Biology subjects

Goldman, D. I.

Publications and source records attributed to Goldman, D. I..

11 recordsLinked to original sources

bioRxiv2024

Neuromechanical Phase Lags and Gait Adaptation in the Nematode C. elegans

Undulation is a locomotor strategy in which waves of bending propagate along the body.This form of locomotion is observed in organisms that span orders of magnitude in size and represent diverse habitats and species. Despite this diversity, common neuromechanical phenomena have been observed across biologically disparate undulators, due to common mechanics. For example, Neuromechanical Phase Lags (NPL), a phenomenon where waves of muscle contraction travel at different speeds than body bends, have been observed in fish, lamprey and lizards. Existing theoretical descriptions of this phenomenon implicate the role of physical body-environment interactions. However, systematic experimental variation of body-environment interactions and measurement of the corresponding phase lags has not been performed. Using the nematode Caenorhabditis elegans we measured muscle and body curvature dynamics simultaneously, performing calcium imaging in the body wall muscles while systematically varying the environmental rheology. A mechanical model demonstrates that the measured phase lags are controlled by the relative strength of elastic torques within the body and resistive forces within the medium. We further show that the phase lags correspond with a difference in the wavenumber of the muscle activity and curvature patterns. Hence, the environmental forces that create NPL also act as a filter that shapes and modulates the gait commanded by the nervous system. Beyond nematodes, the simplicity of our model further suggests that tuning body elasticity may serve as a general means of modulating the degree of mechanical control in other undulators.

biophysics↗

bioRxiv2022

Active and passive mechanics for rough terrain traversal in centipedes

Centipedes coordinate body and limb flexion to generate propulsion. On flat solid surfaces, the limb-stepping patterns can be characterized according to the direction in which limbaggregates propagate, opposite to (retrograde) or with the direction of motion (direct). It is unknown how limb and body dynamics are modified in terrain with terradynamic complexity more representative of their natural heterogeneous environments. Here, we investigated how centipedes that use retrograde and direct limp-stepping patterns, S. polymorpha and S. sexspinosus, respectively, coordinate their body and limbs to navigate laboratory environments which present footstep challenges and terrain rugosity. We recorded the kinematics and measured the locomotive performance of these animals traversing two rough terrains with randomly distributed step heights and compared the kinematics to those on a flat frictional surface. S. polymorpha exhibited similar body and limb dynamics across all terrains and a decrease in speed with increased terrain roughness. Unexpectedly, when placed in a rough terrain, S. sexspinosus changed the limb-stepping pattern from direct to retrograde. Further, for both species, traversal of rough terrains was facilitated by hypothesized passive mechanics: upon horizontal collision of a limb with a block, the limb passively bent and later continued the stepping pattern. While centipedes have many degrees of freedom. our results suggest these animals negotiate limb-substrate interactions and navigate complex terrains, by offloading complex control and leveraging the innate flexibility of their limbs.

animal behavior and cognition↗

bioRxiv2022

The rhizodynamics robot: Automated imaging system for studying long-term dynamic root growth

The study of plant root growth in real time has been difficult to achieve in an automated, high-throughput, and systematic fashion. Dynamic imaging of plant roots is important in order to discover novel root growth behaviors and to deepen our understanding of how roots interact with their environments. We designed and implemented the Generating Rhizodynamic Observations Over Time (GROOT) robot, an automated, high-throughput imaging system that enables time-lapse imaging of 90 containers of plants and their roots growing in a clear gel medium over the duration of weeks to months. The system uses low-cost, widely available materials. As a proof of concept, we employed GROOT to collect images of orchid root growth of multiple species over six months. Beyond imaging plant roots, our system is highly customizable and can be used to collect time-lapse image data of different container sizes and configurations regardless of what is being imaged, making it applicable to many fields that require longitudinal time-lapse recording.

plant biology↗

bioRxiv2021

Emergent collective locomotion in an active polymer model of entangled worm blobs

Numerous worm and arthropod species form physically-connected aggregations in which interactions among individuals give rise to emergent macroscale dynamics and functionalities that enhance collective survival. In particular, some aquatic worms such as the California blackworm (Lumbriculus variegatus) entangle their bodies into dense blobs to shield themselves against external stressors and preserve moisture in dry conditions. Motivated by recent experiments revealing emergent locomotion in blackworm blobs, we investigate the collective worm dynamics by modeling each worm as a self-propelled Brownian polymer. Though our model is two-dimensional, compared to real three-dimensional worm blobs, we demonstrate how a simulated blob can collectively traverse temperature gradients via the coupling between the active motion and the environment. By performing a systematic parameter sweep over the strength of attractive forces between worms, and the magnitude of their directed self-propulsion, we obtain a rich phase diagram which reveals that effective collective locomotion emerges as a result of finely balancing a tradeoff between these two parameters. Our model brings the physics of active filaments into a new meso- and macroscale context and invites further theoretical investigation into the collective behavior of long, slender, semi-flexible organisms.

biophysics↗

bioRxiv2021

A minimal robophysical model of quadriflagellate self-propulsion

Locomotion at the microscale is remarkably sophisticated. Microorganisms have evolved diverse strategies to move within highly viscous environments, using deformable, propulsion-generating appendages such as cilia and flagella to drive helical or undulatory motion. In single-celled algae, these appendages can be arranged in different ways around an approximately 10 {micro}m cell body, and coordinated in distinct temporal patterns. Inspired by the observation that some quadriflagellates (bearing four flagella) have an outwardly similar morphology and flagellar beat pattern, yet swim at different speeds, this study seeks to determine whether variations in swimming performance could arise solely from differences in swimming gait. Robotics approaches are particularly suited to such investigations, where the phase relationships between appendages can be readily manipulated. Here, we developed autonomous, algae-inspired robophysical models that can self-propel in a viscous fluid. These macroscopic robots (length and width = 8.5 cm, height = 2 cm) have four independently actuated flagella that oscillate back and forth under low-Reynolds number conditions (Re[~] [O] (10-1)). We tested the swimming performance of these robot models with appendages arranged in one of two distinct configurations, and coordinated in one of three distinct gaits. The gaits, namely the pronk, the trot, and the gallop, correspond to gaits adopted by distinct microalgal species. When the appendages are inserted perpendicularly around a central body, the robot achieved a net performance of 0.15 - 0.63 body lengths per cycle, with the trot gait being the fastest. Robotic swimming performance was found to be comparable to that of the algal microswimmers across all gaits. By creating a minimal robot that can successfully reproduce cilia-inspired drag-based swimming, our work paves the way for the design of next-generation devices that have the capacity to autonomously navigate aqueous environments.

biophysics↗

bioRxiv2021

Lateral Undulation Aids Biological and Robotic Earthworm Anchoring and Locomotion

Earthworms (Lumbricus terrestris) are characterized by soft, highly flexible and extensible bodies, and are capable of locomoting in most terrestrial environments. Previous studies of earthworm movement have focused on the use of retrograde peristaltic gaits in which controlled contraction of longitudinal and circular muscles results in waves of shortening/thickening and thinning/lengthening of the hydrostatic skeleton. These waves can propel the animal across ground as well as into soil. However, worms can also benefit from axial body bends during locomotion. Such lateral undulation dynamics can aid locomotor function via hooking/anchoring (to provide propulsion), modify travel orientation (to avoid obstacles and generate turns) and even generate snake-like undulatory locomotion in environments where peristaltic locomotion results in poor performance. To the best of our knowledge, the important aspects of locomotion associated with the lateral undulation of an earthworm body are yet to be systematically investigated. In this study, we observed that within confined environments, the worm uses lateral undulation to anchor its body to the walls of their burrows and tip (nose) bending to search the environment. This relatively simple locomotion strategy drastically improved the performance of our soft bodied robophysical model of the earthworm both in a confined (in an acrylic tube) and above-ground heterogeneous environment (rigid pegs), where the peristaltic gait often fails. In summary, lateral undulation facilitates the mobility of earthworm locomotion in diverse environments and can play an important role in the creation of low cost soft robotic devices capable of traversing a variety of environments.

animal behavior and cognition↗

bioRxiv2020

Collective protection and transport in entangled biological and robotic active matter

Living systems at all scales aggregate in large numbers for a variety of functions including mating, predation, and survival. The majority of such systems consist of unconnected individuals that collectively flock, school or swarm. However some aggregations involve physically entangled individuals, which can confer emergent mechanofunctional material properties to the collective. Here we study in laboratory experiments and rationalize in theoretical and robotic models the dynamics of physically entangled and motile self-assemblies of centimeter long California blackworms (L. Variegatus). Thousands of individual worms form braids with their long, slender and flexible bodies to make a three-dimensional, soft and shape-shifting blob. The blob behaves as a living material capable of mitigating damage and assault from environmental stresses through dynamic shape transformations, including minimizing surface area for survival against desiccation and enabling transport (negative thermotaxis) from hazardous environments (like heat). We specifically focus on the locomotion of the blob to understand how an amorphous entangled ball of worms is able to break symmetry to move across a substrate. We hypothesize that the collective blob displays rudimentary differentiation of function across itself, which when combined with entanglement dynamics facilitates directed persistent blob locomotion. To test this, we develop robophysical blobs, which display emergent locomotion in the collective without sophisticated control or programming of any individual robot. The emergent dynamics of the living functional blob and robophysical model can inform the rational design of exciting new classes of adaptive mechanofunctional living materials and emergent swarm robotics. Significance StatementLiving organisms form collectives across all scales, from bacteria to whales, enabling biological functions not accessible by individuals alone. In a few small cases, the individuals are physically connected to each other, forming to a new class of entangled active matter systems with emergent mechanofunctionalities of the collective. Here, we describe the dynamics of macroscopic aquatic worms that braid their long, soft bodies to form large entangled worm blobs. We discover that the worm blob behaves as a living material to undergo dynamic shape transformations to reduce evaporation or break-symmetry and locomote to safety against thermal stresses. We show that the persistent blob locomotion emerges as a consequence of physical entanglement and functional differentiation of individuals based on spatial location within a blob. We validate these principles in robophysical swarming blobs, that pave the way for new classes of mechanofunctional active matter systems and collective emergent robotics.

biophysics↗

bioRxiv2020

Mechanism and function of root circumnutation

AbstractEarly root growth is critical for plant establishment and survival. We have identified a molecular pathway required for oscillatory root tip movement known as circumnutation. Here we report a multiscale investigation of the regulation and function of this phenomenon. We identify key cell signaling events comprising interaction of the ethylene, cytokinin, and auxin hormone signaling pathways. We identify the gene Oryza sativa Histidine Kinase-1/OsHK1, as well as the auxin influx carrier gene OsAUX1, as essential regulators of this process in rice. Robophysical modelling demonstrated the benefits of tip movement for navigating past obstacles, prompting us to challenge mutant and wild-type plants with different substrates. Consistent with model behavior, root circumnutation facilitated exploration of a solid surface and promoted seedling establishment in rocky soil. Thus, the integration of robotics, physics and biology elucidated the functional importance of root circumnutation and uncovered the molecular mechanisms underlying its regulation. One sentence summaryCircumnutation facilitates root exploration.

plant biology↗

bioRxiv2020

Side-Impact Collision: Mechanics of Obstacle Negotiation in Sidewinding Snakes

Snakes excel at moving through cluttered environments, and heterogeneities can be used as propulsive contacts for snakes performing lateral undulation. However, sidewinding, often associated with sandy deserts, cuts a broad path through the environment that may increase the vulnerability to obstacles. Our prior work demonstrated that sidewinding can be represented as a pair of orthogonal body waves (vertical and horizontal) that can be independently modulated to achieve high maneuverability and incline ascent, suggesting that sidewinders may also use template modulations to negotiate obstacles. To test this hypothesis, we recorded overhead video of four sidewinder rattlesnakes (Crotalus cerastes) crossing a line of vertical pegs placed in the substrate. Snakes used three methods to traverse the obstacles: a Propagate Through behavior in which the lifted moving portion of the snake was deformed around the peg and dragged through as the snake continued sidewinding (115/160 runs), Reversal turns that reorient the snake entirely (35/160), or switching to Concertina locomotion (10/160). The Propagate-Through response was only used if the anterior-most region of static contact would propagate along a path anterior to the peg, or if a new region of static contact could be formed near the head to satisfy this condition; otherwise, snakes could only use Reversal Turns or switch to Concertina locomotion. Reversal Turns allowed the snake to re-orient and either escape without further peg contact or resorting to Propagate Through. We developed an algorithm to reproduce the Propagate Through behavior in a robotic model using a modulation of the two-wave template. This range of behavioral strategies provides sidewinders with a versatile range of options for effectively negotiating obstacles in their natural habitat, as well as provide insights into the design and control of robotic systems dealing with heterogeneous habitats.

animal behavior and cognition↗

bioRxiv2019

Mitigating memory effects during undulatory locomotion on hysteretic materials.

Undulatory swimming in flowing media like water is well-studied, but little is known about loco-motion in environments that are permanently deformed by body-substrate interactions like snakes in sand, eels in mud, and nematode worms in rotting fruit. We study the desert-specialist snake Chion-actis occipitalis traversing granular matter and find body inertia is negligible despite rapid transit and speed dependent granular reaction forces. New surface resistive force theory (RFT) calculation reveals how this snakes wave shape minimizes memory effects and optimizes escape performance given physiological limitations (power). RFT explains the morphology and waveform dependent performance of a diversity of non-sand-specialist, but overpredicts the capability of snakes with high slip. Robophysical experiments recapitulate aspects of these failure-prone snakes and elucidate how reencountering previously remodeled material hinders performance. This study reveals how memory effects stymied the locomotion of a diversity of snakes in our previous studies [Marvi et al, Science, 2014] and suggests the existence of a predictive model for history-dependent granular physics.

biophysics↗

bioRxiv2018

A histidine kinase gene is required for large radius root tip circumnutation and surface exploration in rice

The intricate growth patterns that accompany plant organ elongation have long intrigued biologists 1. Circumnutation refers to the circular or elliptical growth of the tip of a plant organ around a central axis. While the utility of circumnutation for climbing plants is clear, its function in roots is less obvious. Additionally, the genetic requirements for root circumnutation are not known. Here we show that mutations in a gene encoding a histidine kinase abolish large radius root tip circumnutation in rice. Using a gel-based imaging system and a whole genome sequenced mutant population, we identified three different mutant alleles of the gene OsHK1 that exhibit increased seedling root depth. Time-lapse imaging indicated that this phenotype is likely due to a lack of large radius root tip circumnutation in OsHK1 mutants. Treatment of mutant roots with the plant hormone zeatin rescues circumnutation, indicating that OsHK1 functions in a cytokinin-related signaling pathway. We found that OsHK1 mutants are impaired in their ability to explore flat surfaces, suggesting that circumnutation facilitates root exploration at the interface of compacted soil horizons.

plant biology↗