Digital cranial endocast of Riograndia guaibensis (Late Triassic,Brazil) sheds light on the evolution of the brain in non-mammalian cynodonts

Abstract

A digital cranial endocast of the specimen UFRGS-PV-596-T of Riograndia guaibensis was obtained from μCT scan images. This is a small cynodont, closely related to mammaliaforms, from the Late Triassic of Brazil. Riograndia has large olfactory bulb casts and the cerebral hemispheres region is relatively wider than in other non-mammaliaform cynodonts. Impressions of vessels were observed and a conspicuous mark on the dorsal surface was interpreted as the transverse sinus. The calculated encephalization quotient is greater than the range seen in most other non-mammaliaform cynodonts. The ratios between linear and area measurements of the dorsal surface suggest four evolutionary changes from a basal eucynodont morphology to mammaliaforms, involving an evolutionary increase of the relative size of the olfactory bulbs and the width of the cerebral hemispheres and cerebellum. The data supports the hypothesis of the neurological evolution of the mammalian lineage starting with a trend for an increase of the olfactory bulbs, which is associated with adaptations in the nasal cavity. This trend is suggested to be linked to the selective pressures for small-sized faunivorous, and probably nocturnal, animals, and represents an initial improvement of the sensory receptor system, subsequently leading to further development of the ‘superior’ structures for sensorial processing and integration.     

Forelimb Kinematics of Rats Using XROMM,with Implications for Small Eutherians and Their Fossil Relatives

The earliest eutherian mammals were small-bodied locomotor generalists with a forelimb morphology that strongly resembles that of extant rats. Understanding the kinematics of the humerus, radius, and ulna of extant rats can inform and constrain hypotheses concerning typical posture and mobility in early eutherian forelimbs. The locomotion of Rattus norvegicus has been extensively studied, but the three-dimensional kinematics of the bones themselves remains under-explored. Here, for the first time, we use markerless XROMM (Scientific Rotoscoping) to explore the three-dimensional long bone movements in Rattus norvegicus during a normal, symmetrical gait (walking). Our data show a basic kinematic profile that agrees with previous studies on rats and other small therians: rats maintain a crouched forelimb posture throughout the step cycle, and the ulna is confined to flexion/extension in a parasagittal plane. However, our three-dimensional data illuminate long-axis rotation (LAR) movements for both the humerus and the radius for the first time. Medial LAR of the humerus throughout stance maintains an adducted elbow with a caudally-facing olecranon process, which in turn maintains a cranially-directed manus orientation (pronation). The radius also shows significant LAR correlated with manus pronation and supination. Moreover, we report that elbow flexion and manus orientation are correlated in R. norvegicus: as the elbow angle becomes more acute, manus supination increases. Our data also suggest that manus pronation and orientation in R. norvegicus rely on a divided system of labor between the ulna and radius. Given that the radius follows the flexion and extension trajectory of the ulna, it must rotate at the elbow (on the capitulum) so that during the stance phase its distal end lies medial to ulna, ensuring that the manus remains pronated while the forelimb is supporting the body. We suggest that forelimb posture and kinematics in Juramaia, Eomaia, and other basal eutherians were grossly similar to those of rats, and that humerus and radius LAR may have always played a significant role in forelimb and manus posture in small eutherian mammals.     

Anatomy and histochemistry of spread-wing posture in birds. I. Wing drying posture in the double-crested cormorant,Phalacrocorax auritus

Spread-wing postures of birds often have been studied with respect to the function of behavior, but ignored with regard to the mechanism by which the birds accomplish posture. The double-crested cormorant, Phalacrocorax auritus, was used as a model for this study of spread-wing posture. Those muscles capable of positioning and maintaining the wing in extension and protraction were assayed histochemically for the presence of slow (postural) muscle fibers. Within the forelimb of Phalacrocorax, Mm. coracobrachialis cranialis, pectoralis thoracicus (cranial portion), deltoideus minor, triceps scapularis, and extensor metacarpi radialis pars dorsalis and ventralis were found to contain populations of slow-twitch or slow-tonic muscle fibers. These slow fibers in the above muscles are considered to function during spread-wing posture in this species. J Morphol 233:67–76, 1997. © 1997 Wiley-Liss, Inc.     

The interplay between speed,kinetics, and hand postures during primate terrestrial locomotion

Nonprimate terrestrial mammals may use digitigrade postures to help moderate distal limb joint moments and metapodial stresses that may arise during high‐speed locomotion with high‐ground reaction forces (GRF). This study evaluates the relationships between speed, GRFs, and distal forelimb kinematics in order to evaluate if primates also adopt digitigrade hand postures during terrestrial locomotion for these same reasons. Three cercopithecine monkey species (Papio anubis, Macaca mulatta, Erythrocebus patas) were videotaped moving unrestrained along a horizontal runway instrumented with a force platform. Three‐dimensional forelimb kinematics and GRFs were measured when the vertical force component reached its peak. Hand posture was measured as the angle between the metacarpal segment and the ground (MGA). As predicted, digitigrade hand postures (larger MGA) are associated with shorter GRF moment arms and lower wrist joint moments. Contrary to expectations, individuals used more palmigrade‐like (i.e. less digitigrade) hand postures (smaller MGA) when the forelimb was subjected to higher forces (at faster speeds) resulting in potentially larger wrist joint moments. Accordingly, these primates may not use their ability to alter their hand postures to reduce rising joint moments at faster speeds. Digitigrady at slow speeds may improve the mechanical advantage of antigravity muscles crossing the wrist joint. At faster speeds, greater palmigrady is likely caused by joint collapse, but this posture may be suited to distribute higher GRFs over a larger surface area to lower stresses throughout the hand. Thus, a digitigrade hand posture is not a cursorial (i.e. high speed) adaptation in primates and differs from that of other mammals. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Differential expression of choline kinase isoforms in skeletal muscle explains the phenotypic variability in the rostrocaudal muscular dystrophy mouse

Choline kinase in mammals is encoded by two genes, Chka and Chkb. Disruption of murine Chka leads to embryonic lethality, whereas a spontaneous genomic deletion in murine Chkb results in neonatal forelimb bone deformity and hindlimb muscular dystrophy. Surprisingly, muscular dystrophy isn't significantly developed in the forelimb. We have investigated the mechanism by which a lack of choline kinase β, encoded by Chkb, results in minimal muscular dystrophy in forelimbs. We have found that choline kinase β is the major isoform in hindlimb muscle and contributes more to choline kinase activity, while choline kinase α is predominant in forelimb muscle and contributes more to choline kinase activity. Although choline kinase activity is decreased in forelimb muscles of Chkb^−/− mice, the activity of CTP:phosphocholine cytidylyltransferase is increased, resulting in enhanced phosphatidylcholine biosynthesis. The activity of phosphatidylcholine phospholipase C is up-regulated while the activity of phospholipase A₂ in forelimb muscle is not altered. Regeneration of forelimb muscles of Chkb^−/− mice is normal when challenged with cardiotoxin. In contrast to hindlimb muscle, mega-mitochondria are not significantly formed in forelimb muscle of Chkb^−/− mice. We conclude that the relative lack of muscle degeneration in forelimbs of Chkb^−/− mice is due to abundant choline kinase α and the stable homeostasis of phosphatidylcholine.     

Study of Biomphalaria Tenagophila Tenagophila, B. t. Guaibensis and B. Occidentalis by Polymerase Chain Reaction Amplification and Restriction Enzyme Digestion of the Ribosomal RNA Intergenic Spacer Regions

Biomphalaria tenagophila tenagophila, B. tenagophila guaibensisand B. occidentalis are indistinguishable on the basis of shellmorphology and the majority of organs of the genital system.Only B. t. tenagophila is susceptible to infection with Schistosomamansoni. The identification of this species is important forepidemiological studies of schistosomiasis. Snails from differentsites in Brazil, Argentine and Uruguay were studied using thePolymerase Chain Reaction (PCR) and Restriction Fragment LengthPolymorphism (RFLP) of the Ribosomal RNA Internal TranscribedSpacers (ITS) using seven enzymes. Profiles resulting from digestionwith AluI showed some invariant species-specific products allowingcorrect identification of B. t. tenagophila, B. occidentalisand B. t. guaibensis. Profiles obtained with other enzymes didnot permit species identification as extensive intraspecificpolymorphism or invariant RFLP profiles were observed. Restriction profiles obtainedwith all enzymes were used to calculate the percentage of bandsharing between all individual snails and these data were usedfor a cluster analysis. A closer relationship between B. occidentalisand B. t. guaibensis than B. t. tenagophila and the subspeciesB. t. guaibensis was observed. Based on previous morphologicaldata and these molecular data, we propose grouping B. t. tenagophila,B. occidentalis and B. t. guaibensis into a B. tenagophila complex. (Received 22 December 1997; accepted 26 May 1998)     

Macrauchenia patachonica Owen, 1838: Limb bones morphology,locomotory biomechanics,and paleobiological inferences

Macrauchenia patachonica Owen, 1838 was among the last and largest litopterns, an extinct order of South American native ungulates. Macrauchenia patachonica had anatomical peculiarities as extremely retracted nasals, enlarged cervical vertebrae, and limb bones proportions without good living analogs that lead to asking about its paleobiology. To quantitatively assess the strange combination of limb bone features in M. patachonica, we constructed an indicator of differences in anatomical adaptations for efficient running between forelimb and hind limb (IDFH). We also made a multivariate analysis using data on osteological ratios of living mammals and two other litopterns. We discuss several biomechanical and paleobiological implications of the striking differences between hind limb and forelimb design in M. patachonica. Our main suggestion is that M. patachonica, during fast locomotion, probably used a posture with the neck in a horizontal position.     

Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer)

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch-dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m _m), pennation angle, and fiber length (FL) to calculate physiological cross-sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass-specific m _m, PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m _m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch-digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch-digging.     

Functional Anatomy of the Forelimb Muscles of the Ocelot (Leopardus pardalis)

The myology of most members of the cat family (Felidae) is poorly documented. This study describes the forelimb myology of the ocelot (Leopardus pardalis) and compares the forelimb anatomy of the ocelot to that of other well-documented felids (Felis catus, Panthera leo). A substantial number of myological features vary among the three species and are distributed in a manner consistent with major ecomorphological variables (prey size preference and locomotor repertoire). The origin of m. triceps brachii caput longum is most extensive in Panthera leo, consistent with the fact that this species pursues prey over greater distances compared to F. catus or L. pardalis. In addition, the origins and insertions of the pronator and supinator musculature are reduced in Felis catus, which has little need to supinate during locomotion or prey capture. Furthermore, muscles serving the digits are best developed in the lion and ocelot, both of which make greater use of the forelimb for grasping and manipulation than does the domestic cat. However, while the lion probably retains the primitive morphology for the family, the ocelot shows evidence of secondary adaptation to increased mobility of the digits. Overall, results indicate that additional studies of felid forelimb myology are warranted, as they are likely to provide valuable functional insights.     

Architectural Properties of Sloth Forelimb Muscles (Pilosa: Bradypodidae)

Tree sloths have reduced skeletal muscle mass, and yet they are able to perform suspensory behaviors that require both strength and fatigue resistance to suspend their body mass for extended periods of time. The muscle architecture of sloths is hypothesized to be modified in ways that will enhance force production to compensate for this reduction in limb muscle mass. Our objective is to test this hypothesis by quantifying architecture properties in the forelimb musculature of the brown-throated three-toed sloth (Bradypus variegatus: N = 4). We evaluated architecture from 52 forelimb muscles by measuring muscle moment arm (r _m), muscle mass (MM), belly length (ML), fascicle length (L_F), pennation angle (θ), and physiological cross-sectional area (PCSA), and these metrics were used to estimate isometric force, joint torque, and power. Overall, the musculature becomes progressively more pennate from the extrinsic to intrinsic regions of the forelimb, and the flexors are more well developed than the extensors as predicted. However, most muscles are indicative of a mechanical design for fast joint rotational velocity instead of large joint torque (i.e., strength), although certain large, parallel-fibered shoulder (e.g., m. latissimus dorsi) and elbow (e.g., m. brachioradialis) flexors are capable of producing appreciable torques by having elongated moment arms. This type of functional tradeoff between joint rotational velocity and mechanical advantage is further exemplified by muscle gearing in Bradypus that pairs synergistic muscles with opposing L_F/r _m ratios in each functional group. These properties are suggested to facilitate the slow, controlled movements in sloths. In addition, the carpal/digital flexors have variable architectural properties, but their collective PCSA and joint torque indicates the capability for maintaining grip force and carpal stability while distributing load from the manus to the shoulder. The observed specializations provide a basis for understanding sustained suspension in sloths.     

Androgen regulation of neuromuscular junction structure and function in a sexually dimorphic muscle of the frog Xenopus laevis

Specific forelimb muscles in anurans are sexually dimorphic and underlie the androgen-dependent clasping response of males during amplexus. Previous studies have reported that androgen treatment slows the contractile properties of these sexually dimorphic forelimb muscles. In amphibians, the expression of functionally distinct acetycholine (ACh) receptors, the levels of acetylcholinesterase (AChE), the extent of multiple innervation, and the structure of individual end plates vary with the contractile properties of the muscle fibers. In higher vertebrates, androgens have been reported to alter the expression of ACh receptors, AChE, and the neuromodulator, calcitonin gene-related peptide (CGRP). To determine whether the known androgen-dependent changes in contraction of androgen-sensitive forelimb muscles are accompanied by concomitant changes in synaptic structure or function, we have compared functional neuromuscular transmission, the pattern of innervation, and CGRP immunoreactivity in nerve or muscle preparation from castrated (C) and castrated and testosterone-treated (CT) adult male Xenopus laevis. CGRP expression in androgen receptor (AR)-immunopositive neurons was increased in CT animals. However, no significant differences were found in ACh-mediated single channel or macroscopic currents, the extent of multiple end plates, or end plate morphology for forelimb fibers isolated from C and CT Xenopus. In contrast, analysis of forelimb fibers from gonadally intact adult females and juvenile animals of both sexes revealed that macroscopic synaptic currents were significantly shorter in these animals than in either C or CT adult males. Our data suggest that forelimb fibers in sexually dimorphic muscles of Xenopus do show significant differences in synaptic transmission; however, neither end-plate organization nor functional neuromuscular transmission are subject to activational effects of androgens in adult male frogs. © 1995 John Wiley & Sons, Inc.     

Lumbar posture and muscular activity while sitting during office work

PurposeField study, cross-sectional study to measure the posture and sEMG of the lumbar spine during office work for a better understanding of the lumbar spine within such conditions.ScopeThere is high incidence of low back pain in office workers. Currently there is little information about lumbar posture and the activity of lumbar muscles during extended office work.MethodsThirteen volunteers were examined for around 2 h of their normal office work. Typical tasks were documented and synchronised to a portable long term measuring device for sEMG and posture examination. The correlation of lumbar spine posture and sEMG was tested statistically.ResultsThe majority of time spent in office work was sedentary (82%). Only 5% of the measured time was undertaken in erect body position (standing or walking). The sEMG of the lumbar muscles under investigation was task dependent. A strong relation to lumbar spine posture was found within each task. The more the lumbar spine was flexed, the less there was activation of lumbar muscles (P < .01). Periods of very low or no activation of lumbar muscles accounted for about 30% of relaxed sitting postures.ConclusionBecause of very low activation of lumbar muscles while sitting, the load is transmitted by passive structures like ligaments and intervertebral discs. Due to the viscoelasticity of passive structures and low activation of lumbar muscles, the lumbar spine may incline into de-conditioning. This may be a reason for low back pain.     

Distribution of muscle fibers in skeletal muscles of the cheetah (Acinonyx jubatus)

We examine the muscle fiber population of skeletal muscles from whole body in the cheetah (Acinonyx jubatus). In the present experiments, we showed the characteristics of fiber composition in the cheetah by comparative studies among the cheetah, domestic cat, and the beagle dog. Fiber population was determined on muscle fibers stained with monoclonal antibody to each myosin heavy chain isoform. Histochemical analysis demonstrated that many muscles in the cheetah and domestic cat had a low percentage of Type I fibers and a high percentage of Type IIx fibers, while those in the beagle dog showed a high percentage of Type IIa. The hindlimb muscles in the cheetah had a higher percentage of Type II (Type IIa + IIx) fiber than the forelimb muscles. This fact suggests that the propulsive role of the hindlimb is greater than the forelimb in the cheetah. The longissimus in the cheetah had a high percentage of Type IIx fibers over a wide range from the thoracic to lumbar parts, while the population of muscle fibers in this muscle was different depending on the parts in the domestic cat and beagle dog. This indicates that the cheetah can produce a strong and quick extension of the spinal column and increase its stiffness during locomotion. Furthermore, we found the notable difference of muscle fiber type population between flexors and extensors of digits in the cheetah. The present experiments show the characteristics of muscle fibers in the cheetah, corresponded to its ability to perform high-speed running.     

Positional information in the forelimb of the axolotl: experiments with double-half tissues

It has been demonstrated recently that upper forelimbs of axolotls comprised of symmetrically arranged soft tissues do not regenerate (P. W. Tank, 1978,J. Exp. Zool.204, 325–336). These double-half forelimb stumps contained skin, muscle, and loose connective tissues in symmetrical arrangement. The present study explores the roles of muscle, skin, and epidermis in the regeneration of double-half forelimbs by grafting them separately to create forelimb stumps bearing symmetrical arrangements of these individual tissues. Forelimb stumps bearing symmetrically arranged flexor and extensor muscles and normally arranged skin underwent complete regeneration (96%). Forelimbs comprised of double-half skin overlying normally arranged muscles and deep tissues formed hypomorphic structures and nonregenerates (56%) with some single and multiple regenerates. Limbs with double-half deep tissues and complete epidermis either regenerated distally incomplete patterns (47%), single patterns (33%), or multiple patterns (20%). Those forelimbs comprised of double-half skin and no muscle regenerated incomplete patterns in the majority of cases (56%) but single and multiple limbs also were formed. Based on these results it can be concluded that no single type of tissue is solely responsible for the regenerative failure experienced by double-half forelimbs in the earlier study. The complete failure of forelimb regeneration occurs only when all types of soft tissues tested (skin, muscle, and deep connective tissues) are present in symmetrical arrangement.     

Locomotor function shapes the passive mechanical properties and operating lengths of muscle

Locomotor muscles often perform diverse roles, functioning as motors that produce mechanical energy, struts that produce force and brakes that dissipate mechanical energy. In many vertebrate muscles, these functions are not mutually exclusive and a single muscle often performs a range of mechanically diverse tasks. This functional diversity has obscured the relationship between a muscle''s locomotor function and its mechanical properties. I use hopping in toads as a model system for comparing muscles that primarily produce mechanical energy with muscles that primarily dissipate mechanical energy. During hopping, hindlimb muscles undergo active shortening to produce mechanical energy and propel the animal into the air, whereas the forelimb muscles undergo active lengthening to dissipate mechanical energy during landing. Muscles performing distinct mechanical functions operate on different regions of the force–length curve. These findings suggest that a muscle''s operating length may be shaped by potential trade-offs between force production and sarcomere stability. In addition, the passive force–length properties of hindlimb and forelimb muscles vary, suggesting that passive stiffness functions to restrict the muscle''s operating length in vivo. These results inform our understanding of vertebrate muscle variation by providing a clear link between a muscle''s locomotor function and its mechanical properties.     

The effects of upper limb posture and a sub-maximal gripping task on corticospinal excitability to muscles of the forearm

Variations in handgrip force influences shoulder muscle activity, and this effect is dependent upon upper limb position. Previous work suggests that neural coupling between proximal and distal muscles with changes in joint position is a possible mechanism but these studies tend to use artificially constrained postures that do not reflect activities of daily living. The purpose of this study was to examine the effects of upper limb posture on corticospinal excitability to the forearm muscles during workplace relevant arm positions. Motor evoked potentials (MEPs) were elicited in four forearm muscles via transcranial magnetic stimulation at six arm positions (45°, 90° and 120° of humeral elevation in both the flexion and abduction planes). MEPs were delivered as stimulus–response curves (SRCs) at rest and at constant intensity during two gripping tasks. Boltzmann plateau levels were smaller for the flexor carpi radialis in flexion at 45° versus 90° (p = 0.0008). Extensor carpi radialis had a greater plateau during flexion than abduction (p = 0.0042). Corticospinal excitability to the forearm muscles were influenced by upper limb posture during both the resting and gripping conditions. This provides further evidence that upper limb movements are controlled as a whole rather than segmentally and is relevant for workplace design considerations.     

EMG in rotation–flexion of the torso

The objective of this study was to determine the magnitude and phasic relationship of the torso muscles in rotation–flexion of varying degree of asymmetries of the trunk. Nineteen normal young subjects (7 males and 12 females) were stabilized on a posture stabilizing platform and instructed to assume a flexed and right rotated posture. A combination 20°, 40° and 60° of rotation and 20°, 40° and 60° of flexion resulted in nine postures. These postures were assumed in a random order. The subjects were asked to exert their maximal voluntary isometric contraction (MVC) in the plane of rotation of the posture assumed for a period of 5 s. The surface EMG from the external and internal obliques, rectus abdominis, latissimus dorsi and erector spinae at the 10th thoracic and 3rd lumbar vertebral levels was recorded. The abdominal muscles had the least response at 40° of flexion, the dorsal muscles had the highest magnitude.With increasing right rotation, the left external oblique continued to decrease its activity. The ANOVA revealed that rotation and muscles had a significant main effect on normalized peak EMG (p < 0.02) in both genders. There was a significant interaction between rotation and flexion in both genders (p < 0.02) and rotation and muscle in females. The erector spinae activity was highest at 40° flexion, due to greater mechanical disadvantage and having not reached the state of flexion–relaxation. The abdominal muscle activity declined with increasing asymmetry, due to the decreasing initial muscle length. The EMG activity was significantly affected by rotation than flexion (p < 0.02).     

Cellular and molecular investigations into the development of the pectoral girdle

The forelimbs of higher vertebrates are composed of two portions: the appendicular region (stylopod, zeugopod and autopod) and the less prominent proximal girdle elements (scapula and clavicle) that brace the limb to the main trunk axis.We show that the formation of the muscles of the proximal limb occurs through two distinct mechanisms. The more superficial girdle muscles (pectoral and latissimus dorsi) develop by the “In–Out” mechanism whereby migration of myogenic cells from the somites into the limb bud is followed by their extension from the proximal limb bud out onto the thorax. In contrast, the deeper girdle muscles (e.g. rhomboideus profundus and serratus anterior) are induced by the forelimb field which promotes myotomal extension directly from the somites. Tbx5 inactivation demonstrated its requirement for the development of all forelimb elements which include the skeletal elements, proximal and distal muscles as well as the sternum in mammals and the cleithrum of fish. Intriguingly, the formation of the diaphragm musculature is also dependent on the Tbx5 programme. These observations challenge our classical views of the boundary between limb and trunk tissues. We suggest that significant structures located in the body should be considered as components of the forelimb.