The integration of sensory feedback in the modulation of anuran landing preparation.

Controlled landing requires preparation. Mammals and bipedal birds vary how they prepare for landing by predicting the timing and magnitude of impact from the integration of visual and non-visual information. Here, we explore how the cane toad Rhinella marina - an animal that moves primarily through hopping - integrates sensory information to modulate landing preparation. Earlier work suggests that toads may modulate landing preparation using predictions of impact timing and/or magnitude based on non-visual sensory feedback during takeoff rather than visual cues about the landing itself. We disentangled takeoff and landing conditions by hopping toads off platforms of different heights while measuring electromyographic (EMG) activity of an elbow extensor (m. anconeus) and capturing high-speed images to quantify whole body and forelimb kinematics. This enabled us to test how toads integrate visual and non-visual information in landing preparation. We asked two questions: (1) when they conflict, do toads correlate landing preparation with takeoff or landing conditions? And (2) for hops with the same takeoff conditions, does visual information alter the timing of landing preparation? We found that takeoff conditions are a better predictor of the onset of landing preparation than landing conditions, but that visual information is not ignored. When hopping off higher platforms, toads start to prepare for landing later when takeoff conditions are invariant. This suggests that, unlike mammals, toads prioritize non-visual sensory feedback about takeoff conditions to coordinate landing, but that they do integrate visual information to fine-tune landing preparation.

Sensory Feedback and Animal Locomotion: Perspectives from Biology and Biorobotics: An Introduction to the Symposium.

The successful completion of many behaviors relies on sensory feedback. This symposium brought together researchers using novel techniques to study how different stimuli are encoded, how and where multimodal feedback is integrated, and how feedback modulates motor output in diverse modes of locomotion (aerial, aquatic, and terrestrial) in a diverse range of taxa (insects, fish, tetrapods), and in robots. Similar to biological organisms, robots can be equipped with integrated sensors and can rely on sensory feedback to adjust the output signal of a controller. Engineers often look to biology for inspiration on how animals have evolved solutions to problems similar to those experienced in robotic movement. Similarly, biologists too must proactively engage with engineers to apply computer and robotic models to test hypotheses and answer questions on the capacity and roles of sensory feedback in generating effective movement. Through a diverse group of researchers, including both biologists and engineers, the symposium attempted to catalyze new interdisciplinary collaborations and identify future research directions for the development of bioinspired sensory control systems, as well as the use of robots to test hypotheses in neuromechanics.

Vision fine-tunes preparation for landing in the cane toad, Rhinella marina.

In toad hopping, the hindlimbs generate the propulsive force for take-off while the forelimbs resist the impact forces associated with landing. Preparing to perform a safe landing, in which impact forces are managed appropriately, likely involves the integration of multiple types of sensory feedback. In toads, vestibular and/or proprioceptive feedback is critical for coordinated landing; however, the role of vision remains unclear. To clarify this, we compare pre-landing forelimb muscle activation patterns before and after removing vision. Specifically, we recorded EMG activity from two antagonistic forelimb muscles, the anconeus and coracoradialis, which demonstrate distance-dependent onset timing and recruitment intensity, respectively. Toads were first recorded hopping normally and then again after their optic nerves were severed to remove visual feedback. When blind, toads exhibited hop kinematics and pre-landing muscle activity similar to when sighted. However, distance-dependent relationships for muscle activity patterns were more variable, if present at all. This study demonstrates that blind toads are still able to perform coordinated landings, reinforcing the importance of proprioceptive and/or vestibular feedback during hopping. But the increased variability in distance-dependent activity patterns indicates that vision is more responsible for fine-tuning the motor control strategy for landing.

Evidence toads may modulate landing preparation without predicting impact time.

Within anurans (frogs and toads), cane toads (Bufo marinus) perform particularly controlled landings in which the forelimbs are exclusively used to decelerate and stabilize the body after impact. Here we explore how toads achieve dynamic stability across a wide range of landing conditions. Specifically, we suggest that torques during landing could be reduced by aligning forelimbs with the body's instantaneous velocity vector at impact (impact angle). To test whether toad forelimb orientation varies with landing conditions, we used high-speed video to collect forelimb and body kinematic data from six animals hopping off platforms of different heights (0, 5 and 9 cm). We found that toads do align forelimbs with the impact angle. Further, toads align forelimbs with the instantaneous velocity vector well before landing and then track its changes until touchdown. This suggests that toads may be prepared to land well before they hit the ground rather than preparing for impact at a specific moment, and that they may use a motor control strategy that allows them to perform controlled landings without the need to predict impact time.

Consequences of lost endings: caudal autotomy as a lens for focusing attention on tail function during locomotion.

Autotomy has evolved in many animal lineages as a means of predator escape, and involves the voluntary shedding of body parts. In vertebrates, caudal autotomy (or tail shedding) is the most common form, and it is particularly widespread in lizards. Here, we develop a framework for thinking about how tail loss can have fitness consequences, particularly through its impacts on locomotion. Caudal autotomy is fundamentally an alteration of morphology that affects an animal's mass and mass distribution. These morphological changes affect balance and stability, along with the performance of a range of locomotor activities, from running and climbing to jumping and swimming. These locomotor effects can impact on activities critical for survival and reproduction, including escaping predators, capturing prey and acquiring mates. In this Commentary, we first review work illustrating the (mostly) negative effects of tail loss on locomotor performance, and highlight what these consequences reveal about tail function during locomotion. We also identify important areas of future study, including the exploration of new behaviors (e.g. prey capture), increased use of biomechanical measurements and the incorporation of more field-based studies to continue to build our understanding of the tail, an ancestral and nearly ubiquitous feature of the vertebrate body plan.

Sensory feedback and coordinating asymmetrical landing in toads.

Coordinated landing requires anticipating the timing and magnitude of impact, which in turn requires sensory input. To better understand how cane toads, well known for coordinated landing, prioritize visual versus vestibular feedback during hopping, we recorded forelimb joint angle patterns and electromyographic data from five animals hopping under two conditions that were designed to force animals to land with one forelimb well before the other. In one condition, landing asymmetry was due to mid-air rolling, created by an unstable takeoff surface. In this condition, visual, vestibular and proprioceptive information could be used to predict asymmetric landing. In the other, animals took off normally, but landed asymmetrically because of a sloped landing surface. In this condition, sensory feedback provided conflicting information, and only visual feedback could appropriately predict the asymmetrical landing. During the roll treatment, when all sensory feedback could be used to predict an asymmetrical landing, pre-landing forelimb muscle activity and movement began earlier in the limb that landed first. However, no such asymmetries in forelimb preparation were apparent during hops onto sloped landings when only visual information could be used to predict landing asymmetry. These data suggest that toads prioritize vestibular or proprioceptive information over visual feedback to coordinate landing.

Forelimb kinematics during hopping and landing in toads.

Coordinated landing in a variety of animals involves the re-positioning of limbs prior to impact to safely decelerate the body. However, limb kinematics strategies for landing vary considerably among species. For example, human legs are increasingly flexed before impact as drop height increases, while turkeys increasingly extend their legs before impact with increasing drop height. In anurans, landing typically involves the use of the forelimbs to decelerate the body after impact. Few detailed, quantitative descriptions of anuran forelimb kinematics during jumping exist and it is not known whether they prepare for larger landing forces by changing forelimb kinematics. In this study, we used high-speed video of 51 hops from five cane toads (Bufo marinus) to test the hypothesis that forelimb kinematics change predictably with distance. We measured excursions of the elbow (flexion/extension) and humerus (protraction/retraction and elevation/depression) throughout every hop. The results indicate that elbow and humeral excursions leading up to impact increase significantly with hop length, but do so without any change in the rate of movement. Instead, because the animal is in the air longer during longer hops, near-constant velocity movements lead to the larger excursions. These larger excursions in elbow extension result in animals hitting the ground with more extended forelimbs in longer hops, which in turn allows animals to decelerate over a greater distance.

Pre-landing wrist muscle activity in hopping toads.

Coordinated landing requires preparation. Muscles in the limbs important for decelerating the body should be activated prior to impact so that joints may be stiffened and limbs stabilized during landing. Moreover, because landings vary in impact force and timing, muscle recruitment patterns should be modulated accordingly. In toads, which land using their forelimbs, previous work has demonstrated such modulation in muscles acting at the elbow, but not at the shoulder. In this study, we used electromyography and high-speed video to test the hypothesis that antagonistic muscles acting at the wrists of toads are activated in advance of impact, and that these activation patterns are tuned to the timing and force of impact. We recorded from two wrist extensors: extensor carpi ulnaris (ECU) and extensor digitorum communis longus (EDCL), and two wrist flexors: flexor carpi ulnaris (FCU) and palmaris longus (PL). Each muscle was recorded in 4-5 animals (≥15 hops per animal). In all muscles, activation intensity was consistently greatest shortly before impact, suggesting the importance of these muscles during landing. Pre-landing recruitment intensity regularly increased with aerial phase duration (i.e. hop distance) in all muscles except PL. In addition, onset timing in both wrist flexors was also modulated with hop distance, with later onset times being associated with longer hops. Thus, activation patterns in major flexors and extensors of the wrist are tuned to hop distance with respect to recruitment intensity, onset timing or both.

Indirect evidence for elastic energy playing a role in limb recovery during toad hopping.

Elastic energy is critical for amplifying muscle power during the propulsive phase of anuran jumping. In this study, we use toads (Bufo marinus) to address whether elastic recoil is also involved after take-off to help flex the limbs before landing. The potential for such spring-like behaviour stems from the unusually flexed configuration of a toad's hindlimbs in a relaxed state. Manual extension of the knee beyond approximately 90° leads to the rapid development of passive tension in the limb as underlying elastic tissues become stretched. We hypothesized that during take-off, the knee regularly extends beyond this, allowing passive recoil to help drive limb flexion in mid-air. To test this, we used high-speed video and electromyography to record hindlimb kinematics and electrical activity in a hindlimb extensor (semimembranosus) and flexor (iliofibularis). We predicted that hops in which the knees extended further during take-off would require less knee flexor recruitment during recovery. Knees extended beyond 90° in over 80% of hops, and longer hops involved greater degrees of knee extension during take-off and more intense semimembranosus activity. However, knee flexion velocities during recovery were maintained despite a significant decrease in iliofibularis intensity in longer hops, results consistent with elastic recoil playing a role.

Biomechanics and control of landing in toads.

Anything that jumps must land, but unlike during jumping when muscles produce energy to accelerate the body into the air, controlled landing requires muscles to dissipate energy and decelerate the body. Among anurans, toads (genus Bufo) exhibit highly coordinated landing behaviors, using their forelimbs to stabilize the body after touch-down as they lower their hindlimbs to the ground. Moreover, toads land frequently, as they cover distances by stringing together long series of relatively short hops. We have been using toads as a model to understand the biomechanics and motor control strategies of coordinated landing. Our results show that toads prepare for landing differently depending on how far they hop. For example, the forelimbs are extended farther prior to impact after long hops than after short ones. Such kinematic alterations are mirrored by predictable modulation of the recruitment intensity of forelimb muscles before impact, such that longer hops lead to higher levels of pre-landing recruitment of muscles. These differences in kinematics and muscular activity help to control the most flexed configuration of the elbow that is achieved after impact, which in turn constrains the extent to which muscles involved in dissipating energy are stretched. Indeed, a combination of in vivo and in vitro experiments has shown that the elbow-extending anconeus muscle, which is stretched during landing as the elbow flexes, rarely reaches lengths longer than those on the plateau of the muscle's length-tension curve (where damage becomes more likely). We have also been studying how movements of the hindlimbs after take-off help to stabilize animals during landing. In particular, the immediate and rapid flexion of a toad's knees after take-off leads to a repositioning of the animal's center of mass (COM) that better aligns it with ground-reaction forces (GRFs) at impact and reduces torques that would destabilize the animal. Finally, recent work on sensory feedback involved in preparation for landing demonstrates that vision is not required for coordinated landing. Toads can effectively utilize proprioceptive and/or vestibular information during take-off to help inform themselves about landing conditions, but may also use other sensory modalities after take-off to modulate landing behavior.

The impact of tail loss on stability during jumping in green anoles (Anolis carolinensis).

Lizards that undergo caudal autotomy experience a variety of consequences, including decreased locomotor performance in a number of cases. One mode of locomotion common to many arboreal lizard species is jumping, and yet little is known about the effects of autotomy on this locomotor mode. In this article we review recent literature demonstrating the importance of the lizard tail as an in-air stabilizer. First, we review work highlighting how a variety of lizards from diverse families can use their tails to control body position in midair. We then move on to cover recent work demonstrating how in at least one species, Anolis carolinensis, tail loss can lead to remarkable instabilities after takeoff during jumping. Such instabilities occur even when animals are jumping toward specific targets both below and above them, although individual variation in the response to tail loss is considerable. Finally, we report results from a study examining whether increased jumping experience after autotomy facilitates the recovery of in-air stability during jumping. Our work suggests it does not, at least not consistently after 5 wk, indicating that any fitness consequences associated with decreased jumping stability are likely to be long term.

Total recoil: perch compliance alters jumping performance and kinematics in green anole lizards (Anolis carolinensis).

Jumping is a common form of locomotion for many arboreal animals. Many species of the arboreal lizard genus Anolis occupy habitats in which they must jump to and from unsteady perches, e.g. narrow branches, vines, grass and leaves. Anoles therefore often use compliant perches that could alter jump performance. In this study we conducted a small survey of the compliance of perches used by the arboreal green anole Anolis carolinensis in the wild (N=54 perches) and then, using perches within the range of compliances used by this species, investigated how perch compliance (flexibility) affects the key jumping variables jump distance, takeoff duration, takeoff angle, takeoff speed and landing angle in A. carolinensis in the laboratory (N=11). We observed that lizards lost contact with compliant horizontal perches prior to perch recoil, and increased perch compliance resulted in decreased jump distance and takeoff speed, likely because of the loss of kinetic energy to the flexion of the perch. However, the most striking effect of perch compliance was an unexpected one; perch recoil following takeoff resulted in the lizards being struck on the tail by the perch, even on the narrowest perches. This interaction between the perch and the tail significantly altered body positioning during flight and landing. These results suggest that although the use of compliant perches in the wild is common for this species, jumping from these perches is potentially costly and may affect survival and behavior, particularly in the largest individuals.

Loading effects on jump performance in green anole lizards, Anolis carolinensis.

Locomotor performance is a crucial determinant of organismal fitness but is often impaired in certain circumstances, such as increased mass (loading) resulting from feeding or gravidity. Although the effects of loading have been studied extensively for striding locomotion, its effects on jumping are poorly understood. Jumping is a mode of locomotion that is widely used across animal taxa. It demands large amounts of power over a short time interval and, consequently, may be affected by loading to a greater extent than other modes of locomotion. We placed artificial loads equal to 30% body mass on individuals of the species Anolis carolinensis to simulate the mass gain following the consumption of a large meal. We investigated the effects of loading on jump performance (maximum jump distance and accuracy), kinematics and power output. Loading caused a significant 18% decline in maximum jump distance and a significant 10% decline in takeoff speed. In other words, the presence of the load caused the lizards to take shorter and slower jumps, whereas takeoff angle and takeoff duration were not affected. By contrast, jump accuracy was unaffected by loading, although accuracy declined when lizards jumped to farther perches. Finally, mass-specific power output did not increase significantly when lizards jumped with loads, suggesting that the ability to produce mechanical power may be a key limiting factor for maximum jump performance. Our results suggest that mass gain after a large meal can pose a significant locomotor challenge and also imply a tradeoff between fulfilling energy requirement and moving efficiently in the environment.

Hopping isn't always about the legs: forelimb muscle activity patterns during toad locomotion.

Although toads are not known for their jumping ability, they are excellent at landing, using their forelimbs to stabilize and decelerate the body as they transition between hops. Forelimb muscles must play important roles during this landing behavior, but to date our understanding of forelimb muscle function during jumping in anurans, particularly after takeoff, is quite limited. Here, we use simultaneous high-speed video and electromyography to characterize the timing and intensity of electrical activity patterns of six muscles that act at the shoulder or elbow joints in the cane toad, Bufo marinus. In particular, we aim to address the importance of these muscles with respect to various potential roles during hopping (e.g. contributing to propulsion during takeoff, resisting impact forces during landing). Five of the six recorded muscles exhibited their highest average intensities during the aerial phase of the hop, with the most intense activity present near forelimb touchdown. In contrast, no muscles exhibited high levels of activity in the initial phase of takeoff. We interpret these data to indicate that the forelimb muscles studied here are likely unimportant in augmenting force production during takeoff, but are critical for both mid-air forelimb positioning and resisting the forces associated with impact. The onset timing of elbow extensors seems to occur at a nearly fixed interval before impact, regardless of hop length, suggesting that these muscles are particularly tuned to resisting impact.

Do toads have a jump on how far they hop? Pre-landing activity timing and intensity in forelimb muscles of hopping Bufo marinus.

During jumping or falling in humans and various other mammals, limb muscles are activated before landing, and the intensity and timing of this pre-landing activity are scaled to the expected impact. In this study, we test whether similarly tuned anticipatory muscle activity is present in hopping cane toads. Toads use their forelimbs for landing, and we analysed pre-landing electromyographic (EMG) timing and intensity in relation to hop distance for the m. coracoradialis and m. anconeus, which act antagonistically at the elbow, and are presumably important in stabilizing the forelimb during landing. In most cases, a significant, positive relationship between hop distance and pre-landing EMG intensity was found. Moreover, pre-landing activation timing of m. anconeus was tightly linked to when the forelimbs touched down at landing. Thus, like mammals, toads appear to gauge the timing and magnitude of their impending impact and activate elbow muscles accordingly. To our knowledge these data represent the first demonstration of tuned pre-landing muscle recruitment in anurans and raise questions about how important the visual, vestibular and/or proprioceptive systems are in mediating this response.

Losing stability: tail loss and jumping in the arboreal lizard Anolis carolinensis.

Voluntary loss of an appendage, or autotomy, is a remarkable behavior that is widespread among many arthropods and lower vertebrates. Its immediate benefit, generally escape from a predator, is balanced by various costs, including impaired locomotor performance, reproductive success and long-term survival. Among vertebrates, autotomy is most widespread in lizards, in which tail loss has been documented in close to 100 species. Despite numerous studies of the potential costs of tail autotomy in lizards, none have focused on the importance of the tail in jumping. Using high-speed video we recorded jumps from six lizards (Anolis carolinensis) both before and after removing 80% of the tail to test the hypothesis that tail loss has a significant effect on jumping kinematics. Several key performance metrics, including jump distance and takeoff velocity, were not affected by experimental tail removal, averaging 21 cm and 124 cm s(-1), respectively, in both tailed and tailless lizards. However, in-air stability during jumping was greatly compromised after tail removal. Lizards without tails rotated posteriorly more than 30 deg., on average, between takeoff and landing (and sometimes more than 90 deg.) compared with an average of 5 deg. of rotation in lizards with intact tails. Such exaggerated posterior rotation prevents coordinated landing, which is critical for animals that spend much of their time jumping to and from small branches. This work augments recent experiments demonstrating the importance of the tail as a mid-air stabilizer during falling in geckos, and emphasizes new and severe functional costs associated with tail autotomy in arboreal lizards.

The role of hind limb flexor muscles during swimming in the toad, Bufo marinus.

Most work examining muscle function during anuran locomotion has focused largely on the roles of major hind limb extensors during jumping and swimming. Nevertheless, the recovery phase of anuran locomotion likely plays a critical role in locomotor performance, especially in the aquatic environment, where flexing limbs can increase drag on the swimming animal. In this study, I use kinematic and electromyographic analyses to explore the roles of four anatomical flexor muscles in the hind limb of Bufo marinus during swimming: m. iliacus externus, a hip flexor; mm. iliofibularis and semitendinosus, knee flexors; and m. tibialis anticus longus, an ankle flexor. Two general questions are addressed: (1) What role, if any, do these flexors play during limb extension? and (2) How do limb flexors control limb flexion? Musculus iliacus externus exhibits a large burst of EMG activity early in limb extension and shows low levels of activity during recovery. Both m. iliofibularis and m. semitendinosus are biphasically active, with relatively short but intense bursts during limb extension followed by longer and typically weaker secondary bursts during recovery. Musculus tibialis anticus longus becomes active mid way through recovery and remains active through the start of extension in the next stroke. In conclusion, flexors at all three joints exhibit some activity during limb extension, indicating that they play a role in mediating limb movements during propulsion. Further, recovery is controlled by a complex pattern of flexor activation timing, but muscle intensities are generally lower, suggesting relatively low force requirements during this phase of swimming.

Patterns of strain and activation in the thigh muscles of goats across gaits during level locomotion.

Unlike homologous muscles in many vertebrates, which appear to function similarly during a particular mode of locomotion (e.g. red muscle in swimming fish, pectoralis muscle in flying birds, limb extensors in jumping and swimming frogs), a major knee extensor in mammalian quadrupeds, the vastus lateralis, appears to operate differently in different species studied to date. In rats, the vastus undergoes more stretching early in stance than shortening in later stance. In dogs, the reverse is true; more substantial shortening follows small amounts of initial stretching. And in horses, while the vastus strain trajectory is complex, it is characterized mainly by shortening during stance. In this study, we use sonomicrometry and electromyography to study the vastus lateralis and biceps femoris of goats, with three goals in mind: (1) to see how these muscles work in comparison to homologous muscles studied previously in other taxa; (2) to address how speed and gait impact muscle actions and (3) to test whether fascicles in different parts of the same muscle undergo similar length changes. Results indicate that the biceps femoris undergoes substantial shortening through much of stance, with higher strains in walking and trotting [32-33% resting length (L0)] than galloping (22% L0). These length changes occur with increasing biceps EMG intensities as animals increase speed from walking to galloping. The vastus undergoes a stretch-shorten cycle during stance. Stretching strains are higher during galloping (15% L0) than walking and trotting (9% L0). Shortening strains follow a reverse pattern and are greatest in walking (24% L0), intermediate in trotting (20% L0) and lowest during galloping (17% L0). As a result, the ratio of stretching to shortening increases from below 0.5 in walking and trotting to near 1.0 during galloping. This increasing ratio suggests that the vastus does relatively more positive work than energy absorption at the slower speeds compared with galloping, although an understanding of the timing and magnitude of force production is required to confirm this. Length-change regimes in proximal, middle and distal sites of the vastus are generally comparable, suggesting strain homogeneity through the muscle. When strain rates are compared across taxa, vastus shortening velocities exhibit the scaling pattern predicted by theoretical and empirical work: fascicles shorten relatively faster in smaller animals than larger animals (strain rates near 2 L s-1 have been reported for trotting dogs and were found here for goats, versus 0.6-0.8 L s-1 reported in horses). Interestingly, biceps shortening strain rates are very similar in both goats and rats during walking (1-1.5 L s-1) and trotting (1.5-2.5 L s-1, depending on speed of trot), suggesting that the ratio of in vivo shortening velocities (V) to maximum shortening velocities (Vmax) is smaller in small animals (because of their higher V(max)).

Morphology and mechanics of myosepta in a swimming salamander (Siren lacertina).

In contrast to the complex, three-dimensional shape of myomeres in teleost fishes, the lateral hypaxial muscles of salamanders are nearly planar and their myosepta run in a roughly straight line from mid-lateral to mid-ventral. We used this relatively simple system as the basis for a mathematical model of segmented musculature. Model results highlight the importance of the mechanics of myosepta in determining the shortening characteristics of a muscle segment. We used sonomicrometry to measure the longitudinal deformation of myomeres and the dorsoventral deformation of myosepta in a swimming salamander (Siren lacertina). Sonomicrometry results show that the myosepta allow some dorsoventral lengthening, indicating an amplification of myomere shortening that is greater than that produced by muscle fiber angle alone (10% muscle fiber shortening produces 28.7% myomere shortening). Polarized light and DIC microscopy of isolated hypaxial myosepta revealed that the collagen fiber orientation in hypaxial myomeres is primarily mediolateral. The mediolateral collagen fiber orientation, combined with our finding that the hypaxial myosepta lengthen dorsoventrally during swimming, suggests that one possible function of hypaxial myosepta in S. lacertina is to increase the strain amplification of the muscle fibers by reducing the mediolateral bulging of the myomeres and redirecting the bulging toward the dorsoventral direction.