Effects of adequate vestibular stimulation on locomotor activity in the guinea pig fore- and hindlimb muscles. Tilting around a transverse axis

The effects of adequate vestibular stimulation occurring as the animal tilted around its transverse axis on locomotor activity of the fore- and hindlimb muscles produced by electrical brainstem stimulation were investigated during experiments on guinea pigs decerebrated at the precollicular level. An increase and decrease in forelimb and hindlimb extensor activity, respectively, at the standing phase of the locomotor cycle were observed when the animal was tilted head-downward. The reverse changes took place in the limb extensor muscles when the animal was tilted head-up. Forelimb extensor activity during the swing phase increased and decreased when the animal was tilted head-up and head-downward, respectively. Phase shifts of changes in locomotor activity of the forelimb extensors altered from 60 to –30°, from –150 to 220° in hindlimb extensors, and from –140 to –220° in forelimb flexors during sinusoidal tilting in the 0.02–0.4 Hz frequency range and an amplitude of ±20°. Mechanisms underlying the changes observed in locomotor muscle activity are discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 19, No. 6, pp. 833–838, November–December, 1987.     

Effects of adequate vestibular stimulation on locomotor activity in fore- and hindlimb muscles in the guinea pig. Movement along a vertical axis

The effects of applying adequate vestibular stimulation to the mesencephalic locomotor region on locomotor activity in fore- and hindlimb muscles was investigated during experiments on decerebrate guinea pigs. This stimulation was produced by linear sinusoidal shifting of the animal along a vertical axis at rates of 0.08, 0.2, 0.4, and 0.8 Hz (with peak accelerations of 0.010, 0.063, 0.252, and 1.010 m·sec^–2 respectively). A downwards shift was found to increase electromyographic extensor muscle activity in fore- and hindlimbs occurring during the swing phase of the locomotor cycle. An upwards movement was accompanied by the opposite changes in muscle activity. Minimum acceleration required to produce an alteration in muscle activity equaled 0.063 m·sec^–2 (0.006g). These alterations were characterized by cyclical delay in relation to linear (active) acceleration. Phase lags in the activity of fore- and hindlimb extensor muscles at the rate of 0.8 Hz reached 63° and 86° respectively. Changes in flexor muscle activity ran counterphasically to these; phasic delay equalled 264° and 275° respectively. The part played by the vestibular system in control over locomotor activity in vertebrate muscles is discussed.A. A. Bogomolets Institute of Physiology, Academy of Sciences of the Ukrainian SSR, Kiev. Translated from Neirofiziologiya, Vol. 21, No. 2, pp. 192–197, March–April, 1989.     

Forelimb and hindlimb forces in walking and galloping primates

One trait that distinguishes the walking gaits of most primates from those of most mammalian nonprimates is the distribution of weight between the forelimbs and hindlimbs. Nonprimate mammals generally experience higher vertical peak substrate reaction forces on the forelimb than on the hindlimb. Primates, in contrast, generally experience higher vertical peak substrate reaction forces on the hindlimb than on the forelimb. It is currently unclear whether this unusual pattern of force distribution characterizes other primate gaits as well. The available kinetic data for galloping primates are limited and present an ambiguous picture about peak-force distribution among the limbs. The present study investigates whether the pattern of forelimb-to-hindlimb force distribution seen during walking in primates is also displayed during galloping. Six species of primates were video-recorded during walking and galloping across a runway or horizontal pole instrumented with a force-plate. The results show that while the force differences between forelimb and hindlimb are not significantly different from zero during galloping, the pattern of force distribution is generally the same during walking and galloping for most primate species. These patterns and statistical results are similar to data collected during walking on the ground. The pattern of limb differentiation exhibited by primates during walking and galloping stands in contrast to the pattern seen in most nonprimate mammals, in which forelimb forces are significantly higher. The data reported here and by Demes et al. ([1994] J. Hum. Evol. 26:353-374) suggest that a relative reduction of forelimb vertical peak forces is part of an overall difference in locomotor mechanics between most primates and most nonprimate mammals during both walking and galloping.     

Foot morphology and locomotor adaptation in Eocene primates

Locomotor diversity of Eocene primates of North America and Europe was well developed, with species of both Adapidae and Omomyidae showing a wide spectrum of movements. Besides documenting the locomotor diversity in the Eocene, this paper shows that adapid foot morphology shares derived features with extant strepsirhines. Thus, the Omomyidae best resemble the ancestral euprimate in terms of foot morphology and locomotion. The generalized locomotor repertoire of the modern cheirogaleids represents the best model for the movement pattern of the ancestral euprimate.     

The musculoskeletal anatomy of the reindeer (Rangifer tarandus): fore- and hindlimb

Reindeer are numerous and widespread across the northern Holarctic. They are efficient long distance migrants and are able to cope with variations in substrate, such as ice, snow, uneven forest floor, wetland and flat grassland. However, as with the vast majority of quadrupedal vertebrates, no quantitative musculoskeletal anatomical information exists for these animals making it difficult to analyse the biomechanics of their locomotor behaviour. In this paper, we describe the gross anatomy of the limb musculature and quantify muscle and tendon morphology. Reindeer show slight hindlimb dominance in muscle and tendon mass, with muscle mass primarily proximally situated and tendon distally situated. Extensor muscles are heavier than flexors, but tendon mass is broadly similar in both extensors and flexors. The only complete quadrupedal data sets available for comparison are for hares and greyhounds making it difficult to identify general patterns. There are no obvious body mass effects and reindeer often comes out as intermediate between hare and greyhound. However, greyhound seem less hindlimb dominated in terms of muscle but both greyhound and hare have much higher masses of tendon compared to reindeer, particularly in their hindlimbs. All these quadrupeds show the commonly observed trait of much larger tendons and less massive muscles in distal limb segments; this reduces the inertial cost of accelerating the limbs. Generally, there is a dearth of available quantitative anatomical data of complete animals. This lack of information is hindering attempts to gain a better understanding of musculoskeletal function in quadrupeds.     

Functional differentiation of fore- and hindlimb muscles inMacaca fuscata determined on the basis of enzymatic activities

When the functional differentiation of 83 kinds of limb and trunk muscles ofMacaca fuscata was investigated on the basis of the activities of two glycolytic enzymes [lactate dehydrogenase (LDH) and aldolase] and one oxidative enzyme [succinate dehydrogenase (SDH)], the forelimb rather than the hindlimb muscles proved have higher oxidative activities. These results indicated that, inMacaca fuscata, the forelimb muscles have a higher resistance to fatigue, and that the hindlimb muscles have a higher tetanic tension on the basis of the relationships between enzymatic activities and functional properties of the muscle fiber types. These findings were interpreted in relation to the fact thatMacaca fuscata is a quadrupedal primate with arboreal habits, as compared with nonprimate terrestrial quadrupeds. The two-joint muscles and the superficial muscles contract more rapidly than do the other muscles in the hindlimb, thereby suggesting that both types of muscles readily adapt to quick movement.     

Substrate alters forelimb to hindlimb peak force ratios in primates

It is often claimed that the walking gaits of primates are unusual because, unlike most other mammals, primates appear to have higher vertical peak ground reaction forces on their hindlimbs than on their forelimbs. Many researchers have argued that this pattern of ground reaction force distribution is part of a general adaptation to arboreal locomotion. This argument is frequently used to support models of primate locomotor evolution. Unfortunately, little is known about the force distribution patterns of primates walking on arboreal supports, nor do we completely understand the mechanisms that regulate weight distribution in primates. We collected vertical peak force data for seven species of primates walking quadrupedally on instrumented terrestrial and arboreal supports. Our results show that, when walking on arboreal vs. terrestrial substrates, primates generally have lower vertical peak forces on both limbs but the difference is most extreme for the forelimb. We found that force reduction occurs primarily by decreasing forelimb and, to a lesser extent, hindlimb stiffness. As a result, on arboreal supports, primates experience significantly greater functional differentiation of the forelimb and hindlimb than on the ground. These data support long-standing theories that arboreal locomotion was a critical factor in the differentiation of the forelimbs and hindlimbs in primates. This change in functional role of the forelimb may have played a critical role in the origin of primates and facilitated the evolution of more specialized locomotor behaviors.     

Passive stiffness of hindlimb muscles in anurans with distinct locomotor specializations

Anurans (frogs and toads) have been shown to have relatively compliant skeletal muscles. Using a meta-analysis of published data we have found that muscle stiffness is negatively correlated with joint range of motion when examined across mammalian, anuran and bird species. Given this trend across a broad phylogenetic sample, we examined whether the relationship held true within anurans. We identified four species that differ in preferred locomotor mode and hence joint range of motion (Lithobates catesbeianus, Rhinella marina, Xenopus laevis and Kassina senegalensis) and hypothesized that smaller in vivo angles (more flexed) at the knee and ankle joint would be associated with more compliant extensor muscles. We measured passive muscle tension during cyclical stretching (20%) around L₀ (sarcomere lengths of 2.2 μm) in fiber bundles extracted from cruralis and plantaris muscles. We found no relationship between muscle stiffness and range of motion for either muscle–joint complex. There were no differences in the passive properties of the cruralis muscle among the four species, but the plantaris muscles of the Xenopus and Kassina were significantly stiffer than those of the other two species. Our results suggest that in anurans the stiffness of muscle fibers is a relatively minor contributor to stiffness at the level of joints and that variation in other anatomical properties including muscle–tendon architecture and joint mechanics as well as active control likely contribute more significantly to range of motion during locomotion.     

Experimental evolution and phenotypic plasticity of hindlimb bones in high-activity house mice

Studies of rodents have shown that both forced and voluntary chronic exercise cause increased hindlimb bone diameter, mass, and strength. Among species of mammals, "cursoriality" is generally associated with longer limbs as well as relative lengthening of distal limb segments, resulting in an increased metatarsal/femur (MT/F) ratio. Indeed, we show that phylogenetic analyses of previously published data indicate a positive correlation between body mass-corrected home range area and both hindlimb length and MT/F in a sample of 19 species of Carnivora, although only the former is statistically significant in a multiple regression. Therefore, we used an experimental evolution approach to test for possible adaptive changes (in response to selective breeding and/or chronic exercise) in hindlimb bones of four replicate lines of house mice bred for high voluntary wheel running (S lines) for 21 generations and in four nonselected control (C) lines. We examined femur, tibiafibula, and longest metatarsal of males housed either with or without wheel access for 2 months beginning at 25-28 days of age. As expected from previous studies, mice from S lines ran more than C (primarily because the former ran faster) and were smaller in body size (both mass and length). Wheel access reduced body mass (but not length) of both S and C mice. Analysis of covariance (ANCOVA) revealed that body mass was a statistically significant predictor of all bone measures except MT/F ratio; therefore, all results reported are from ANCOVAs. Bone lengths were not significantly affected by either linetype (S vs. C) or wheel access. However, with body mass as a covariate, S mice had significantly thicker femora and tibiafibulae, and wheel access also significantly increased diameters. Mice from S lines also had heavier feet than C, and wheel access increased both foot and tibiafibula mass. Thus, the directions of evolutionary and phenotypic adaptation are generally consistent. Additionally, S-line individuals with the mini-muscle phenotype (homozygous for a Mendelian recessive allele that halves hindlimb muscle mass [Garland et al., 2002, Evolution 56:1,267-1,275]) exhibited significantly longer and thinner femora and tibiafibulae, with no difference in bone masses. Two results were considered surprising. First, no differences were found in the MT/F ratio (the classic indicator of cursoriality). Second, we did not find a significant interaction between linetype and wheel access for any trait, despite the higher running rate of S mice.     

Primate limb bones and locomotor types in arboreal or terrestrial environments

Postcranial limb bones were compared among primates of different locomotor types. Seventy-one primate species, in which all families of primates were included, were grouped into nine locomotor types. Osteometrical data on long bones and data on the cross-sectional geometry of the humerus and the femur were studied by means of allometric analysis and principal component analysis. Relatively robust forelimb bones were observed in the primate group which adopted the relatively terrestrial locomotor type compared with the group that adopted the arboreal locomotor type. The difference resembled the previously reported comparison between terrestrial and arboreal groups among all quadrupedal mammals. The degree of arboreality in daily life is connected with the degree of hindlimb dominance, or the ratio of force applied to the fore- and hindlimb in positional behaviour and also with the shape, size and robusticity of limb bones.     

Fossil primates and the evolution of some primate locomotor systems

Of Paleocene primates only Plesiadapis is complete enough to reconstruct locomotor patterns; it was an arboreal scrambler, perhaps functioning like a large squirrel. Eocene lemurs (adapids) show an array of locomotor types much like certain modern Malagasy lemurs. The European Eocene tarsiid Necrolemur and the American Hemiacodon show the beginning of saltatory specializations in possession of elongated calcaneum and astragalus. Although not a direct anthropoid ancestor Necrolemur seems one of the best models for representing the early locomotor type from which higher primates arose. The Oligocene primates of Egypt (among which are the earliest undoubted pongids) are preserved with a forest fauna. Structures of long bones suggest they were arboreal. A considerable number of Miocene ape bones are known and those of Pliopithecus and Dryopithecus indicate similar adaptations. Of African Miocene forms, Dryopithecus major was a large, gorilla-sized animal, and hence perhaps primarily terrestrial. D. africanus was somewhat more arboreally adapted and a partial brachiator. The Italian fossil Oreopithecus, a coal-swamp dweller, shows indications of bipedality in pelvic structure. Ramapithecus, which is presumably ancestral to Australopithecus, shows palatal and facial patterns much like these later hominids, and probably hence had locomotor patterns more like men than like living apes; its lack of the dental specializations of apes strongly supports this suggestion.     

The effects of substratum inclination on locomotor patterns in primates

To explore the change from the horizontal quadrupedal walking to the vertical climbing in primates, I designed an experiment on an inclined substratum. The subjects were an adult male Japanese macaque and a 2-year-old female white-handed gibbon. The animals moved on a substratum made of bamboo pipe (8 cm diameter). The inclination of the substratum was changed from 15 degrees to 65 degrees in 5-degree increments for the Japanese macaque and from 20 degrees to 70 degrees with 10-degree increments for the white-handed gibbon. I placed surface electrodes and telemetry transmitters on the subjects to record the activity of the long head of the triceps brachii and the long head of the biceps brachii muscles. The Japanese macaque utilized horizontal quadrupedal walking until the incline was 15 degrees. Vertical climbing began at an inclination of 55 degrees. The intermediate locomotor mode was observed between 20 degrees and 50 degrees. The white-handed gibbon changed the locomotor mode from horizontal quadrupedal walking to vertical climbing at 40 degrees. I believe that the difference observed in locomotor mode between these two species was mainly due to differences in the intermembral index. The white-handed gibbon had a large intermembral index, which meant she had longer forelimbs and could therefore change locomotor mode at a lower inclination of the substratum.     

Mediolateral reaction forces and forelimb anatomy in quadrupedal primates: implications for interpreting locomotor behavior in fossil primates

The forelimb joints of terrestrial primate quadrupeds appear better able to resist mediolateral (ML) shear forces than those of arboreal quadrupedal monkeys. These differences in forelimb morphology have been used extensively to infer locomotor behavior in extinct primate quadrupeds. However, the nature of ML substrate reaction forces (SRF) during arboreal and terrestrial quadrupedalism in primates is not known. This study documents ML-SRF magnitude and orientation and forelimb joint angles in six quadrupedal anthropoid species walking across a force platform attached to terrestrial (wooden runway) and arboreal supports (raised horizontal poles). On the ground all subjects applied a lateral force in more than 50% of the steps collected. On horizontal poles, in contrast, all subjects applied a medially directed force to the substrate in more than 75% of the steps collected. In addition, all subjects on arboreal supports combined a lower magnitude peak ML-SRF with a change in the timing of the ML-SRF peak force. As a result, during quadrupedalism on the poles the overall SRF resultant was relatively lower than it was on the runway. Most subjects in this study adduct their humerus while on the poles. The kinetic and kinematic variables combine to minimize the tendency to collapse or translate forelimbs joints in an ML plane in primarily arboreal quadrupedal primates compared to primarily terrestrial quadrupedal ones. These data allow for a more complete understanding of the anatomy of the forelimb in terrestrial vs. arboreal quadrupedal primates. A better understanding of the mechanical basis of morphological differences allows greater confidence in inferences concerning the locomotion of extinct primate quadrupeds.     

Differentiation of muscle fiber types in the chicken hindlimb

The differentiation of myotubes into fiber types was studied by examining the ATPase staining characteristics of chicken embryo thigh muscles. Two distinct fiber types, designated type IEMB and IIEMB, could be distinguished as early as stage 29. Paralysis of the embryo with d-tubocurarine prevented the differentiation of type IEMB but not type IIEMB characteristics. The two embryonic fiber types differed from each other, and mature type I and II fibers, in the acid and alkali labilities of their ATPases. Myotubes which were type IEMB at stage 29 matured into type I fibers, whereas those which were type IIEMB predominantly but not exclusively developed into type II fibers. The process of maturation involved sequential changes in the staining characteristics of the myotubes. Thus, the ultimate fiber type of a myotube can be detected long before it expresses its mature characteristics.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Pneumatized spaces,sinuses and spongy bones in the skulls of primates

The earliest attempts to understand the "pneumatized spaces" in the skulls of primates in general were focussed on the hollow spaces and the epithelium which covers their surfaces. More recent approaches consider the sinuses as a means to optimise skull architecture. Still, many attempts to get hold of the meaning of the intriguing pneumatized spaces circle around the air filled volumes they enclose. Here, we would like to reverse the approach and focus our biomechanic interpretation on the walls surrounding the big, empty, or at least not mechanically resistant spaces, and their mechanical properties. As a working hypothesis, we consider not only the walls of the more or less closed cavities, or sinuses, but also the braincase, the orbits, and the nasal channel as thin-walled shells of which we know that they can carry surprisingly large loads with a minimum of material. Details of the wall's profiles fit with this approach. From the same viewpoint, the bubble-like, air-filled cavernous systems in the ethmoid or temporal bones, and the marrow-filled spongy substance in the upper jaw are looked at as honeycomb-structures, which provide mechanical properties that are biologically advantageous and allow the saving of weight.     

Development of behaviour in the hindlimb of Xenopus laevis

The paper is one of a series of studies of the ontogeny of the innervation of the vertebrate limb in which the histogenesis of the nerves is correlated with the development of the pattern of behaviour in the limb. Here, the motility of the developing limb in tadpoles of Xenopus laevis is described, both in the normal larva and those in which the spinal cord is isolated from the brain. In spinal tadpoles the responses of the limb to electrical stimulation are correlated with its normal behaviour.