arXiv subjects

Thierry Emonet

Publications and source records attributed to Thierry Emonet.

13 recordsLinked to original sources

arXiv2026

A behavior-environment information loop drives sensory navigation

As organisms navigate the environment to locate critical resources, their behavioral actions must be tightly coupled to their sensory inputs. Here, we introduce an information-theoretic framework that quantifies this coupling using transfer entropy, which measures information flow between sensory inputs and behavioral outputs. Information flow from sensory inputs to behavior defines a "reactive" component of a navigational strategy, whereas information flow from behavior to sensory inputs defines an "active" component, whereby actions shape subsequent sensory experiences. Analyzing these bidirectional information flows enables us to both predict navigational performance and dissect navigation strategies from trajectories. Using a minimal model that captures the active and reactive components, we connect macroscopic performance to microscopic information flows. We then apply the framework to experimentally measured trajectories of bacteria, worms, and flies, as well as to machine learning agents navigating sensory landscapes. Across systems, bidirectional information flow reliably predicts navigation efficiency, revealing a common behavioral-environment feedback loop. Decomposing active and reactive information flows further exposes distinct strategies underlying bacterial chemotaxis, the spatial dependency of the navigation strategy in fly olfactory navigation, and the learned policies of a reinforcement-trained agent. Together, these results establish bidirectional information flow as a unifying principle for understanding navigation in biological and artificial systems.

physics.bio-ph↗

arXiv2026

On the Information Required for Feedback Control

Biological systems across scales, along with many engineering problems, must control noisy systems with limited information. Here we study information-limited feedback control of stochastic systems to achieve target steady states, and derive a lower bound on the information rate from controlled system to controller. This framework allows us to obtain performance-information Pareto frontiers for wide-ranging control problems with limited information. For systems with state-independent passive dynamics, the bound is saturated by an explicit optimal control protocol which probabilistically time-reverses the passive dynamics. We showcase these results through applications to nonlinear particle localization, microbial navigation, and experimentally realized information engines.

cond-mat.stat-mech↗

arXiv2026

Discrete turn strategies emerge in information-limited navigation

Navigation up a smooth sensory gradient is one of the simplest behavioural tasks, and some organisms solve it by making continuous adjustments to their course. Bacteria instead employ a variety of discrete strategies, including run and tumble motion, direction reversals, and turns by specific angles. Here we ask what drives the choice of these strategies, framing the problem as maximising up-gradient speed with a given amount of sensory information per unit time. We find that, without directional information on which way to turn, behavioural strategies that take discrete actions perform better than gradual steering. As the amount of information is increased, we see a series of transitions between optimal strategies, including a shift from direction reversals to fully re-orienting tumbles. Among more complex re-orientation strategies, we show that discrete turn angles are best, and observe transitions in the number of angles employed by the optimal strategy. More broadly, such emergent simplicity in behaviour is a tractable example of a widespread phenomenon in which biology chooses a discrete solution, despite the underlying physics being continuous.

physics.bio-ph↗

arXiv2024

Bifurcation enhances temporal information encoding in the olfactory periphery

Living systems continually respond to signals from the surrounding environment. Survival requires that their responses adapt quickly and robustly to the changes in the environment. One particularly challenging example is olfactory navigation in turbulent plumes, where animals experience highly intermittent odor signals while odor concentration varies over many length- and timescales. Here, we show theoretically that Drosophila olfactory receptor neurons (ORNs) can exploit proximity to a bifurcation point of their firing dynamics to reliably extract information about the timing and intensity of fluctuations in the odor signal, which have been shown to be critical for odor-guided navigation. Close to the bifurcation, the system is intrinsically invariant to signal variance, and information about the timing, duration, and intensity of odor fluctuations is transferred efficiently. Importantly, we find that proximity to the bifurcation is maintained by mean adaptation alone and therefore does not require any additional feedback mechanism or fine-tuning. Using a biophysical model with calcium-based feedback, we demonstrate that this mechanism can explain the measured adaptation characteristics of Drosophila ORNs.

q-bio.NC↗

arXiv2024

Chemotaxing E. coli do not count single molecules

Organisms use specialized sensors to measure their environments, but the fundamental principles that determine their accuracy remain largely unknown. In Escherichia coli chemotaxis, we previously found that gradient-climbing speed is bounded by the amount of information that cells acquire from their environment, and that E. coli operate near this bound. However, it remains unclear what prevents them from acquiring more information. Past work argued that E. coli's chemosensing is limited by the physics of molecules stochastically arriving at cells' receptors, without direct evidence. Here, we show instead that E. coli are far from this physical limit. To show this, we develop a theoretical approach that uses information rates to quantify how accurately behaviorally-relevant signals can be estimated from available observations: molecule arrivals for the physical limit; chemotaxis signaling activity for E. coli. Measuring these information rates in single-cell experiments across multiple background concentrations, we find that E. coli encode two orders of magnitude less information than the physical limit. Thus, E. coli chemosensing is limited by internal noise in signal processing rather than the physics of molecule diffusion, motivating investigation of what specific physical and biological constraints shaped the evolution of this prototypical sensory system.

physics.bio-ph↗

arXiv2024

Lattice ultrasensitivity amplifies signals in E. coli without fine-tuning

The E. coli chemosensory lattice, consisting of receptors, kinases, and adaptor proteins, is an important test case for biochemical signal processing. Kinase output is characterized by precise adaptation to a wide range of background ligand levels and large gain in response to small relative changes in concentration. Existing models of this lattice achieve their gain through allosteric interactions between either receptors or core units of receptors and kinases. Here we introduce a model which operates through an entirely different mechanism in which receptors gate inherently far from equilibrium enzymatic reactions between neighboring kinases. Our lattice model achieves gain through a mechanism more closely related to zero-order ultrasensitivity than to allostery. Thus, we call it lattice ultrasensitivity (LU). Unlike other lattice critical models, the LU model can achieve arbitrarily high gain through time-scale separation, rather than through fine-tuning. The model also captures qualitative experimental results which are difficult to reconcile with existing models. We discuss possible implementations in the lattice's baseplate where long flexible linkers could potentially mediate interactions between neighboring core units.

physics.bio-ph↗

arXiv2021

E. coli chemotaxis is information-limited

Organisms must acquire and use environmental information to guide their behaviors. However, it is unclear whether and how information quantitatively limits behavioral performance. Here, we relate information to behavioral performance in Escherichia coli chemotaxis. First, we derive a theoretical limit for the maximum achievable gradient-climbing speed given a cell's information acquisition rate. Next, we measure cells' gradient-climbing speeds and the rate of information acquisition by the chemotaxis pathway. We find that E. coli make behavioral decisions with much less than the 1 bit required to determine whether they are swimming up-gradient. However, they use this information efficiently, performing near the theoretical limit. Thus, information can limit organisms' performance, and sensory-motor pathways may have evolved to efficiently use information from the environment.

physics.bio-ph↗

arXiv2017

Feedback Between Motion and Sensation Provides Nonlinear Boost in Run-and-tumble Navigation

Many organisms navigate gradients by alternating straight motions (runs) with random reorientations (tumbles), transiently suppressing tumbles whenever attractant signal increases. This induces a functional coupling between movement and sensation, since tumbling probability is controlled by the internal state of the organism which, in turn, depends on previous signal levels. Although a negative feedback tends to maintain this internal state close to adapted levels, positive feedback can arise when motion up the gradient reduces tumbling probability, further boosting drift up the gradient. Importantly, such positive feedback can drive large fluctuations in the internal state, complicating analytical approaches. Previous studies focused on what happens when the negative feedback dominates the dynamics. By contrast, we show here that there is a large portion of physiologically-relevant parameter space where the positive feedback can dominate, even when gradients are relatively shallow. We demonstrate how large transients emerge because of non-normal dynamics (non-orthogonal eigenvectors near a stable fixed point) inherent in the positive feedback, and further identify a fundamental nonlinearity that strongly amplifies their effect. Most importantly, this amplification is asymmetric, elongating runs in favorable directions and abbreviating others. The result is a "ratchet-like" gradient climbing behavior with drift speeds that can approach half the maximum run speed of the organism. Our results thus show that the classical drawback of run-and-tumble navigation --- wasteful runs in the wrong direction --- can be mitigated by exploiting the non-normal dynamics implicit in the run-and-tumble strategy.

q-bio.CB↗

arXiv2017

Non-genetic diversity modulates population performance

Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non-genetic diversity, it remains unclear how different phenotypes contribute to the performance of biological function at the population level. We developed a microfluidic device to simultaneously measure the phenotype and chemotactic performance of tens of thousands of individual, freely-swimming Escherichia coli as they climbed a gradient of attractant. We discovered that spatial structure spontaneously emerged from initially well-mixed wild type populations due to non-genetic diversity. By manipulating the expression of key chemotaxis proteins, we established a causal relationship between protein expression, non- genetic diversity, and performance that was theoretically predicted. This approach generated a complete phenotype-to-performance map, in which we found a nonlinear regime. We used this map to demonstrate how changing the shape of a phenotypic distribution can have as large of an effect on collective performance as changing the mean phenotype, suggesting that selection could act on both during the process of adaptation.

q-bio.CB↗

arXiv2015

Adaptability of non-genetic diversity in bacterial chemotaxis

Bacterial chemotaxis systems are as diverse as the environments that bacteria inhabit, but how much environmental variation can cells tolerate with a single system? Diversification of a single chemotaxis system could serve as an alternative, or even evolutionary stepping-stone, to switching between multiple systems. We hypothesized that mutations in gene regulation could lead to heritable control of chemotactic diversity. By simulating foraging and colonization of E. coli using a single-cell chemotaxis model, we found that different environments selected for different behaviors. The resulting trade-offs show that populations facing diverse environments would ideally diversify behaviors when time for navigation is limited. We show that advantageous diversity can arise from changes in the distribution of protein levels among individuals, which could occur through mutations in gene regulation. We propose experiments to test our prediction that chemotactic diversity in a clonal population could be a selectable trait that enables adaptation to environmental variability.

q-bio.PE↗

arXiv2014

Limits of feedback control in bacterial chemotaxis

Inputs to signaling pathways can have complex statistics that depend on the environment and on the behavioral response to previous stimuli. Such behavioral feedback is particularly important in navigation. Successful navigation relies on proper coupling between sensors, which gather information during motion, and actuators, which control behavior. Because reorientation conditions future inputs, behavioral feedback can place sensors and actuators in an operational regime different from the resting state. How then can organisms maintain proper information transfer through the pathway while navigating diverse environments? In bacterial chemotaxis, robust performance is often attributed to the zero integral feedback control of the sensor, which guarantees that activity returns to resting state when the input remains constant. While this property provides sensitivity over a wide range of signal intensities, it remains unclear how other parameters affect chemotactic performance, especially when considering that the swimming behavior of the cell determines the input signal. Using analytical models and simulations that incorporate recent experimental evidences about behavioral feedback and flagellar motor adaptation we identify an operational regime of the pathway that maximizes drift velocity for various environments and sensor adaptation rates. This optimal regime is outside the dynamic range of the motor response, but maximizes the contrast between run duration up and down gradients. In steep gradients, the feedback from chemotactic drift can push the system through a bifurcation. This creates a non-chemotactic state that traps cells unless the motor is allowed to adapt. Although motor adaptation helps, we find that as the strength of the feedback increases individual phenotypes cannot maintain the optimal operational regime in all environments, suggesting that diversity could be beneficial.

q-bio.MN↗

arXiv2013

Adaptation dynamics in densely clustered chemoreceptors

In many sensory systems, transmembrane receptors are spatially organized in large clusters. Such arrangement may facilitate signal amplification and the integration of multiple stimuli. However, this organization likely also affects the kinetics of signaling since the cytoplasmic enzymes that modulate the activity of the receptors must localize to the cluster prior to receptor modification. Here we examine how these spatial considerations shape signaling dynamics at rest and in response to stimuli. As a model, we use the chemotaxis pathway of Escherichia coli, a canonical system for the study of how organisms sense, respond, and adapt to environmental stimuli. In bacterial chemotaxis, adaptation is mediated by two enzymes that localize to the clustered receptors and modulate their activity through methylation-demethylation. Using a novel stochastic simulation, we show that distributive receptor methylation is necessary for successful adaptation to stimulus and also leads to large fluctuations in receptor activity in the steady state. These fluctuations arise from noise in the number of localized enzymes combined with saturated modification kinetics between localized enzymes and receptor substrate. An analytical model explains how saturated enzyme kinetics and large fluctuations can coexist with an adapted state robust to variation in the expression level of the pathway constituents, a key requirement to ensure the functionality of individual cells within a population. This contrasts with the well-mixed covalent modification system studied by Goldbeter and Koshland in which mean activity becomes ultrasensitive to protein abundances when the enzymes operate at saturation. Large fluctuations in receptor activity have been quantified experimentally. Here we clarify their mechanistic relationship with well-studied aspects of the chemotaxis system, precise adaptation and functional robustness.

q-bio.MN↗

arXiv2007

Relationship between cellular response and behavioral variability in bacterial chemotaxis

Bacterial chemotaxis in Escherichia coli is a canonical system for the study of signal transduction. A remarkable feature of this system is the coexistence of precise adaptation in population with large fluctuating cellular behavior in single cells (Korobkova et al. 2004, Nature, 428, 574). Using a stochastic model, we found that the large behavioral variability experimentally observed in non-stimulated cells is a direct consequence of the architecture of this adaptive system. Reversible covalent modification cycles, in which methylation and demethylation reactions antagonistically regulate the activity of receptor-kinase complexes, operate outside the region of first-order kinetics. As a result, the receptor-kinase that governs cellular behavior exhibits a sigmoidal activation curve. This curve simultaneously amplifies the inherent stochastic fluctuations in the system and lengthens the relaxation time in response to stimulus. Because stochastic fluctuations cause large behavioral variability and the relaxation time governs the average duration of runs in response to small stimuli, cells with the greatest fluctuating behavior also display the largest chemotactic response. Finally, Large-scale simulations of digital bacteria suggest that the chemotaxis network is tuned to simultaneously optimize the random spread of cells in absence of nutrients and the cellular response to gradients of attractant.

q-bio.MN↗