Axial-Appendicular Dynamics and the Integration of Breathing and Gait in Mammal

SYNOPSIS. This paper proposes a biomechanical model for locomotor-respiratorycoupling (LRC) in galloping mammals in which gait and breathingcycles are phase-locked on a 1:1 basis. It also explores someof the physiological and neuromotor implications of LRC. The mechanical coupling of locomotor and respiratory cyclesdepends upon the coordinated, reciprocal oscillations of thecranio-cervical and lumbo-pelvic components of the axial systemand their attendant actions on the intervening thorax via muscularlinkages. Concurrently, accelerational and decelerational forcesimparted to the axial system by the limbs help to drive lungventilation by inducing inertial displacements of a "visceralpiston’ connected to the diaphragm. Several lines of evidence(including cineradiographic data) suggest that an importantfunction of the crural diaphragm is to control the displacementof the visceral piston. The kinematics of LRC indicate thatthe interosseous intercostal muscles must simultaneously operateto assure thoracic stability against locomotor stresses as wellas to promote breathing. The former may be their more essentialrole, however. The characteristic design of the rib cage incursorial mammals (=deep and narrow) appears to maximize theleverage of certain "accessory respiratory muscles" (i.e., sternocleidomastoid,scalenes) while minimizing torsional loading of the thorax duringforelimb support. Physiological implications of LRC include the prediction thatlarge mammals will breathe relatively faster and with relativelysmaller lung volumes when galloping than small species. An additionalprediction, that running mammals could automatically gear lungventilation to speed by simply linking breathing rate to stridefrequency and depth of breath (=tidal volume) to stride length,appears to be supported by experimental data from horses. Finally,the neuromotor basis of LRC probably depends upon the directinteraction of central pattern generators for locomotion andrespiration. This interaction might be modulated, however, byafferent input from thoracic mechanoreceptors, particularlythe intercostal stretch receptors.     

Locomotion energetics and gait characteristics of a rat-kangaroo,<Emphasis Type="Italic"> Bettongia penicillata</Emphasis>, have some kangaroo-like features

The locomotory characteristics of kangaroos and wallabies are unusual, with both energetic costs and gait parameters differing from those of quadrupedal running mammals. The kangaroos and wallabies have an evolutionary history of only around 5 million years; their closest relatives, the rat-kangaroos, have a fossil record of more than 26 million years. We examined the locomotory characteristics of a rat-kangaroo, Bettongia penicillata. Locomotory energetics and gait parameters were obtained from animals exercising on a motorised treadmill at speeds from 0.6 m s⁻¹ to 6.2 m s⁻¹. Aerobic metabolic costs increased as hopping speed increased, but were significantly different from the costs for a running quadruped; at the fastest speed, the cost of hopping was 50% of the cost of running. Therefore B. penicillata can travel much faster than quadrupedal runners at similar levels of aerobic output. The maximum aerobic output of B. penicillata was 17 times its basal metabolism. Increases in speed during hopping were achieved through increases in stride length, with stride frequency remaining constant. We suggest that these unusual locomotory characteristics are a conservative feature among the hopping marsupials, with an evolutionary history of 20–30 million years. Communicated by I.D. Hume An erratum to this article can be found at     

Posture, gait and the ecological relevance of locomotor costs and energy-saving mechanisms in tetrapods

A reanalysis of locomotor data from functional, energetic, mechanical and ecological perspectives reveals that limb posture has major effects on limb biomechanics, energy-saving mechanisms and the costs of locomotion. Regressions of data coded by posture (crouched vs. erect) reveal nonlinear patterns in metabolic cost, limb muscle mass, effective mechanical advantage, and stride characteristics. In small crouched animals energy savings from spring and pendular mechanisms are inconsequential and thus the metabolic cost of locomotion is driven by muscle activation costs. Stride frequency appears to be the principal functional parameter related to the decreasing cost of locomotion in crouched animals. By contrast, the shift to erect limb postures invoked a series of correlated effects on the metabolic cost of locomotion: effective mechanical advantage increases, relative muscle masses decrease, metapodial limb segments elongate dramatically (as limbs shift from digitigrade to unguligrade designs) and biological springs increase in size and effectiveness. Each of these factors leads to decreases in the metabolic cost of locomotion in erect forms resulting from real and increasing contributions of pendular savings and spring savings. Comparisons of the relative costs and ecological relevance of different gaits reveal that running is cheaper than walking in smaller animals up to the size of dogs but running is more expensive than walking in horses. Animals do not necessarily use their cheapest gaits for their predominant locomotor activity. Therefore, locomotor costs are driven more by ecological relevance than by the need to optimize locomotor economy.     

Using body size to understand the structural design of animals: quadrupedal locomotion.

Many parameters of gait and performance, including stride frequency, stride length, maximum speed, and rate of O2 uptake are experimentally found to be power-law functions of body weight in running quadrupeds. All of these parameters are reasonably easy to measure except maximum speed, where the question arises whether one means top sprinting speed or top speed for sustained running. Moreover, differences in training and motivation make comparisons of top speed difficult. The problem is circumvented by comparing animals running at the transition between trotting and galloping, a physiologically similar speed. Theoretical models are proposed which preserve either geometric similarity, elastic similarity, or static stress similarity between animals of large and small body weights. The model postulating elastic similarity provides the best correlation with published data on body and bone proportions, body surface area, resting metabolic rate, and basal heart and lung frequencies. It also makes the most successful prediction of stride frequency, stride length, limb excursion angles, and the metabolic power required for running at the trot-gallop transition in quadrupeds ranging in size from mice to horses.     

Decision-Making in Przewalski Horses (Equus ferus przewalskii) is Driven by the Ecological Contexts of Collective Movements

We addressed decision-making processes in the collective movements of two groups of Przewalski horses ( Equus ferus przewalskii ) living in a semi free-ranging population. We investigated whether different patterns of group movement are related to certain ecological contexts (habitat use and group activity) and analysed the possible decision-making processes involved. We found two distinct patterns; 'single-bout' and 'multiple-bout' movements occurred in both study groups. The movements were defined by the occurrence of collective stops between bouts and differed by their duration, distance covered and ecological context. For both movements, we found that a preliminary period involving several horses occurred before departure. In single-bout movements, all group members rapidly joined the first moving horse, independently of the preliminary period. In multiple-bout movements, however, the joining process was longer; in particular when the number of decision-makers and their pre-departure behaviour before departure increased. Multiple-bout movements were more often used by horses to switch habitats and activities. This observation demonstrates that the horses need more time to resolve motivational conflicts before these departures. We conclude that decision-making in Przewalski horses is based on a shared consensus process driven by ecological determinants.     

Grip and limb force limits to turning performance in competition horses

Manoeuverability is a key requirement for successful terrestrial locomotion, especially on variable terrain, and is a deciding factor in predator-prey interaction. Compared with straight-line running, bend running requires additional leg force to generate centripetal acceleration. In humans, this results in a reduction in maximum speed during bend running and a published model assuming maximum limb force as a constraint accurately predicts how much a sprinter must slow down on a bend given his maximum straight-line speed. In contrast, greyhounds do not slow down or change stride parameters during bend running, which suggests that their limbs can apply the additional force for this manoeuvre. We collected horizontal speed and angular velocity of heading of horses while they turned in different scenarios during competitive polo and horse racing. The data were used to evaluate the limits of turning performance. During high-speed turns of large radius horizontal speed was lower on the bend, as would be predicted from a model assuming a limb force limit to running speed. During small radius turns the angular velocity of heading decreased with increasing speed in a manner consistent with the coefficient of friction of the hoof-surface interaction setting the limit to centripetal force to avoid slipping.     

Effects of alcohol (ethanol) on the fetus

Alcohol (ethanol) use during pregnancy can produce a wide spectrum of effects in the developing embryo/fetus that are dependent on the maternal drinking pattern. The effects of chronic ethanol exposure on the developing conceptus are reviewed with primary focus on ethanol teratogenesis, manifesting in the human as the fetal alcohol syndrome or fetal alcohol effects. The effects of acute ethanol exposure on the near-term fetus are described, including suppressed fetal breathing movements, electrocorticographic (ECoG) activity and electrooculographic (EOG) activity. The ethanol-induced suppression of fetal breathing movements is a very sensitive index of acute exposure of the near-term fetus to ethanol, and appears to involve a direct mechanism of action rather than an indirect mechanism involving suppression of electrocortical activity. The disposition of ethanol and its pharmacologically active proximate metabolite, acetaldehyde, and the activity of alcohol dehydrogenase and aldehyde dehydrogenase in the near-term maternal-fetal unit are described, and a pharmacokinetic model is proposed. The effects of short-term ethanol exposure on the near-term fetus include the development of tolerance to the ethanol-induced suppression of fetal breathing movements, low-voltage ECoG activity and EOG activity. The development of tolerance occurs more rapidly to the latter two fetal biophysical activities. The mechanism of tolerance development appears to be pharmacodynamic (functional) in nature, as there is no increase in the rate of ethanol elimination from the maternal-fetal unit. The role of prostaglandins (PGs) in the mechanism of the ethanol-induced suppression of fetal breathing movements is described. In the near-term fetus, there is a direct relationship between fetal blood ethanol concentration and fetal plasma PGE2 concentration, and an inverse relationship between the incidence of fetal breathing movements and each of fetal plasma and fetal cerebrospinal fluid (CSF) PGE2 concentrations. Indomethacin, a PG synthetase inhibitor, selectively blocks and reverses the ethanol-induced suppression of fetal breathing movements. These data support the postulates that the ethanol-induced suppression of fetal breathing movements is mediated by increased PGE2 concentration in the near-term fetus and that the ability of indomethacin to antagonize the ethanol-induced suppression of fetal breathing movements is due to its biochemical action to decrease fetal PGE2 concentration.(ABSTRACT TRUNCATED AT 400 WORDS)     

Locomotor-respiratory coupling during wheelchair propulsion.

Visceral movement due to impact loading is believed to play a role in the locomotor-respiratory coupling (LRC) that has been detected in a number of mammalian species. In the bird and bat species in which LRC has been described, the effect of the wing muscles on the timing of respiration appears to be a dominant influence. To test the hypothesis that LRC occurs in humans propelling wheelchairs (where there is no impact loading and the arms are used for locomotion), we studied 10 wheelchair athletes on a motorized treadmill at three speeds. Each subject's data were analyzed by spectral analysis (based on the fast Fourier transform), which detected apparent LRC (rates within 1% of a single-digit integer ratio) in 12 (40%) of the 30 test settings. However, a control analysis, in which each subject's arm-thrust rates were compared with another subject's breathing rates, revealed apparent (but false) coupling in 8 (27%), not significantly less often (using the chi 2 test). These findings appear to refute the hypothesis that LRC occurs during wheelchair propulsion. These data are consistent with the theory that the visceral piston is important to LRC and suggest that rhythmic arm movements are insufficient to induce the phenomenon in this setting.     

Estimation of temporal parameters during sprint running using a trunk-mounted inertial measurement unit

The purpose of this study was to identify consistent features in the signals supplied by a single inertial measurement unit (IMU), or thereof derived, for the identification of foot-strike and foot-off instants of time and for the estimation of stance and stride duration during the maintenance phase of sprint running. Maximal sprint runs were performed on tartan tracks by five amateur and six elite athletes, and durations derived from the IMU data were validated using force platforms and a high-speed video camera, respectively, for the two groups. The IMU was positioned on the lower back trunk (L1 level) of each athlete. The magnitudes of the acceleration and angular velocity vectors measured by the IMU, as well as their wavelet-mediated first and second derivatives were computed, and features related to foot-strike and foot-off events sought. No consistent features were found on the acceleration signal or on its first and second derivatives. Conversely, the foot-strike and foot-off events could be identified from features exhibited by the second derivative of the angular velocity magnitude. An average absolute difference of 0.005 s was found between IMU and reference estimates, for both stance and stride duration and for both amateur and elite athletes. The 95% limits of agreement of this difference were less than 0.025 s. The results proved that a single, trunk-mounted IMU is suitable to estimate stance and stride duration during sprint running, providing the opportunity to collect information in the field, without constraining or limiting athletes' and coaches' activities.     

What are the relations between mechanics, gait parameters, and energetics in terrestrial locomotion?

Are the different energy-conserving mechanics (i.e., pendulum and spring) used in different gaits reflected in differences in energetics and/or stride parameters? The analysis included published data from several species and new data from horses. When changing from pendulum to spring mechanics, there is a change in the slope of metabolic rate (MR) vs. speed in all species, in birds and quadrupeds there is no step increase, and in humans there are conflicting reports. At the trot-gallop transition, where quadrupeds are hypothesized to change from spring mechanics to some combination of spring and pendulum mechanics, there is a change in slope of MR vs. speed in horses but not in other species. Stride frequency (SF) is a logarithmic function of walking speed in all species, a linear function of trotting/running speed, and nearly independent of speed in galloping. In humans and horses there is a discontinuity in SF at the walk-trot (run) transition but not in birds. The slope of time of contact vs. speed does not change with mechanics in most species, but it does in humans. In horses and humans, there is a discontinuity at the walk-trot (run) transition and data for other species do not permit generalization. Duty factor (DF) in humans is greater than 0.5 in walking (pendulum mechanics) and less than 0.5 when running (spring mechanics). However, this is not true in many species that have DF>0.5 at the lowest speeds where they use spring mechanics. When trotting at low speeds, horses use forelimb DF>0.5 and hind limb DF<0.5. Thus, it is confusing to distinguish between walking and running by DF.     

Stride length and its determinants in humans, early hominids, primates, and mammals

Primate stride lengths during quadrupedal locomotion are very long when compared to those of nonprimate quadrupedal mammals at the speed of trot/gallop transition. These exceptional lengths are a consequence of the relatively long limbs of primates and the large angular excursions of their limbs during quadrupedalism. When quadrupedal primates employ bipedal gaits they exhibit much lower angular excursions. Consequently their bipedal stride lengths do not appear to be exceptional in length when compared to other mammals. Angular excursions of the lower limbs of modern humans are not exceptionally large. However, when running, humans exhibit relatively long periods of flight (i.e., they have low duty factors) when compared to other mammals including primates. Because of these long periods of flight and their relative long lower limbs, humans have running stride lengths that are at the lower end of the range of stride lengths of quadrupedal primates. The stride length of the Laetoli hominid trails are evaluated in this context.     

Force and flexibility of flailing myxobacteria

Myxococcus xanthus is a common Gram-negative bacterium that moves by a process called gliding motility. In myxobacteria, two distinct mechanisms for gliding have been discovered. S-type motility requires the extension, attachment, and retraction of type IV pili. The other mechanism, designated as A-type motility, may be driven by the secretion and swelling of slime; however, experiments to confirm or refute this model are still lacking and the force exerted by this mechanism has not been measured. A previously published experiment found that when an M. xanthus cell became stuck at one end, the cell underwent flailing motions. Based on this experiment, I propose an elastic model that can estimate the force produced by the A-motility engine and the bending modulus of a single myxobacterial cell. The model estimates a bending modulus of 3 x 10(-14) erg cm and a force between 50-150 pN. This force is comparable to that predicted by slime extrusion, and the bending modulus is 30-fold smaller than that measured in Bacillus subtilis. This model suggests experiments that can further quantify this process.     

The Effects of Rhythmicity and Amplitude on Transfer of Motor Learning

We perform rhythmic and discrete arm movements on a daily basis, yet the motor control literature is not conclusive regarding the mechanisms controlling these movements; does a single mechanism generate both movement types, or are they controlled by separate mechanisms? A recent study reported partial asymmetric transfer of learning from discrete movements to rhythmic movements. Other studies have shown transfer of learning between large-amplitude to small-amplitude movements. The goal of this study is to explore which aspect is important for learning to be transferred from one type of movement to another: rhythmicity, amplitude or both. We propose two hypotheses: (1) Rhythmic and discrete movements are generated by different mechanisms; therefore we expect to see a partial or no transfer of learning between the two types of movements; (2) Within each movement type (rhythmic/discrete), there will be asymmetric transition of learning from larger movements to smaller ones. We used a learning-transfer paradigm, in which 70 participants performed flexion/extension movements with their forearm, and switched between types of movement, which differed in amplitude and/or rhythmicity. We found partial transfer of learning between discrete and rhythmic movements, and an asymmetric transfer of learning from larger movements to smaller movements (within the same type of movement). Our findings suggest that there are two different mechanisms underlying the generation of rhythmic and discrete arm movements, and that practicing on larger movements helps perform smaller movements; the latter finding might have implications for rehabilitation.     

Failure of accentuated vertical body movements to induce cardiac-locomotor coupling.

Cardiac-locomotor coupling (CLC) has been reported during a variety of rhythmic human activities. One reason postulated for such coupling is that axial movements of the viscera during some activities (the "visceral piston") may enhance expulsion of blood from the heart; if so, accentuated vertical movements of the body should provide a powerful stimulus to coupling. To test this hypothesis, we studied 20 subjects hopping and 20 others skipping rope for greater than or equal to 10 min while electrocardiographic and force-platform signals were recorded, from which we derived the subjects' exercise and heart rates. The incidence and intensity of apparent coupling in the test subjects were compared with those of cross-over controls, where the heart rate of each subject was related to the hopping or skipping rate of a matched subject. Ratios consistent with coupling were seen in 10 (50%) hopping subjects under test conditions and in 13 (65%) under control conditions; among skipping subjects, the incidences were 11 (55%) and 10 (50%). In neither group of subjects was the difference in the incidences or the intensities of apparent CLC statistically significant. Our failure to detect CLC while our subjects were hopping or skipping suggests that the visceral piston is unimportant to the CLC phenomenon.     

Keratocyte-like locomotion in amiB-null Dictyostelium cells

Starved Dictyostelium amoebae continuously change their shape and they are elongated along the front-rear axis during locomotion. In contrast, we found that disruption of the amiB gene, which had been identified as a gene required for the aggregation process during development, caused these cells to move in a manner similar to fish keratocytes. Starved amiB- cells were elongated laterally and had one large lamellipodium along the front side arc of the cell. These cells moved unidirectionally for long distances maintaining the half-moon shape, and this movement followed the predictions of the graded radial extension model, which was originally developed to describe the keratocyte movements. Furthermore, the distributions of actin, Arp2, and myosin II in amiB- cells were similar to those in keratocytes. Therefore, locomotion by keratocytes and amiB- cells appears to be driven by similar mechanisms of cytoskeletal regulation. Double knockout cells lacking both AmiB and myosin II were still able to move unidirectionally in a keratocyte-like manner, although the frequency of those movements was lower. Thus, myosin II is dispensable for the unidirectional movement, though it likely functions in the maintenance of the characteristic half-moon shape. This mutant cell can be a useful tool for further molecular genetic analysis of the mechanism of cell locomotion.     

An investigation of colour discrimination with horses (Equus caballus)

The ability of four horses (Equus caballus) to discriminate coloured (three shades of blue, green, red, and yellow) from grey (neutral density) stimuli, produced by back projected lighting filters, was investigated in a two response forced-choice procedure. Pushes of the lever in front of a coloured screen were occasionally reinforced, pushes of the lever in front of a grey screen were never reinforced. Each colour shade was randomly paired with a grey that was brighter, one that was dimmer, and one that approximately matched the colour in terms of brightness. Each horse experienced the colours in a different order, a new colour was started after 85% correct responses over five consecutive sessions or if accuracy showed no trend over sessions. All horses reached the 85% correct with blue versus grey, three horses did so with both yellow and green versus grey. All were above chance with red versus grey but none reached criterion. Further analysis showed the wavelengths of the green stimuli used overlapped with the yellow. The results are consistent with histological and behavioural studies that suggest that horses are dichromatic. They differ from some earlier data in that they indicate horses can discriminate yellow and blue, but that they may have deficiencies in discriminating red and green.     

Cineradiographic study of forelimb movements during quadrupedal walking in the brown lemur (Eulemur fulvus, Primates: Lemuridae)

Movements of forelimb joints and segments during walking in the brown lemur (Eulemur fulvus) were analyzed using cineradiography (150 frames/sec). Metric gait parameters, forelimb kinematics, and intralimb coordination are described. Calculation of contribution of segment displacements to stance propulsion shows that scapular retroversion in a fulcrum near the vertebral border causes more than 60% of propulsion. The contribution by the shoulder joint is 30%, elbow joint 5%, and wrist joint 1%. Correlation analysis was applied to reveal the interdependency between metric and kinematic parameters. Only the effective angular movement of the elbow joint during stance is speed-dependent. Movements of all other forelimb joints and segments are independent of speed and influence, mainly, linear gait parameters (stride length, stance length). Perhaps the most important result is the hitherto unknown and unexpected degree of scapular mobility. Scapular movements consist of ante-/retroversion, adduction/abduction, and scapular rotation about the longitudinal axis. Inside rotation of the scapula (60 degrees -70 degrees ), together with flexion in the shoulder joint, mediates abduction of the humerus, which is not achieved in the shoulder joint, and is therefore strikingly different from humeral abduction in man. Movements of the shoulder joint are restricted to flexion and extension. At touch down, the shoulder joint of the brown lemur is more extended compared to that of other small mammals. The relatively long humerus and forearm, characteristic for primates, are thus effectively converted into stride length. Observed asymmetries in metric and kinematic behavior of the left and right forelimb are caused by an unequal lateral bending of the spinal column.     

Shoulder movements during quadrupedal locomotion in arboreal primates

The kinematics of scapula and shoulder joint movements were analyzed in three species of arboreal quadrupedal primates using cineradiography. Our findings indicate that scapular movement is highly important for forelimb movement in primates with this ancestral mode of locomotion. Retroversion of the scapula (syn. caudal rotation or extension) during the stance phase contributes more than 40% to the stride length of the forelimb. Lateral forelimb excursions, a general feature for arboreal primates, are based on complex three-dimensional scapular movements guided by the clavicle. Humeral abduction is achieved by scapular abduction and transversal rotation of the scapula about its longitudinal axis, and is therefore strikingly different from humeral abduction in humans. At the same time, the movements of the shoulder joint are limited to flexion and extension only.     

Experimental platform to facilitate novel back brace development for the improvement of spine stability

Abstract

The spine or ‘back’ has many functions including supporting our body frame whilst facilitating movement, protecting the spinal cord and nerves and acting as a shock absorber. In certain instances, individuals may develop conditions that not only cause back pain but also may require additional support for the spine. Common movements such as twisting, standing and bending motions could exacerbate these conditions and intensify this pain. Back braces can be used in certain instances to constrain such motion as part of an individual’s therapy and have existed as both medical and retail products for a number of decades. Arguably, back brace designs have lacked the innovation expected in this time. Existing designs are often found to be heavy, overly rigid, indiscrete and largely uncomfortable. In order to facilitate the development of new designs of back braces capable of being optimised to constrain particular motions for specific therapies, a numerical and experimental design strategy has been devised, tested and proven for the first time. The strategy makes use of an experimental test rig in conjunction with finite element analysis simulations to investigate and quantify the effects of back braces on flexion, extension, lateral bending and torsional motions as experienced by the human trunk. This paper describes this strategy and demonstrates its effectiveness through the proposal and comparison of two novel back brace designs.