanding of organism-level behavior requires predictive models that can capture the richness of behavioral phenotypes, yet are simple enough to connect with underlying mechanistic processes. Here we investigate the motile behavior of nematodes at the level of their translational motion on surfaces driven by undulatory propulsion. We broadly sample the nematode behavioral repertoire by measuring motile trajectories of the canonical lab strain $C. elegans$ N2 as well as wild strains and distant species. We focus on trajectory dynamics over timescales spanning the transition from ballistic (straight) to diffusive (random) movement and find that salient features of the motility statistics are captured by a random walk model with independent dynamics in the speed, bearing and reversal events. We show that the model parameters vary among species in a correlated, low-dimensional manner suggestive of a common mode of behavioral control and a trade-off between exploration and exploitation. The distribution of phenotypes along this primary mode of variation reveals that not only the mean but also the variance varies considerably across strains, suggesting that these nematode lineages employ contrasting ``bet-hedging'' strategies for foraging., Comment: 46 pages, 18 figures, 6 tables

For an understanding of DNA elasticity at high mechanical loads (F > 30 pN), its helical nature needs to be taken into account, in the form of coupling between the twist and stretch degrees of freedom. The prevailing model for DNA elasticity, the worm-like chain, was previously extended to include this twist-stretch coupling, giving rise to the twistable worm-like chain. Motivated by DNA's charged nature, and the known effects of ionic charges on the molecule's persistence length and stretch modulus, we explored the impact of buffer ionic conditions on twist-stretch coupling. After developing a robust fitting approach for force-extension data, we find that DNA's helical twist is stabilized at high concentrations of the magnesium divalent cation., Comment: 4 pages, 5 figures

What fascinates us about animal behavior is its richness and complexity, but understanding behavior and its neural basis requires a simpler description. Traditionally, simplification has been imposed by training animals to engage in a limited set of behaviors, by hand scoring behaviors into discrete classes, or by limiting the sensory experience of the organism. An alternative is to ask whether we can search through the dynamics of natural behaviors to find explicit evidence that these behaviors are simpler than they might have been. We review two mathematical approaches to simplification, dimensionality reduction and the maximum entropy method, and we draw on examples from different levels of biological organization, from the crawling behavior of C. elegans to the control of smooth pursuit eye movements in primates, and from the coding of natural scenes by networks of neurons in the retina to the rules of English spelling. In each case, we argue that the explicit search for simplicity uncovers new and unexpected features of the biological system, and that the evidence for simplification gives us a language with which to phrase new questions for the next generation of experiments. The fact that similar mathematical structures succeed in taming the complexity of very different biological systems hints that there is something more general to be discovered.

Animal behaviors are sometimes decomposable into discrete, stereotyped elements. In one model, such behaviors are triggered by specific commands; in the extreme case, the discreteness of behavior is traced to the discreteness of action potentials in the individual command neurons. We use the crawling behavior of the nematode C. elegans to explore the opposite extreme, in which discreteness and stereotypy emerges from the dynamics of the entire behavior. A simple stochastic model for the worm's continuously changing body shape during crawling has attractors corresponding to forward and backward motion; noise-driven transitions between these attractors correspond to abrupt reversals. We show that, with no free parameters, this model generates reversals at a rate within error bars of that observed experimentally, and the relatively stereotyped trajectories in the neighborhood of the reversal also are predicted correctly.

Organisms move through the world by changing their shape, and here we explore the mapping from shape space to movements in the nematode C. elegans as it crawls on a planar agar surface. We characterize the statistics of the trajectories through the correlation functions of the orientation angular velocity, orientation angle and the mean-squared displacement, and we find that the loss of orientational memory has significant contributions from both abrupt, large amplitude turning events and the continuous dynamics between these events. Further, we demonstrate long-time persistence of orientational memory in the intervals between abrupt turns. Building on recent work demonstrating that C. elegans movements are restricted to a low-dimensional shape space, we construct a map from the dynamics in this shape space to the trajectory of the worm along the agar. We use this connection to illustrate that changes in the continuous dynamics reveal subtle differences in movement strategy that occur among mutants defective in two classes of dopamine receptors.

The scale invariance of natural images suggests an analogy to the statistical mechanics of physical systems at a critical point. Here we examine the distribution of pixels in small image patches and show how to construct the corresponding thermodynamics. We find evidence for criticality in a diverging specific heat, which corresponds to large fluctuations in how "surprising" we find individual images, and in the quantitative form of the entropy vs. energy. The energy landscape derived from our thermodynamic framework identifies special image configurations that have intrinsic error correcting properties, and neurons which could detect these features have a strong resemblance to the cells found in primary visual cortex.

We consider words as a network of interacting letters, and approximate the probability distribution of states taken on by this network. Despite the intuition that the rules of English spelling are highly combinatorial (and arbitrary), we find that maximum entropy models consistent with pairwise correlations among letters provide a surprisingly good approximation to the full statistics of four letter words, capturing ~92% of the multi-information among letters and even "discovering" real words that were not represented in the data from which the pairwise correlations were estimated. The maximum entropy model defines an energy landscape on the space of possible words, and local minima in this landscape account for nearly two-thirds of words used in written English.

Functional Magnetic Resonance Imaging (fMRI) provides dynamical access into the complex functioning of the human brain, detailing the hemodynamic activity of thousands of voxels during hundreds of sequential time points. One approach towards illuminating the connection between fMRI and cognitive function is through decoding; how do the time series of voxel activities combine to provide information about internal and external experience? Here we seek models of fMRI decoding which are balanced between the simplicity of their interpretation and the effectiveness of their prediction. We use signals from a subject immersed in virtual reality to compare global and local methods of prediction applying both linear and nonlinear techniques of dimensionality reduction. We find that the prediction of complex stimuli is remarkably low-dimensional, saturating with less than 100 features. In particular, we build effective models based on the decorrelated components of cognitive activity in the classically-defined Brodmann areas. For some of the stimuli, the top predictive areas were surprisingly transparent, including Wernicke's area for verbal instructions, visual cortex for facial and body features, and visual-temporal regions for velocity. Direct sensory experience resulted in the most robust predictions, with the highest correlation ($c \sim 0.8$) between the predicted and experienced time series of verbal instructions. Techniques based on non-linear dimensionality reduction (Laplacian eigenmaps) performed similarly. The interpretability and relative simplicity of our approach provides a conceptual basis upon which to build more sophisticated techniques for fMRI decoding and offers a window into cognitive function during dynamic, natural experience., Comment: To appear in: Advances in Neural Information Processing Systems 20, Scholkopf B., Platt J. and Hofmann T. (Editors), MIT Press, 2008

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 C. elegans is surprisingly low dimensional, with just four dimensions accounting for 95% of the shape variance, 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., Comment: 9 pages, 6 figures, minor corrections

We apply an information theoretic treatment of action potential time series measured with microelectrode arrays to estimate the connectivity of mammalian neuronal cell assemblies grown {\it in vitro}. We infer connectivity between two neurons via the measurement of the mutual information between their spike trains. In addition we measure higher point multi-informations between any two spike trains conditional on the activity of a third cell, as a means to identify and distinguish classes of functional connectivity among three neurons. The use of a conditional three-cell measure removes some interpretational shortcomings of the pairwise mutual information and sheds light into the functional connectivity arrangements of any three cells. We analyze the resultant connectivity graphs in light of other complex networks and demonstrate that, despite their {\it ex vivo} development, the connectivity maps derived from cultured neural assemblies are similar to other biological networks and display nontrivial structure in clustering coefficient, network diameter and assortative mixing. Specifically we show that these networks are weakly disassortative small world graphs, which differ significantly in their structure from randomized graphs with the same degree. We expect our analysis to be useful in identifying the computational motifs of a wide variety of complex networks, derived from time series data., Comment: 12 pages, 5 figures

Using both analytical arguments and detailed numerical evidence we show that the first order transition in the type-I 2D Abelian Higgs model can be understood in terms of the statistical mechanics of vortices, which behave in this regime as an ensemble of attractive particles. The well-known instabilities of such ensembles are shown to be connected to the process of phase nucleation. By characterizing the equation of state for the vortex ensemble we show that the temperature for the onset of a clustering instability is in qualitative agreement with the critical temperature. Below this point the vortex ensemble collapses to a single cluster, which is a non-extensive phase, and disappears in the absence of net topological charge. The vortex description provides a detailed mechanism for the first order transition, which applies at arbitrarily weak type-I and is gauge invariant unlike the usual field-theoretic considerations, which rely on asymptotically large gauge coupling., Comment: 4 pages, 6 figures, uses RevTex. Additional references added, some small corrections to the text