Biomechanics of transduction by mechanosensory cilia for prey detection in aquatic organisms.

Surface-feeding aquatic animals navigate towards the source of water disturbances and must differentiate prey from other environmental stimuli. Medicinal leeches locate prey, in part, using a distribution of mechanosensory hairs along their body that deflect under fluid flow. Leech's behavioral responses to surface wave temporal frequency are well documented. However, a surface wave's temporal frequency depends on many underlying environmental and fluid properties that vary substantially in natural habitats (e.g., water depth, temperature). The impact of these variables on neural response and behavior is unknown. Here, we developed a physics-based leech mechanosensor model to examine the impact of environmental and fluid properties on neural response. Our model used the physical properties of a leech cilium and was verified against existing behavioral and electrophysiological data. The model's peak response occurred with waves where the effects of gravity and surface tension were nearly equal (i.e., the phase velocity minimum). This suggests that preferred stimuli are related to the interaction between fundamental properties of the surrounding medium and the mechanical properties of the sensor. This interaction likely tunes the sensor to detect the nondispersive components of the signal, filtering out irrelevant ambient stimuli, and may be a general property of cilia across the animal kingdom.

Uncovering how animals use combinations of magnetic field properties to navigate: a computational approach.

Certain animal species use the earth's magnetic field (i.e., magnetoreception) in conjunction with other sensory modalities to navigate long distances. It is hypothesized that several animals use combinations of magnetic inclination and intensity as unique signatures for localization, potentially enabling migration without a pre-surveyed map. However, it is unknown how animals use magnetic signatures to generate guidance commands. While animal experiments have been invaluable in advancing this area, it is a difficult phenomenon to study in vivo or in situ. Modeling and simulation present a powerful complementary tool that can be used to investigate whether and how animals use magnetic signatures to navigate. This perspective article summarizes work we have conducted that systematically and mechanistically uses modeling and simulation to study the use of magnetic signatures. We have studied this phenomenon from simulated agents that navigate in simple and abstract environments, to physical devices that navigate in realistic environments. The results have consistently demonstrated that this is a plausible way in which animals might navigate, and provided early insights into the environmental and animal-specific factors that are most important to this navigation strategy.

A computational framework for studying energetics and resource management in sea turtle migration and autonomous systems.

Sea turtles complete migrations across vast distances, covering entire ocean basins. To track these migrations, satellite tracking tags are attached to their shells. The impact of these tags must be considered to ensure that turtles' natural behavior is not artificially and adversely impacted through tag-related drag, and that the data collected by a small sample of sea turtles accurately represents the larger population. Additionally, it can be difficult to study animal energetics in the field over large migration distances. In this work, we modify a computational behavior model to study how satellite tracking tags affect turtle migration behavior. Our agent based model contains synthetic magnetic field environments that are used for navigation cues, an ocean current, resource distributions that represent locations of food, and an agent that attempts to migrate to several different goals. The agent loses energy as it progresses, and searches for the resource distributions to replenish itself. Our novel simulation framework demonstrates the relationship between an agent's available energy capacity, its energy consumption based on mechanical power expended, and its ability to navigate to all migratory goal points. This study can be utilized to (1) probe the impacts of an animal's energy capacity and foraging behavior on its resulting navigation and ecology, (2) guide future satellite tag designs, and (3) develop usage recommendations for a suitable tracking tag based on the type of experiment being conducted. Our model can be expanded beyond sea turtles to study other marine species (e.g., sharks, whales). Additionally, this model could be expanded to other domains within the marine environment. For example, it could be modified to examine design trade-offs in remotely operated vehicles (ROVs), which share many of the same operational constraints as sea turtles and other migratory species.

Soft-surface grasping: radular opening in Aplysia californica.

Grasping soft, irregular material is challenging both for animals and robots. The feeding systems of many animals have adapted to this challenge. In particular, the feeding system of the marine mollusk Aplysia californica, a generalist herbivore, allows it to grasp and ingest seaweeds of varying shape, texture and toughness. On the surface of the grasper of A. californica is a structure known as the radula, a thin flexible cartilaginous sheet with fine teeth. Previous in vitro studies suggested that intrinsic muscles, I7, are responsible for opening the radula. Lesioning I7 in vivo does not prevent animals from grasping and ingesting food. New in vitro studies demonstrate that a set of fine muscle fibers on the ventral surface of the radula - the sub-radular fibers (SRFs) - mediate opening movements even if the I7 muscles are absent. Both in vitro and in vivo lesions demonstrate that removing the SRFs leads to profound deficits in radular opening, and significantly reduces feeding efficiency. A theoretical biomechanical analysis of the actions of the SRFs suggests that they induce the radular surface to open around a central crease in the radular surface and to arch the radular surface, allowing it to softly conform to irregular material. A three-dimensional model of the radular surface, based on in vivo observations and magnetic resonance imaging of intact animals, provides support for the biomechanical analysis. These results suggest how a soft grasper can work during feeding, and suggest novel designs for artificial soft graspers.

A bioinspired navigation strategy that uses magnetic signatures to navigate without GPS in a linearized northern Atlantic ocean: a simulation study.

Certain animal species use the Earth's magnetic field (i.e. magnetoreception) in conjunction with other sensory modalities to navigate long distances. It is hypothesized that several animals use combinations of magnetic inclination and intensity as unique signatures for localization, enabling migration without a pre-surveyed map. However, it is unknown how animals use magnetic signatures to generate guidance commands, and the extent to which species-specific capabilities and environmental factors affect a given strategy's efficacy or deterioration. Understanding animal magnetoreception can aid in developing better engineered navigation systems that are less reliant on satellites, which are expensive and can become unreliable or unavailable under a variety of circumstances. Building on previous studies, we implement an agent-based computer simulation that uses two variants of a magnetic signature-based navigation strategy. The strategy can successfully migrate to eight specified goal points in an environment that resembles the northern Atlantic ocean. In particular, one variant reaches all goal points with faster ocean current velocities, while the other variant reaches all goal points with slower ocean current velocities. We also employ dynamic systems tools to examine the stability of the strategy as a proxy for whether it is guaranteed to succeed. The findings demonstrate the efficacy of the strategy and can help in the development of new navigation technologies that are less reliant on satellites and pre-surveyed maps.

A Minimally Invasive Lesion Technique for Muscles Intrinsic to the Odontophore of Aplysia californica.

Aplysia californica is a model system for studying the neural control of learning and behavior. This animal has a semi-open circulatory system, making it possible to access many of its internal structures without causing any significant damage. Many manipulations can be easily performed both in vivo and in vitro, making it a highly tractable model for the analysis of behavior and neural circuitry. To better understand the functions of muscles within the feeding grasper, we have developed a technique for lesioning them without opening the main body cavity of the animal or damaging the outer layers of the feeding organ (i.e., the buccal mass). In this technique, the grasper is partially everted, allowing direct access to the musculature. This procedure allows animals to recover quickly and reliably. This has made it possible to lesion the I7 muscles and sub-radular fibers, allowing us to show that both muscles significantly contribute to the opening in vivo.

Dynameomics: a multi-dimensional analysis-optimized database for dynamic protein data.

The Dynameomics project is our effort to characterize the native-state dynamics and folding/unfolding pathways of representatives of all known protein folds by way of molecular dynamics simulations, as described by Beck et al. (in Protein Eng. Des. Select., the first paper in this series). The data produced by these simulations are highly multidimensional in structure and multi-terabytes in size. Both of these features present significant challenges for storage, retrieval and analysis. For optimal data modeling and flexibility, we needed a platform that supported both multidimensional indices and hierarchical relationships between related types of data and that could be integrated within our data warehouse, as described in the accompanying paper directly preceding this one. For these reasons, we have chosen On-line Analytical Processing (OLAP), a multi-dimensional analysis optimized database, as an analytical platform for these data. OLAP is a mature technology in the financial sector, but it has not been used extensively for scientific analysis. Our project is further more unusual for its focus on the multidimensional and analytical capabilities of OLAP rather than its aggregation capacities. The dimensional data model and hierarchies are very flexible. The query language is concise for complex analysis and rapid data retrieval. OLAP shows great promise for the dynamic protein analysis for bioengineering and biomedical applications. In addition, OLAP may have similar potential for other scientific and engineering applications involving large and complex datasets.

Dynameomics: design of a computational lab workflow and scientific data repository for protein simulations.

Dynameomics is a project to investigate and catalog the native-state dynamics and thermal unfolding pathways of representatives of all protein folds using solvated molecular dynamics simulations, as described in the preceding paper. Here we introduce the design of the molecular dynamics data warehouse, a scalable, reliable repository that houses simulation data that vastly simplifies management and access. In the succeeding paper, we describe the development of a complementary multidimensional database. A single protein unfolding or native-state simulation can take weeks to months to complete, and produces gigabytes of coordinate and analysis data. Mining information from over 3000 completed simulations is complicated and time-consuming. Even the simplest queries involve writing intricate programs that must be built from low-level file system access primitives and include significant logic to correctly locate and parse data of interest. As a result, programs to answer questions that require data from hundreds of simulations are very difficult to write. Thus, organization and access to simulation data have been major obstacles to the discovery of new knowledge in the Dynameomics project. This repository is used internally and is the foundation of the Dynameomics portal site http://www.dynameomics.org. By organizing simulation data into a scalable, manageable and accessible form, we can begin to address substantial questions that move us closer to solving biomedical and bioengineering problems.