TEMPLATES AND ANCHORS: NEUROMECHANICAL HYPOTHESES OF LEGGED LOCOMOTION ON LAND

Locomotion results from complex, high-dimensional, non-linear, dynamically coupled interactions between an organism and its environment. Fortunately, simple models we call templates have been and can be made to resolve the redundancy of multiple legs, joints and muscles by seeking synergies and symmetries. A template is the simplest model (least number of variables and parameters) that exhibits a targeted behavior. For example, diverse species that differ in skeletal type, leg number and posture run in a stable manner like sagittal- and horizontal-plane spring-mass systems. Templates suggest control strategies that can be tested against empirical data. Templates must be grounded in more detailed morphological and physiological models to ask specific questions about multiple legs, the joint torques that actuate them, the recruitment of muscles that produce those torques and the neural networks that activate the ensemble. We term these more elaborate models anchors. They introduce representations of specific biological details whose mechanism of coordination is of interest. Since mechanisms require controls, anchors incorporate specific hypotheses concerning the manner in which unnecessary motion or energy from legs, joints and muscles is removed,leaving behind the behavior of the body in the low-degree-of-freedom template. Locating the origin of control is a challenge because neural and mechanical systems are dynamically coupled and both playa role. The control of slow, variable-frequency locomotion appears to be dominated by the nervous system, whereas during rapid, rhythmic locomotion, the control may reside more within the mechanical system. Anchored templates of many legged, sprawled-postured animals suggest that passive, dynamic self-stabilization from a feedforward, tuned mechanical system can reject rapid perturbations and simplify control. Future progress would benefit from the creation of a field embracing comparative neuromechanics

Static Forces and Moments Generated in the Insect Leg: Comparison of a Three-Dimensional Musculo-Skeletal Computer Model With Experimental Measurements

As a first step towards the integration of information on neural control, biomechanics and isolated muscle function, we constructed a three-dimensional musculo-skeletal model of the hind leg of the death-head cockroach Blaberus discoidalis. We tested the model by measuring the maximum force generated in vivo by the hind leg of the cockroach, the coxa-femur joint angle and the position of this leg during a behavior, wedging, that was likely to require maximum torque or moment production. The product of the maximum force of the leg and its moment arm yielded a measured coxa-femur joint moment for wedging behavior. The maximum musculo-apodeme moment predicted by summing all extensor muscle moments in the model was adequate to explain the magnitude of the coxa-femur joint moment produced in vivo by the cockroach and occurred at the same joint angle measured during wedging. Active isometric muscle forces predicted from our model varied by 3.5-fold among muscles and by as much as 70% with joint angle. Sums of active and passive forces varied by less than 3.5% over the entire range of possible joint angles (0-125º). Maximum musculo-apodeme moment arms varied nearly twofold among muscles. Moment arm lengths decreased to zero and switched to the opposite side of the center of rotation at joint angles within the normal range of motion. At large joint angles (\u3e100º), extensors acted as flexors. The effective mechanical advantage (musculo-apodeme moment arm/leg moment arm = 0.10) resulted in the six femoral extensor muscles of the model developing a summed force (1.4N) equal to over 50 times the body weight. The model\u27s three major force-producing extensor muscles attained 95% of their maximum force, moment arm and moment at the joint angle used by the animal during wedging

A Motor and a Brake: Two Leg Extensor Muscles Acting at the Same Joint Manage Energy Differently in a Running Insect

The individual muscles of a multiple muscle group at a given joint are often assumed to function synergistically to share the load during locomotion. We examined two leg extensors of a running cockroach to test the hypothesis that leg muscles within an anatomical muscle group necessarily manage (i.e. produce, store, transmit or absorb) energy similarly during running. Using electromyographic and video motion-analysis techniques, we determined that muscles 177c and 179 are both active during the first half of the stance period during muscle shortening. Using the in vivo strain and stimulation patterns determined during running, we measured muscle power output. Although both muscles were stimulated during the first half of shortening, muscle 177c generated mechanical energy (28 W kg–1) like a motor, while muscle 179 absorbed energy (–19 W kg–1) like a brake. Both muscles exhibited nearly identical intrinsic characteristics including similar twitch kinetics and force–velocity relationships. Differences in the extrinsic factors of activation and relative shortening velocity caused the muscles to operate very differently during running. Presumed redundancy in a multiple muscle group may, therefore, represent diversity in muscle function. Discovering how muscles manage energy during behavior requires the measurement of a large number of dynamically interacting variables

In Situ Muscle Power Differs Without Varying In Vitro Mechanical Properties in Two Insect Leg Muscles Innervated by the Same Motor Neuron

The mechanical behavior of muscle during locomotion is often predicted by its anatomy, kinematics, activation pattern and contractile properties. The neuromuscular design of the cockroach leg provides a model system to examine these assumptions, because a single motor neuron innervates two extensor muscles operating at a single joint. Comparisons of the in situ measurements under in vivo running conditions of muscle 178 to a previously examined muscle (179) demonstrate that the same inputs (e.g. neural signal and kinematics) can result in different mechanical outputs. The same neural signal and kinematics, as determined during running, can result in different mechanical functions, even when the two anatomically similar muscles possess the same contraction kinetics, force-velocity properties and tetanic force-length properties. Although active shortening greatly depressed force under in vivo-like strain and stimulation conditions, force depression was similarly proportional to strain, similarly inversely proportional to stimulation level, and similarly independent of initial length and shortening velocity between the two muscles. Lastly, passive pre-stretch enhanced force similarly between the two muscles. The forces generated by the two muscles when stimulated with their in vivo pattern at lengths equal to or shorter than rest length differed, however. Overall, differences between the two muscles in their submaximal force-length relationships can account for up to 75% of the difference between the two muscles in peak force generated at short lengths observed during oscillatory contractions. Despite the fact that these muscles act at the same joint, are stimulated by the same motor neuron with an identical pattern, and possess many of the same in vitro mechanical properties, the mechanical outputs of two leg extensor muscles can be vastly different

Moderate Dehydration Decreases Locomotor Performance of the Ghost Crab, Ocypode quadrata

The effect of dehydration on the aerobic metabolism and endurance of sustained, terrestrial locomotion was determined for the ghost crab, Ocypode quadrata, The rate of evaporative water loss, measured as the percentage of decrease in body mass per hour, was influenced by ambient temperature (Tₐ), Increasing Tₐ from 24° C to 30° C (40%-50% relative humidity) increased the rate of water loss from 2.3% h­­­­ˉ¹ ± 0.2% h­­­­ˉ¹ to 3.6% h­­­­ˉ¹ ± 0.6% h­­­­ˉ¹. Crabs were divided into three treatment groups to determine the effect of dehydration on aerobic metabolism: hydrated control crabs, slowly dehydrated crabs, and rapidly dehydrated crabs. Hydrated control crabs lost only 1.2% of their initial body mass. Slowly dehydrated crabs were dehydrated by 3.6% of their initial body mass at a rate of 2.3% hˉ¹. Finally, rapidly dehydrated crabs were dehydrated by 3.6% of their initial body mass at a rate of 3.6% hˉ¹. The maximal rate of oxygen consumption (Vo_2max) determined during treadmill exercise was decreased by 30% for slowly dehydrated crabs and by 70% for rapidly dehydrated crabs, as compared to hydrated controls. The minimum cost of locomotion was independent of the dehydration state for hydrated and slowly dehydrated crabs but was 62% lower for rapidly dehydrated crabs. Endurance was correlated with the speed at which Vo_2max was attained (the maximum aerobic speed [MAS]). The MAS was highest for hydrated control crabs and was decreased by 32% for slowly dehydrated crabs and by 68% for rapidly dehydrated crabs. We conclude that moderate dehydration can substantially decrease the ghost crab\u27s capacity for sustained, terrestrial locomotion

Energy Absorption During Running by Leg Muscles in a Cockroach

Biologists have traditionally focused on a muscle\u27s ability to generate power. By determining muscle length, strain and activation pattern in the cockroach Blaberus discoidalis, we discovered leg extensor muscles that operate as active dampers that only absorb energy during running. Data from running animals were compared with measurements of force and power production of isolated muscles studied over a range of stimulus conditions and muscle length changes. We studied the trochanter-femoral extensor muscles 137 and 179, homologous leg muscles of the mesothoracic and metathoracic legs, respectively. Because each of these muscles is innervated by a single excitatory motor axon, the activation pattern of the muscle could be defined precisely. Work loop studies using sinusoidal strains at 8 Hz showed these trochanter-femoral extensor muscles to be quite capable actuators, able to generate a maximum of 19-25 W kg-1 (at 25ºC). The optimal conditions for power output were four stimuli per cycle (interstimulus interval 11 ms), a strain of approximately 4%, and a stimulation phase such that the onset of the stimulus burst came approximately half-way through the lengthening phase of the cycle. High-speed video analysis indicated that the actual muscle strain during running was 12% in the mesothoracic muscles and 16% in the metathoracic ones. Myographic recordings during running showed on average 3-4 muscle action potentials per cycle, with the timing of the action potentials such that the burst usually began shortly after the onset of shortening. Imposing upon the muscle in vitro the strain, stimulus number and stimulus phase characteristic of running generated work loops in which energy was absorbed (-25 W kg-1) rather than produced. Simulations exploring a wide parameter space revealed that the dominant parameter that determines function during running is the magnitude of strain. Strains required for the maximum power output by the trochanter-femoral extensor muscles simply do not occur during constant, average-speed running. Joint angle ranges of the coxa-trochanter-femur joint during running were 3-4 times greater than the changes necessary to produce maximum power output. None of the simulated patterns of stimulation or phase resulted in power production when strain magnitude was greater than 5%. The trochanter-femoral extensor muscles 137/179 of a cockroach running at its preferred speed of 20 cm s-1 do not operate under conditions which maximize either power output or efficiency. In vitro measurements, however, demonstrate that these muscles absorb energy, probably to provide control of leg flexion and to aid in its reversal

The Role of Reflexes Versus Central Pattern Generators

Animals execute locomotor behaviors and more with ease. They have evolved these breath-taking abilities over millions of years. Cheetahs can run, dolphins can swim and flies can fly like no artificial technology can. It is often argued that if human technology could mimic nature, then biological-like performance would follow. Unfortunately, the blind copying or mimicking of a part of nature [Ritzmann et al., 2000] does not often lead to the best design for a variety of reasons [Vogel, 1998]. Evolution works on the just good enough principle. Optimal designs are not the necessary end product of evolution. Multiple satisfactory solutions can result in similar performances. Animals do bring to our attention amazing designs, but these designs carry with them the baggage of their history. Moreover, natural design is constrained by factors that may have no relationship to human engineered designs. Animals must be able to grow over time, but still function along the way. Finally, animals are complex and their parts serve multiple functions, not simply the one we happen to examine. In short, in their daunting complexity and integrated function, understanding animal behaviors remains as intractable as their capabilities are tantalizing

A Physical Model for Dynamical Arthropod Running on Level Ground

Arthropods with their extraordinary locomotive capabilities have inspired roboticists, giving rise to major accomplishments in robotics research over the past decade. Most notably bio-inspired hexapod robots using only task level open-loop controllers [22, 9] exhibit stable dynamic locomotion over highly broken and unstable terrain. We present experimental data on the dynamics of Sprawl- Hex — a hexapod robot with adjustable body sprawl — consisting of time trajectory of full body configuration and single leg ground reaction forces. The dynamics of SprawlHex is compared and contrasted to that of insects. SprawlHex dynamics has qualitative similarities to that of insects in both sagittal and horizontal plane. SprawlHex presents a step towards construction of an effective physical model to study arthropod locomotion

Gait Generation and Control in a Climbing Hexapod Robot

We discuss the gait generation and control architecture of a bioinspired climbing robot that presently climbs a variety of vertical surfaces, including carpet, cork and a growing range of stucco-like surfaces in the quasi-static regime. The initial version of the robot utilizes a collection of gaits (cyclic feed-forward motion patterns) to locomote over these surfaces, with each gait tuned for a specific surface and set of operating conditions. The need for more flexibility in gait specification (e.g., adjusting number of feet on the ground), more intricate shaping of workspace motions (e.g., shaping the details of the foot attachment and detachment trajectories), and the need to encode gait “transitions” (e.g., tripod to pentapod gait structure) has led us to separate this trajectory generation scheme into the functional composition of a phase assigning transformation of the “clock space” (the six dimensional torus) followed by a map from phase into leg joints that decouples the geometric details of a particular gait. This decomposition also supports the introduction of sensory feedback to allow recovery from unexpected event and to adapt to changing surface geometries