Nonlinear Poisson Effect Governed by a Mechanical Critical Transition.

Under extensional strain, fiber networks can exhibit an anomalously large and nonlinear Poisson effect accompanied by a dramatic transverse contraction and volume reduction for applied strains as small as a few percent. We demonstrate that this phenomenon is controlled by a collective mechanical phase transition that occurs at a critical uniaxial strain that depends on network connectivity. This transition is punctuated by an anomalous peak in the apparent Poisson's ratio and other critical signatures such as diverging nonaffine strain fluctuations.

Origin of Slow Stress Relaxation in the Cytoskeleton.

Dynamically cross-linked semiflexible biopolymers such as the actin cytoskeleton govern the mechanical behavior of living cells. Semiflexible biopolymers nonlinearly stiffen in response to mechanical loads, whereas the cross-linker dynamics allow for stress relaxation over time. Here we show, through rheology and theoretical modeling, that the combined nonlinearity in time and stress leads to an unexpectedly slow stress relaxation, similar to the dynamics of disordered systems close to the glass transition. Our work suggests that transient cross-linking combined with internal stress can explain prior reports of soft glassy rheology of cells, in which the shear modulus increases weakly with frequency.

Normal stress anisotropy and marginal stability in athermal elastic networks.

Hydrogels of semiflexible biopolymers such as collagen have been shown to contract axially under shear strain, in contrast to the axial dilation observed for most elastic materials. Recent work has shown that this behavior can be understood in terms of the porous, two-component nature and consequent time-dependent compressibility of hydrogels. The apparent normal stress measured by a torsional rheometer reflects only the tensile contribution of the axial component σzz on long (compressible) timescales, crossing over to the first normal stress difference, N1 = σxx - σzz at short (incompressible) times. While the behavior of N1 is well understood for isotropic viscoelastic materials undergoing affine shear deformation, biopolymer networks are often anisotropic and deform nonaffinely. Here, we numerically study the normal stresses that arise under shear in subisostatic, athermal semiflexible polymer networks. We show that such systems exhibit strong deviations from affine behavior and that these anomalies are controlled by a rigidity transition as a function of strain.

Reply to the 'Comment on "A symmetrical method to obtain shear moduli from microrheology"' by M. Tassieri, Soft Matter, 2018, 14, DOI.

The Comment on our paper introducing "a symmetric method to obtain shear moduli from microrheology" proposes an interpolation method to generate oversampled data from an original time series that are then used to approximate shear moduli at frequencies "beyond the Nyquist frequency." The author states that this can be done without the use of "preconceived fitting functions," implying that the results are unique and reliable. We disagree with these assertions. While it is possible to generate reasonable looking transforms at frequencies above the Nyquist limit by interpolation, any results obtained above the Nyquist limit will be questionable at best. Moreover, while the cubic spline interpolation the author uses may be standard, it constitutes a particular "preconceived" fit and produces oversampled data that are not unique.

Normal stresses in semiflexible polymer hydrogels.

Biopolymer gels such as fibrin and collagen networks are known to develop tensile axial stress when subject to torsion. This negative normal stress is opposite to the classical Poynting effect observed for most elastic solids including synthetic polymer gels, where torsion provokes a positive normal stress. As shown recently, this anomalous behavior in fibrin gels depends on the open, porous network structure of biopolymer gels, which facilitates interstitial fluid flow during shear and can be described by a phenomenological two-fluid model with viscous coupling between network and solvent. Here we extend this model and develop a microscopic model for the individual diagonal components of the stress tensor that determine the axial response of semiflexible polymer hydrogels. This microscopic model predicts that the magnitude of these stress components depends inversely on the characteristic strain for the onset of nonlinear shear stress, which we confirm experimentally by shear rheometry on fibrin gels. Moreover, our model predicts a transient behavior of the normal stress, which is in excellent agreement with the full time-dependent normal stress we measure.

A symmetrical method to obtain shear moduli from microrheology.

Passive microrheology typically deduces shear elastic loss and storage moduli from displacement time series or mean-squared displacements (MSD) of thermally fluctuating probe particles in equilibrium materials. Common data analysis methods use either Kramers-Kronig (KK) transformation or functional fitting to calculate frequency-dependent loss and storage moduli. We propose a new analysis method for passive microrheology that avoids the limitations of both of these approaches. In this method, we determine both real and imaginary components of the complex, frequency-dependent response function χ(ω) = χ'(ω) + iχ''(ω) as direct integral transforms of the MSD of thermal particle motion. This procedure significantly improves the high-frequency fidelity of χ(ω) relative to the use of KK transformation, which has been shown to lead to artifacts in χ'(ω). We test our method on both model and experimental data. Experiments were performed on solutions of worm-like micelles and dilute collagen solutions. While the present method agrees well with established KK-based methods at low frequencies, we demonstrate significant improvement at high frequencies using our symmetric analysis method, up to almost the fundamental Nyquist limit.

Porosity Governs Normal Stresses in Polymer Gels.

When sheared, most elastic solids including metals, rubbers, and polymer gels dilate perpendicularly to the shear plane. This behavior, known as the Poynting effect, is characterized by a positive normal stress. Surprisingly, fibrous biopolymer gels exhibit a negative normal stress under shear. Here we show that this anomalous behavior originates from the open-network structure of biopolymer gels. Using fibrin networks with a controllable pore size as a model system, we show that the normal-stress response to an applied shear is positive at short times, but decreases to negative values with a characteristic time scale set by pore size. Using a two-fluid model, we develop a quantitative theory that unifies the opposite behaviors encountered in synthetic and biopolymer gels.

Strain-driven criticality underlies nonlinear mechanics of fibrous networks.

Networks with only central force interactions are floppy when their average connectivity is below an isostatic threshold. Although such networks are mechanically unstable, they can become rigid when strained. It was recently shown that the transition from floppy to rigid states as a function of simple shear strain is continuous, with hallmark signatures of criticality [Sharma et al., Nature Phys. 12, 584 (2016)1745-247310.1038/nphys3628]. The nonlinear mechanical response of collagen networks was shown to be quantitatively described within the framework of such mechanical critical phenomenon. Here, we provide a more quantitative characterization of critical behavior in subisostatic networks. Using finite-size scaling we demonstrate the divergence of strain fluctuations in the network at well-defined critical strain. We show that the characteristic strain corresponding to the onset of strain stiffening is distinct from but related to this critical strain in a way that depends on critical exponents. We confirm this prediction experimentally for collagen networks. Moreover, we find that the apparent critical exponents are largely independent of the spatial dimensionality. With subisostaticity as the only required condition, strain-driven criticality is expected to be a general feature of biologically relevant fibrous networks.

Critical behaviour in the nonlinear elastic response of hydrogels.

In this paper we study the elastic response of synthetic hydrogels to an applied shear stress. The hydrogels studied here have previously been shown to mimic the behaviour of biopolymer networks when they are sufficiently far above the gel point. We show that near the gel point they exhibit an elastic response that is consistent with the predicted critical behaviour of networks near or below the isostatic point of marginal stability. This point separates rigid and floppy states, distinguished by the presence or absence of finite linear elastic moduli. Recent theoretical work has also focused on the response of such networks to finite or large deformations, both near and below the isostatic point. Despite this interest, experimental evidence for the existence of criticality in such networks has been lacking. Using computer simulations, we identify critical signatures in the mechanical response of sub-isostatic networks as a function of applied shear stress. We also present experimental evidence consistent with these predictions. Furthermore, our results show the existence of two distinct critical regimes, one of which arises from the nonlinear stretch response of semi-flexible polymers.

Broken Detailed Balance of Filament Dynamics in Active Networks.

Myosin motor proteins drive vigorous steady-state fluctuations in the actin cytoskeleton of cells. Endogenous embedded semiflexible filaments such as microtubules, or added filaments such as single-walled carbon nanotubes are used as novel tools to noninvasively track equilibrium and nonequilibrium fluctuations in such biopolymer networks. Here, we analytically calculate shape fluctuations of semiflexible probe filaments in a viscoelastic environment, driven out of equilibrium by motor activity. Transverse bending fluctuations of the probe filaments can be decomposed into dynamic normal modes. We find that these modes no longer evolve independently under nonequilibrium driving. This effective mode coupling results in nonzero circulatory currents in a conformational phase space, reflecting a violation of detailed balance. We present predictions for the characteristic frequencies associated with these currents and investigate how the temporal signatures of motor activity determine mode correlations, which we find to be consistent with recent experiments on microtubules embedded in cytoskeletal networks.

Nonlinear Mechanics of Athermal Branched Biopolymer Networks.

Naturally occurring biopolymers such as collagen and actin form branched fibrous networks. The average connectivity in branched networks is generally below the isostatic threshold at which central force interactions marginally stabilize the network. In the submarginal regime, for connectivity below this threshold, such networks are unstable toward small deformations unless stabilized by additional interactions such as bending. Here we perform a numerical study on the elastic behavior of such networks. We show that the nonlinear mechanics of branched networks is qualitatively similar to that of filamentous networks with freely hinged cross-links. In agreement with a recent theoretical study,1 we find that branched networks also exhibit nonlinear mechanics consistent with athermal critical phenomena controlled by strain. We obtain the critical exponents capturing the nonlinear elastic behavior near the critical point by performing scaling analysis of the stiffening curves. We find that the exponents evolve with the connectivity in the network. We show that the nonlinear mechanics of disordered networks, independent of the detailed microstructure, can be characterized by a strain-driven second-order phase transition, and that the primary quantitative differences among different architectures are in the critical exponents describing the transition.

On-site residence time in a driven diffusive system: Violation and recovery of a mean-field description.

We investigate simple one-dimensional driven diffusive systems with open boundaries. We are interested in the average on-site residence time defined as the time a particle spends on a given site before moving on to the next site. Using mean-field theory, we obtain an analytical expression for the on-site residence times. By comparing the analytic predictions with numerics, we demonstrate that the mean-field significantly underestimates the residence time due to the neglect of time correlations in the local density of particles. The temporal correlations are particularly long-lived near the average shock position, where the density changes abruptly from low to high. By using domain wall theory, we obtain highly accurate estimates of the residence time for different boundary conditions. We apply our analytical approach to residence times in a totally asymmetric exclusion process (TASEP), TASEP coupled to Langmuir kinetics (TASEP+LK), and TASEP coupled to mutually interactive LK (TASEP+MILK). The high accuracy of our predictions is verified by comparing these with detailed Monte Carlo simulations.

Elastic regimes of subisostatic athermal fiber networks.

Athermal models of disordered fibrous networks are highly useful for studying the mechanics of elastic networks composed of stiff biopolymers. The underlying network architecture is a key aspect that can affect the elastic properties of these systems, which include rich linear and nonlinear elasticity. Existing computational approaches have focused on both lattice-based and off-lattice networks obtained from the random placement of rods. It is not obvious, a priori, whether the two architectures have fundamentally similar or different mechanics. If they are different, it is not clear which of these represents a better model for biological networks. Here, we show that both approaches are essentially equivalent for the same network connectivity, provided the networks are subisostatic with respect to central force interactions. Moreover, for a given subisostatic connectivity, we even find that lattice-based networks in both two and three dimensions exhibit nearly identical nonlinear elastic response. We provide a description of the linear mechanics for both architectures in terms of a scaling function. We also show that the nonlinear regime is dominated by fiber bending and that stiffening originates from the stabilization of subisostatic networks by stress. We propose a generalized relation for this regime in terms of the self-generated normal stresses that develop under deformation. Different network architectures have different susceptibilities to the normal stress but essentially exhibit the same nonlinear mechanics. Such a stiffening mechanism has been shown to successfully capture the nonlinear mechanics of collagen networks.

Stability and anomalous entropic elasticity of subisostatic random-bond networks.

We study the elasticity of thermalized spring networks under an applied bulk strain. The networks considered are subisostatic random-bond networks that, in the athermal limit, are known to have vanishing bulk and linear shear moduli at zero bulk strain. Above a bulk strain threshold, however, these networks become rigid, although surprisingly the shear modulus remains zero until a second, higher, strain threshold. We find that thermal fluctuations stabilize all networks below the rigidity transition, resulting in systems with both finite bulk and shear moduli. Our results show a T(0.66) temperature dependence of the moduli in the region below the bulk strain threshold, resulting in networks with anomalously high rigidity as compared to ordinary entropic elasticity. Furthermore, we find a second regime of anomalous temperature scaling for the shear modulus at its zero-temperature rigidity point, where it scales as T(0.5), behavior that is absent for the bulk modulus since its athermal rigidity transition is discontinuous.

Inherently unstable networks collapse to a critical point.

Nonequilibrium systems that are driven or drive themselves towards a critical point have been studied for almost three decades. Here we present a minimalist example of such a system, motivated by experiments on collapsing active elastic networks. Our model of an unstable elastic network exhibits a collapse towards a critical point from any macroscopically connected initial configuration. Taking into account steric interactions within the network, the model qualitatively and quantitatively reproduces results of the experiments on collapsing active gels.

Nonthermal fluctuations of the mitotic spindle.

We present direct measurements of fluctuations in the nucleus of yeast cells. While prior work has shown these fluctuations to be active and non-thermal in character, their origin and time dependence are not understood. We show that the nuclear fluctuations we observe are quantitatively consistent with uncorrelated, active force fluctuations driving a nuclear medium that is dominated by an uncondensed DNA solution, for which we perform rheological measurements on an in vitro model system under similar conditions to what is expected in the nucleus.

Driven diffusive systems with mutually interactive Langmuir kinetics.

We investigate the simple one-dimensional driven model, the totally asymmetric exclusion process, coupled to mutually interactive Langmuir kinetics. This model is motivated by recent studies on clustering of motor proteins on microtubules. In the proposed model, the attachment and detachment rates of a particle are modified depending upon the occupancy of neighboring sites. We first obtain continuum mean-field equations and in certain limiting cases obtain analytic solutions. We show how mutual interactions increase (decrease) the effects of boundaries on the phase behavior of the model. We perform Monte Carlo simulations and demonstrate that our analytical approximations are in good agreement with the numerics over a wide range of model parameters. We present phase diagrams over a selective range of parameters.

Anomalous discontinuity at the percolation critical point of active gels.

We develop a percolation model motivated by recent experimental studies of gels with active network remodeling by molecular motors. This remodeling was found to lead to a critical state reminiscent of random percolation (RP), but with a cluster distribution inconsistent with RP. Our model not only can account for these experiments, but also exhibits an unusual type of mixed phase transition: We find that the transition is characterized by signatures of criticality, but with a discontinuity in the order parameter.

Elastic response of filamentous networks with compliant crosslinks.

Experiments have shown that elasticity of disordered filamentous networks with compliant crosslinks is very different from networks with rigid crosslinks. Here, we model and analyze filamentous networks as a collection of randomly oriented rigid filaments connected to each other by flexible crosslinks that are modeled as wormlike chains. For relatively large extensions we allow for enthalpic stretching of crosslink backbones. We show that for sufficiently high crosslink density, the network linear elastic response is affine on the scale of the filaments' length. The nonlinear regime can become highly nonaffine and is characterized by a divergence of the elastic modulus at finite strain. In contrast to the prior predictions, we do not find an asymptotic regime in which the differential elastic modulus scales linearly with the stress, although an approximate linear dependence can be seen in a transition from entropic to enthalpic regimes. We discuss our results in light of recent experiments.