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Antonio Carlos Costa

Publications and source records attributed to Antonio Carlos Costa.

8 recordsLinked to original sources

Unraveling phenotypic variation in multiscale behavioral dynamics

Behavioral variability reflects differences in internal and external parameters and provides a substrate for natural selection. However, uncovering its structure is challenging because behavior evolves nonlinearly across multiple timescales. Our goal is to reconstruct phenotypic variation from finite behavioral observations without prescribing the scales at which individuals should be compared. To achieve this, we introduce a multiscale dissimilarity that compares dynamics across all statistically resolvable resolutions by constructing reduced transfer operators at progressively finer scales and weighting their differences by finite-sampling uncertainty. This dissimilarity defines a geometry of dynamical phenotypes, which we reconstruct using diffusion maps. We show that the resulting phenotypic coordinates locally follow the parameter directions to which dynamics are most sensitive. We validate our approach in a stochastic model and apply it to bacterial and larval zebrafish behavior. In bacteria, we identify run speed as a major component of inter-individual variability, associated with the chemotaxis protein CheB. In zebrafish, we find that prior prey experience reshapes behavioral dynamics and phenotypic variability, with paramecia experience concentrating fish in a prey-capture-associated region of phenotypic space. Together, these results provide a framework for identifying internal and environmental variables that structure dynamical phenotypes across scales.

physics.bio-ph↗

Uncovering multiscale structure in the variability of larval zebrafish navigation

Animals chain movements into long-lived motor strategies, exhibiting variability across scales that reflects the interplay between internal states and environmental cues. To reveal structure in such variability, we build Markov models of movement sequences that bridges across time scales and enables a quantitative comparison of behavioral phenotypes among individuals. Applied to larval zebrafish responding to diverse sensory cues, we uncover a hierarchy of long-lived motor strategies, dominated by changes in orientation distinguishing cruising versus wandering strategies. Environmental cues induce preferences along these modes at the population level: while fish cruise in the light, they wander in response to aversive stimuli, or in search for appetitive prey. As our method encodes the behavioral dynamics of each individual fish in the transitions among coarse-grained motor strategies, we use it to uncover a hierarchical structure in the phenotypic variability that reflects exploration-exploitation trade-offs. Across a wide range of sensory cues, a major source of variation among fish is driven by prior and/or immediate exposure to prey that induces exploitation phenotypes. A large degree of variability that is not explained by environmental cues unravels motivational states that override the sensory context to induce contrasting exploration-exploitation phenotypes. Altogether, by extracting the timescales of motor strategies deployed during navigation, our approach exposes structure among individuals and reveals internal states tuned by prior experience.

physics.bio-ph↗

Fluctuating landscapes and heavy tails in animal behavior

Animal behavior is shaped by a myriad of mechanisms acting on a wide range of scales, which hampers quantitative reasoning and the identification of general principles. Here, we combine data analysis and theory to investigate the relationship between behavioral plasticity and heavy-tailed statistics often observed in animal behavior. Specifically, we first leverage high-resolution recordings of C. elegans locomotion to show that stochastic transitions among long-lived behaviors exhibit heavy-tailed first passage time distributions and correlation functions. Such heavy tails can be explained by slow adaptation of behavior over time. This particular result motivates our second step of introducing a general model where we separate fast dynamics on a quasi-stationary multi-well potential, from non-ergodic, slowly varying modes. We then show that heavy tails generically emerge in such a model, and we provide a theoretical derivation of the resulting functional form, which can become a power law with exponents that depend on the strength of the fluctuations. Finally, we provide direct support for the generality of our findings by testing them in a C. elegans mutant where adaptation is suppressed and heavy tails thus disappear, and recordings of larval zebrafish swimming behavior where heavy tails are again prevalent.

cond-mat.stat-mech↗

Statistics of C. elegans turning behavior reveals optimality under biasing constraints

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.

q-bio.NC↗

Maximally predictive states: from partial observations to long timescales

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 $C. elegans$.

physics.bio-ph↗

Adaptive, locally-linear models of complex dynamics

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.

q-bio.QM↗

Capturing the Continuous Complexity of Behavior in C. elegans

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.

q-bio.NC↗

Modeling the ballistic-to-diffusive transition in nematode motility reveals variation in exploratory behavior across species

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.

q-bio.NC↗