Resolving head rotation for human bipedalism

Alignment of the body to the gravitational vertical is considered to be the key to human bipedalism. However, changes to the semicircular canals during human evolution suggest that the sense of head rotation that they provide is important for modern human bipedal locomotion. When walking, the canals signal a mix of head rotations associated with path turns, balance perturbations, and other body movements. It is uncertain how the brain uses this information. Here, we show dual roles for the semicircular canals in balance control and navigation control. We electrically evoke a head-fixed virtual rotation signal from semicircular canal nerves as subjects walk in the dark with their head held in different orientations. Depending on head orientation, we can either steer walking by "remote control" or produce balance disturbances. This shows that the brain resolves the canal signal according to head posture into Earth-referenced orthogonal components and uses rotations in vertical planes to control balance and rotations in the horizontal plane to navigate. Because the semicircular canals are concerned with movement rather than detecting vertical alignment, this result shows the importance of movement control and agility rather than precise vertical alignment of the body for human bipedalism.     

An analysis of the mechanical forces in each semicircular canal of the cat under single and combined rotations

The vector equation for the general motion of a body in an inertial system is used to analyze the accelerations in the semicircular canals of the cat when the head undergoes rotation about a vertical axis only, rotation about the naso-occipital axis only, and both rotations simultaneously. The corresponding mean forces and mean pressures in the endolymph are calculated by means of a closed line integral along each canal circumference. The importance of the area of the semicircular canal and of its orientation in space become evident. One can see through this mathematical analysis that the input pattern received by the labyrinthine system depends on a set of well-specified geometrical and mechanical conditions, which must be precisely evaluated in order to interpret the nystagmic outputs.     

Mechanics of Coriolis stimulus and inducing factors of motion sickness.

To specify inducing factors of motion sickness comprised in Coriolis stimulus, or cross-coupled rotation, the sensation of rotation derived from the semicircular canal system during and after Coriolis stimulus under a variety of stimulus conditions, was estimated by an approach from mechanics with giving minimal hypotheses and simplifications on the semicircular canal system and the sensory nervous system. By solving an equation of motion of the endolymph during Coriolis stimulus, rotating angle of the endolymph was obtained, and the sensation of rotation derived from each semicircular canal was estimated. Then the sensation derived from the whole semicircular canal system was particularly considered in two cases of a single Coriolis stimulus and cyclic Coriolis stimuli. The magnitude and the direction of sensation of rotation were shown to depend on an angular velocity of body rotation and a rotating angle of head movement (amplitude of head oscillation when cyclic Coriolis stimuli) irrespective of initial angle (center angle) of the head relative to the vertical axis. The present mechanical analysis of Coriolis stimulus led a suggestion that the severity of nausea evoked by Coriolis stimulus is proportional to the effective value of the sensation of rotation caused by the Coriolis stimulus.     

Rotations in a vertebrate setting: evaluation of the symmetry group of the disynaptic canal-neck projection

Organizational structures intrinsic to nervous systems can be more precisely analyzed and compared with other logical structures once they are expressed in mathematical languages. A standard mathematical language for expressing organizational structure is that of groups. Groups are especially well suited to organizational structures involving multiple symmetries such as spatial structures. The vestibular system is widely believed to mediate many neural functions involving spatial structure. The vestibular nuclei receive direct projections from the vestibular endorgans, the semicircular canals and the otolith organs. The near-orthogonal directions of the semicircular canals are embedded in the bone. However, those canal directions are external to the nervous system. This study addresses the way the three-dimensional space of rotations is also embedded in the group structure of neural connectivity. Although we know a great deal about physical rotation, it is not clear that nervous systems organize rotations in the same way as physicists do. It would make sense for nervous systems to organize rotations in such a way as to provide physiologically relevant information about performing or compensating for rotations. The vestibular nuclei, which might be expected to display an organization that binds rotations into a rotation space, do not give a clear organization. This may be because of the multiplicity of spatial functions performed by the vestibular nuclei; rather than one spatial organization, the vestibular nuclei are likely to accommodate multiple, related spatial organizations. This study evaluates one particular data set from the literature that specifies the organization of the disynaptic canal-neck projection; other projections and neuronal populations may have other intrinsic organizations. The data are evaluated directly for their symmetry group. In the symmetry group, the vertebrate requirement that physiology have a right and left is found to be satisfied in two ways: (i) by a hexagonal symmetry arising from the right-left doubling of front and back, (ii) along with separate organizations on the two sides that may be required to operate independently to some extent. The eight observed muscle innervation patterns from the data are the complete set of possible combinations of inhibitory/excitatory polarities from three canal pairs. These eight innervation patterns are organized as the vertices of a cube. The two types of side muscles provide the vertical direction. As the head rotates in physical space, the cube rotates in sensorimotor space. Like the canal-neck projection, otolith projections and proprioceptive afferents contact both the vestibular nuclei and neck motoneurons. They may have a similar organization, perhaps with extensions of the same pattern. Otherwise, like a checkerboard superimposed over a paisley, they will form an overlapping organization with the disynaptic canal-neck projection. Further research is required to determine whether the sensorimotor spatial structure of the canal-neck projection is widespread in nervous systems or whether there are several complete structures that are fragmented and reintegrated.     

Turning Semicircular Canal Function on Its Head: Dinosaurs and a Novel Vestibular Analysis

Previous investigations have correlated vestibular function to locomotion in vertebrates by scaling semicircular duct radius of curvature to body mass. However, this method fails to discriminate bipedal from quadrupedal non-avian dinosaurs. Because they exhibit a broad range of relative head sizes, we use dinosaurs to test the hypothesis that semicircular ducts scale more closely with head size. Comparing the area enclosed by each semicircular canal to estimated body mass and to two different measures of head size, skull length and estimated head mass, reveals significant patterns that corroborate a connection between physical parameters of the head and semicircular canal morphology. Head mass more strongly correlates with anterior semicircular canal size than does body mass and statistically separates bipedal from quadrupedal taxa, with bipeds exhibiting relatively larger canals. This morphologic dichotomy likely reflects adaptations of the vestibular system to stability demands associated with terrestrial locomotion on two, versus four, feet. This new method has implications for reinterpreting previous studies and informing future studies on the connection between locomotion type and vestibular function.     

A mathematical model of the response of semicircular canal and otolith to head rotation under gravity

The mathematical model of the system composed of two sensors: semicircular canal and sacculus, is presented. The system is described by three series of blocks: biomechanical block, mechanoelectrical transduction mechanism and hair cell ionic currents and membrane potential dynamics. The response of the aforecited system to various stimuli (head rotation under gravity and falling) was investigated. The identification of the model parameters was fulfilled for the experimental data, obtained for the axolotle (Ambystoma tigrinum) in Institute of Physiology, Autonomous University of Puebla, Mexico. The comparative analysis of canal and sacculus membrane potential was realized.     

The Video Head Impulse Test (vHIT) Detects Vertical Semicircular Canal Dysfunction

Background

The video head impulse test (vHIT) is a useful clinical tool to detect semicircular canal dysfunction. However vHIT has hitherto been limited to measurement of horizontal canals, while scleral search coils have been the only accepted method to measure head impulses in vertical canals. The goal of this study was to determine whether vHIT can detect vertical semicircular canal dysfunction as identified by scleral search coil recordings.

Methods

Small unpredictable head rotations were delivered by hand diagonally in the plane of the vertical semicircular canals while gaze was directed along the same plane. The planes were oriented along the left-anterior-right-posterior (LARP) canals and right-anterior-left-posterior (RALP) canals. Eye movements were recorded simultaneously in 2D with vHIT (250 Hz) and in 3D with search coils (1000 Hz). Twelve patients with unilateral, bilateral and individual semicircular canal dysfunction were tested and compared to seven normal subjects.

Results

Simultaneous video and search coil recordings were closely comparable. Mean VOR gain difference measured with vHIT and search coils was 0.05 (SD = 0.14) for the LARP plane and −0.04 (SD = 0.14) for the RALP plane. The coefficient of determination R² was 0.98 for the LARP plane and 0.98 for the RALP plane and the results of the two methods were not significantly different. vHIT and search coil measures displayed comparable patterns of covert and overt catch-up saccades.

Conclusions

vHIT detects dysfunction of individual vertical semicircular canals in vestibular patients as accurately as scleral search coils. Unlike search coils, vHIT is non-invasive, easy to use and hence practical in clinics.     

The primate subarcuate fossa and its relationship to the semicircular canals part II: adult interspecific variation

Studies have reported an empirical link between the size of the semicircular canals and locomotor agility across adult primates. In this paper, we investigate the possibility that this relationship does not follow from the function of the semicircular canals to sense head rotations, but rather reflects spatial constraints imposed by the subarcuate fossa. The latter sits among the three canals and contains the petrosal lobule of the cerebellar paraflocculus, a structure involved in neural processing of locomotion-related eye movements. Hence, it is feasible that agility-related variations of lobule and fossa size affect the arc size of the surrounding semicircular canals. The present study tests such hypothetical correlations by evaluating canal size, fossa size, and agility among extant adult primates. Phylogenetically informed multivariate regression analyses show that, after controlling for body mass, the size of the subarcuate fossa has a significant positive effect on the overall size of the anterior canal and the width of the posterior canal. Multivariate regressions involving the height of the posterior canal and overall size of the lateral canal are not significant. Further bivariate analyses confirm that fossa size is unlikely to play a role in the previously reported link between agility and the size of the posterior and lateral canals. However, fossa size, especially its opening though the arc of the anterior canal, cannot be excluded as a factor that influences the size of the anterior canal more than agility. The findings show that the most reliable functional signals pertaining to locomotion in species that possess a patent subarcuate fossa are likely to come from the lateral canal and are least likely to come from the anterior canal.     

The semicircular canals of the hagfish Myxine glutinosa

The internal radius (r) and radius of curvature (R) of the single semicircular canals of Myxine glutinosa have unusual dimensions. In mammals and fish the increase in dimension of r and R with respect to body weight is small; in fish r is larger than in mammals of equivalent weight in order to increase the sensitivity of the canals to angular rotation and R increases correspondingly (Jones & Spells, 1963). In Myxine r is larger than in fish or mammals yet R is smaller. It is argued that the large internal radius is the result of the need to increase the sensitivity of a single canal which has to signal rotation in three planes while the small radius of curvature follows from the absence of a cupula. In order to verify that the cristae of the canals do respond to rotational velocity, recordings were obtained from the nerves serving the canals during rotation in the horizontal plane. The frequency response of several afferents recorded simultaneously at sinusoidal rotations between 0.25 and 2.0 Hz was in the form of a sine wave 90 in advance of head position, as would be expected of a velocity transducer. The gain of single afferents was an order of magnitude less than those reported for other vertebrates.     

The use of matrices in analyzing the three-dimensional behavior of the vestibulo-ocular reflex

The vestibulo-ocular reflex rotates the eye about the axis of a head rotation at the same speed but in the opposite direction to make the visual axes in space independent of head motion. This reflex works in all three degrees of freedom: roll, pitch, and yaw. The rotations may be described by vectors and the reflex by a transformation in the form of a matrix. The reflex consists of three parts: sensory, central, and motor. The transduction of head rotation into three neural signals, which may also be described by a vector, is described by a canal matrix. The neural, motorcommand vector is transformed to an eye rotation by a muscle matrix. Since these two matrices are known, one can solve for the central matrix which gives the strength of the connections between all the vestibular neurons and all the eye-muscle motoneurons. The role of the metric tensor in these transformations is described. This method of analysis is used in three applications. A lesion may be simulated by altering the elements in any or all of the three component matrices. By matrix multiplication, the resulting abnormal behavior of the reflex can be described quantitatively in all degrees of freedom. The method is also used to directly compare the differences in brain-stem connections between humans and rabbits that accommodate the altered actions of the muscles of the two species. Finally the method allows a quantitative assessment of the changes that take place in the brainstem connections when plastic changes are induced by artificially dissociating head movements from apparent motion of the visual environment.     

Simulation of vestibular semicircular canal responses during righting movements of a freely falling cat

The righting maneuver of a freely falling cat was filmed at 1000 pictures per second, and the head position about the roll axis was digitized from each film frame using a graphics input tablet. The head angular velocity and acceleration were computed from the roll axis position trajectory. Head acceleration trajectories approximated two periods of a damped sinusoid at a frequency of 26 Hz. Head acceleration peak amplitudes exceeded 120,000 deg/s². These trajectories were used as stimuli for the horizontal semicircular canals in a computer simulation of first-order afferent responses during the fall. Linear system afferent response dynamics, characterized in a previous study of the cat horizontal canal using pseudorandom rotations, provided the basis for linear predictions of falling cat afferent responses. Results showed predicted single afferent firing rates that exceeded physiological values; and variations in afferent sensitivities and phase were predicted among different neurons. Fast head movement information could be carried by ensemble populations of vestibular neurons, and a phase-locking encoding hypothesis is proposed which accomplishes this. Implications for central program versus peripheral vestibular feedback strategies for motor control during falling are presented and discussed.     

Comparative anatomy of the bony labyrinth of extant and extinct porpoises (Cetacea: Phocoenidae)

The inner ear anatomy of cetaceans, now more readily accessible by means of nondestructive high‐resolution X‐ray computed tomographic (CT) scanning, provides a window into their acoustic abilities and ecological preferences. Inner ear labyrinths also may be a source for additional morphological characters for phylogenetic analyses. In this study, we explore digital endocasts of the inner ear labyrinths of representative species of extinct and extant porpoises (Mammalia: Cetacea: Phocoenidae), a clade of some of the smallest odontocete cetaceans, which produce some of the highest‐frequency clicks for biosonar and communication. Metrics used to infer hearing ranges based on cochlear morphology indicate that all taxa considered could hear high‐frequency sounds, thus the group had already acquired high‐frequency hearing capabilities by the Miocene (9–11 Mya) at the latest. Vestibular morphology indicates that extant species with pelagic preferences have similarly low semicircular canal deviations from 90°, values indicating more sensitivity to head rotations. Species with near‐shore preferences have higher canal deviation values, indicating less sensitivity to head rotations. Extending these analyses to the extinct species, we demonstrate a good match between those predicted to have coastal (such as Semirostrum cerutti) preferences and high canal deviation values. We establish new body length relationships based on correlations with inner ear labyrinth volume, which can be further explored among other aquatic mammals to infer body size of specimens consisting of fragmentary material.     

Timing of secondary vestibular neuron responses to a range of rotational head movements

Secondary vestibular neurons exhibit a wide variety of responses to a head movement, with the response of each secondary neuron depending upon the particular primary afferents converging onto it. A single head movement is thereby registered in a distributed manner. This paper focuses on implications of afferent convergence to the relative timing of secondary neuron response modulation during rotational movements about a combination of horizontal axes. In particular, the neurons of interest are those that receive input from afferents innervating the vertical semicircular canals, and the movements of interest are those that have a sinusoidal component about one vertical canal axis and a sinusoidal component about another, approximately orthogonal, vertical canal axis. Under these conditions, the present research shows that it is possible for two or more secondary neurons to have a different relative timing of response (i.e., different relative phase of the periodic modulation in firing rate) for different head movements, and for the neurons to switch their order of response for different movements. For particular head movements, those same neurons will respond in phase. From the point of view of the nervous system, the relative timing of neuron responses may tell which movement is taking place, but with certain restrictions as discussed in the present paper. Shown here is that, among those head movements for which the two components of rotation may be at any phase relative to one another and have any relative amplitude, an in-phase response of just two neurons cannot identify a single motion. Two neurons that respond in phase for one motion must respond in phase for an entire range of motions; all motions in that range are thus response-equivalent, in the sense that the pair of neurons cannot distinguish between the two motions. On the other hand, an in-phase response of three neurons can identify a single motion, for certain patterns of primary afferent convergence. Received: 16 December 1996 / Accepted in revised form: 3 April 1998     

The bony labyrinth of Neanderthals

This paper presents a comprehensive comparative analysis of the Neanderthal bony labyrinth, a structure located inside the petrous temporal bone. Fifteen Neanderthal specimens are compared with a Holocene human sample, as well as with a small number of European Middle Pleistocene hominins, and early anatomically modern and European Upper Palaeolithic humans. Compared with Holocene humans the bony labyrinth of Neanderthals can be characterized by an anterior semicircular canal arc which is smaller in absolute and relative size, is relatively narrow, and shows more torsion. The posterior semicircular canal arc is smaller in absolute and relative size as well, it is more circular in shape, and is positioned more inferiorly relative to the lateral canal plane. The lateral semicircular canal arc is absolutely and relatively larger. Finally, the Neanderthal ampullar line is more vertically inclined relative to the planar orientation of the lateral canal. The European Upper Palaeolithic and early modern humans are most similar, although not fully identical to Holocene humans in labyrinthine morphology. The European Middle Pleistocene hominins show the typical semicircular canal morphology of Neanderthals, with the exception of the arc shape and inferiorly position of the posterior canal and the strongly inclined ampullar line. The marked difference between the labyrinths of Neanderthals and modern humans can be used to assess the phylogenetic affinities of fragmentary temporal bone fossils. However, this application is limited by a degree of overlap between the morphologies. The typical shape of the Neanderthal labyrinth appears to mirror aspects of the surrounding petrous pyramid, and both may follow from the phylogenetic impact of Neanderthal brain morphology moulding the shape of the posterior cranial fossa. The functionally important arc sizes of the Neanderthal semicircular canals may reflect a pattern of head movements different from that of modern humans, possibly related to aspects of locomotor behaviour and the kinematic properties of their head and neck.     

Spinal shape changes resulting from scoliotic spine surgical instrumentation expressed as intervertebral rotations and centers of rotation

This paper reports the changes in spinal shape resulting from scoliotic spine surgical instrumentation expressed as intervertebral rotations and centers of rotation. The objective is to test the hypothesis that the type of spinal instrumentation system (Cotrel-Dubousset versus Colorado) does not influence these motion parameters. Intervertebral rotations and centers of rotation of the scoliotic spines were computed from the pre- and post-operative radiographs of 82 patients undergoing spinal correction. The three-dimensional (3D) reconstruction of six anatomical landmarks was achieved for each of the thoracic and lumbar vertebrae. A least-squares approach based on singular value decomposition was used to calculate the rigid body transformation parameters. Average centers of rotation for all intervertebral levels are located in the neural canal at the mid-sagittal plane and approximately at the superior endplate level of the inferior vertebra. Intervertebral rotations have components in all planes: 6.7 degrees (frontal), 5.5 degrees (sagittal) and 4.5 degrees (transverse) RMS for all intervertebral levels. Nearly all intervertebral rotations and centers of rotation are not significantly different for the two instrumentation systems. Various intervertebral rotations and 3D reconstruction errors were simulated on a theoretical model of a lumbar functional unit to assess the proposed method. Intervertebral rotation errors were 1.7 degrees when simulating 3D errors of 3mm on the position of the landmarks. Maximum errors for the position of centers of rotation were below 1cm in the case of intervertebral rotations larger than 2.5 degrees (most cases), but were larger (38 mm) for small intervertebral rotations (<1 degrees ). The type of instrumentation system did not influence intervertebral rotations and centers of rotation. These results provide valuable data for the development and validation of simulation models for surgical instrumentation of idiopathic scoliosis.     

Spatial coordination of compensatory eye movements in vertebrates: form and function

The semicircular canals of the labyrinth of vertebrates provide one way of motion detection in three-dimensional space. The fully developed form of the vertebrate labyrinth consists of six semicircular canals, three on each side of the head, whose spatial arrangement (vertical canals are placed diagonally in the head, horizontal canals are oriented earth horizontally) follows three interconnected principles: 1) bilateral symmetry, 2) push-pull operational mode, and 3) mutual orthogonality. Other sensory and motor systems related to vestibular reflexes, such as the extraocular muscles or the "optokinetic" coordinate axes encoded in the activity of the visually driven cells of the accessory optic system, share the same geometrical framework. This framework is also reflected in the anatomical networks mediating compensatory eye movements, linking each of the semicircular canals to a particular set of extraocular muscles (so-called principal vestibuloocular reflex connections to yoke muscles). These classical vestibulo-oculomotor relationships have been verified at many levels of the vertebrate hierarchy, including lateral- and frontal-eyed animals. The particular spatial orientation of the semicircular canals requires further comment and phylogenetic evaluation. The spatial arrangement of the vertical canals is already present in fossil ostracoderms, and is also exemplified in lampreys, the modern forms of once abundant agnathan species that populated the Silurian and Devonian oceans. The lampreys and ostracoderms lack horizontal canals, which appear later in all descendent vertebrates. The fully developed vertebrate labyrinth with its six semicircular canals displays distinct differences that are obvious when comparing distant taxa (e.g. elasmobranchs versus other vertebrates). Whereas the common crus of the semicircular canals in teleosts through mammals is formed between the anterior and the posterior semicircular canal, it occurs between the anterior and the horizontal canal in elasmobranchs. However, despite this morphological difference, these two vertebrate labyrinth prototypes constitute a functionally identical solution. A similar analysis holds for certain invertebrate species (crab, octopus, squid), which display an even wider variety in the physical expressions of movement detection systems when compared to vertebrates. Although the physical expressions of motion detection systems differ in the animal kingdom, the functional solutions (providing the best signal-to-noise ratio) with adherence to bilateral symmetry, push-pull operational mode, and mutual orthogonality are identical.(ABSTRACT TRUNCATED AT 400 WORDS)     

Perspectives for the comprehensive examination of semicircular canal and otolith function.

A review is presented on the three-dimensional aspects of the vestibulo-oculomotor system and the current functional tests for unilateral examination of the individual receptors in the vestibular labyrinth. In the presentation, attention is directed towards the recently developed vestibular tests, which promise a more comprehensive examination of labyrinth function. More explicitly, unilateral tests for the utricle, saccule and the individual semicircular canals are discussed. Caloric irrigation and rotatory testing are widely used as tests for the integrity of the (horizontal) semicircular canals. Little useful diagnosis is made however on the vertical canals, not to mention the otolith organs. A promising approach to the examination of individual semicircular canal function has been described. This involves the perception of self-rotation in each of the planes of the semicircular canals. The patient/subject is rotated by an arbitrary amount on a standard Barany chair and then required to return the chair to its original position, by joystick control of the chair velocity. In order to test the vertical canals, the head of the subject/patient is positioned so that the plane of each canal lies in the plane of rotation. A promising unilateral test of saccular function involves the use of vestibular evoked myogenic potentials. Here it has been demonstrated that the saccules can be activated using brief, high-intensity acoustic clicks. The myogenic potential is measured using surface electrodes over the sternocleidomastoid muscles. Initial data from patients has indicated that the test is specific for unilateral saccule disorders. The unilateral test of utricle function is based on the eccentric displacement profile. Thus, eccentric displacement of the head to 3.5 cm during constant velocity rotation about the earth-vertical axis generates an adequate unilateral stimulation of the otolith organ, without involving the semicircular canals. This paradigm has also proved efficient in localizing peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In contrast to the otolith-ocular response, the subjective visual vertical also reflects the processing of otolithic information in the higher brain centres (thalamus, vestibular cortex). Exploitation of the two complementary approaches therefore provides useful information for both experimental and clinical scientists. Of direct interest is the finding that testing with the subject rotating on-centre is sufficient to localize peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In addition to caloric testing, which has remained the classical unilateral test of vestibular function, the newly developed tests should improve the differential diagnosis of vestibular disorders.     

Semicircular canal system in early primates

Mammals with more rapid and agile locomotion have larger semicircular canals relative to body mass than species that move more slowly. Measurements of semicircular canals in extant mammals with known locomotor behaviours can provide a basis for testing hypotheses about locomotion in fossil primates that is independent of postcranial remains, and a means of reconstructing locomotor behaviour in species known only from cranial material. Semicircular canal radii were measured using ultra high resolution X-ray CT data for 9 stem primates (“plesiadapiforms”; n = 11), 7 adapoids (n = 12), 4 omomyoids (n = 5), and the possible omomyoid Rooneyia viejaensis (n = 1). These were compared with a modern sample (210 species including 91 primates) with known locomotor behaviours. The predicted locomotor agilities for extinct primates generally follow expectations based on known postcrania for those taxa. “Plesiadapiforms” and adapids have relatively small semicircular canals, suggesting they practiced less agile locomotion than other fossil primates in the sample, which is consistent with reconstructions of them as less specialized for leaping. The derived notharctid adapoids (excluding Cantius) and all omomyoids sampled have relatively larger semicircular canals, suggesting that they were more agile, with Microchoerus in particular being reconstructed as having had very jerky locomotion with relatively high magnitude accelerations of the head. Rooneyia viejaensis is reconstructed as having been similarly agile to omomyids and derived notharctid adapoids, which suggests that when postcranial material is found for this species it will exhibit features for some leaping behaviour, or for a locomotor mode requiring a similar degree of agility.