Iliocostalis muscles in three mammals (dolphin,goat and human): Their identification,structure and innervation

Iliocostalis (IC) muscles were studied in four dolphin embryos, three goat embryos and four Japanese adult cadavers through macroscopic dissection. The IC muscles of the dolphin were located on the lateral aspect of the trunk and displayed an intercostal arrangement. In contrast, the IC muscles in both the goat and human showed a double-layered architecture formed by a multisegmental muscle-tendon complex and were located on the lateral and medial sides of the costal angle, respectively. Generally, the nerve to the iliocostalis (NIC) in the dolphin and goat did not form a common trunk with the nerve to the longissimus on the epaxial plane, whereas in humans the NIC ran parallel to the nerve to the longissimus part of the way. The individual NIC ran caudolaterally, innervating the one lower (caudal) metameric division of the IC muscle in the dolphin and piercing the fascia of the IC muscles at a point in the next caudal intercostal level in the goat and human. In the upper thoracic part of the goat and human, the caudal shift of innervation was obscured, where the IC muscles were close to the vertebrae. The course of the NIC was closely related to that of the lateral cutaneous branch. The present study shows that the NIC is commonly destined for the one lower intercostal level among the three mammalian species, with their respective IC muscles having distinctly different structural complexity.     

Local modulation of the Wnt/β-catenin and bone morphogenic protein (BMP) pathways recapitulates rib defects analogous to cerebro-costo-mandibular syndrome

Ribs are seldom affected by developmental disorders, however, multiple defects in rib structure are observed in the spliceosomal disease cerebro-costo-mandibular syndrome (CCMS). These defects include rib gaps, found in the posterior part of the costal shaft in multiple ribs, as well as missing ribs, shortened ribs and abnormal costotransverse articulations, which result in inadequate ventilation at birth and high perinatal mortality. The genetic mechanism of CCMS is a loss-of-function mutation in SNRPB, a component of the major spliceosome, and knockdown of this gene in vitro affects the activity of the Wnt/β-catenin and bone morphogenic protein (BMP) pathways. The aim of the present study was to investigate whether altering these pathways in vivo can recapitulate rib gaps and other rib abnormalities in the model animal. Chick embryos were implanted with beads soaked in Wnt/β-catenin and BMP pathway modulators during somitogenesis, and incubated until the ribs were formed. Some embryos were harvested in the preceding days for analysis of the chondrogenic marker Sox9, to determine whether pathway modulation affected somite patterning or chondrogenesis. Wnt/β-catenin inhibition manifested characteristic rib phenotypes seen in CCMS, including rib gaps (P < 0.05) and missing ribs (P < 0.05). BMP pathway activation did not cause rib gaps but yielded missing rib (P < 0.01) and shortened rib phenotypes (P < 0.05). A strong association with vertebral phenotypes was also noted with BMP4 (P < 0.001), including scoliosis (P < 0.05), a feature associated with CCMS. Reduced expression of Sox9 was detected with Wnt/β-catenin inhibition, indicating that inhibition of chondrogenesis precipitated the rib defects in the presence of Wnt/β-catenin inhibitors. BMP pathway activators also reduced Sox9 expression, indicating an interruption of somite patterning in the manifestation of rib defects with BMP4. The present study demonstrates that local inhibition of the Wnt/β-catenin and activation of the BMP pathway can recapitulate rib defects, such as those observed in CCMS. The balance of Wnt/β-catenin and BMP in the somite is vital for correct rib morphogenesis, and alteration of the activity of these two pathways in CCMS may perturb this balance during somite patterning, leading to the observed rib defects.     

Fibre type composition in the lumbar perivertebral muscles of primates: implications for the evolution of orthogrady in hominoids

The axial musculoskeletal system is important for the static and dynamic control of the body during both locomotor and non‐locomotor behaviour. As a consequence, major evolutionary changes in the positional habits of a species are reflected by morpho‐functional adaptations of the axial system. Because of the remarkable phenotypic plasticity of muscle tissue, a close relationship exists between muscle morphology and function. One way to explore major evolutionary transitions in muscle function is therefore by comparative analysis of fibre type composition. In this study, the three‐dimensional distribution of slow and fast muscle fibres was analysed in the lumbar perivertebral muscles of two lemuriform (mouse lemur, brown lemur) and four hominoid primate species (white‐handed gibbon, orangutan, bonobo, chimpanzee) in order to develop a plausible scenario for the evolution of the contractile properties of the axial muscles in hominoids and to discern possible changes in muscle physiology that were associated with the evolution of orthogrady. Similar to all previously studied quadrupedal mammals, the lemuriform primates in this study exhibited a morpho‐functional dichotomy between deep slow contracting local stabilizer muscles and superficial fast contracting global mobilizers and stabilizers and thus retained the fibre distribution pattern typical for quadrupedal non‐primates. In contrast, the hominoid primates showed no regionalization of the fibre types, similar to previous observations in Homo. We suggest that this homogeneous fibre composition is associated with the high functional versatility of the axial musculature that was brought about by the evolution of orthograde behaviours and reflects the broad range of mechanical demands acting on the trunk in orthograde hominoids. Because orthogrady is a derived character of euhominoids, the uniform fibre type distribution is hypothesized to coincide with the evolution of orthograde behaviours.     

From the Cover: Swimming muscles power suction feeding in largemouth bass

Most aquatic vertebrates use suction to capture food, relying on rapid expansion of the mouth cavity to accelerate water and food into the mouth. In ray-finned fishes, mouth expansion is both fast and forceful, and therefore requires considerable power. However, the cranial muscles of these fishes are relatively small and may not be able to produce enough power for suction expansion. The axial swimming muscles of these fishes also attach to the feeding apparatus and have the potential to generate mouth expansion. Because of their large size, these axial muscles could contribute substantial power to suction feeding. To determine whether suction feeding is powered primarily by axial muscles, we measured the power required for suction expansion in largemouth bass and compared it to the power capacities of the axial and cranial muscles. Using X-ray reconstruction of moving morphology (XROMM), we generated 3D animations of the mouth skeleton and created a dynamic digital endocast to measure the rate of mouth volume expansion. This time-resolved expansion rate was combined with intraoral pressure recordings to calculate the instantaneous power required for suction feeding. Peak expansion powers for all but the weakest strikes far exceeded the maximum power capacity of the cranial muscles. The axial muscles did not merely contribute but were the primary source of suction expansion power and generated up to 95% of peak expansion power. The recruitment of axial muscle power may have been crucial for the evolution of high-power suction feeding in ray-finned fishes.Muscles produce the astonishing range of motions seen in living animals. Some of the most powerful movements occur during locomotor behaviors such as flying (1), leaping (2), and sprinting (3), and this power is usually generated by large axial and appendicular muscles of the body. Feeding movements such as biting (4) or chewing (5) are typically forceful rather than powerful and rely on the smaller cranial muscles of the head. However, powerful movements and muscles may be found in some feeding systems, such as the suction-feeding behavior of ray-finned fishes.Suction feeding is a powerful prey capture behavior used by most of the over 30,000 species of ray-finned fishes. Fish generate suction by rapid expansion of the mouth cavity—increasing volume and lowering pressure—to accelerate water and prey into the mouth (6). Mouth expansion is facilitated by an exceptionally kinetic cranial skeleton, which is arranged in linkages that allow a single input motion to generate movement of multiple and sometimes distant bones (reviewed in ref. 7). Although the morphology of the cranial skeleton varies hugely across species, the power that moves these linkages, and thereby expands the mouth to suck in water and prey, must always be generated by muscles.The power for suction expansion might be expected to come from cranial muscles, as it does in most vertebrate feeding systems, but it is thought that many fishes may also use axial muscles to power suction feeding (8, 9). The cranial muscles in fishes are indeed active during suction feeding (10) and attach to the cranial skeleton such that their shortening should contribute to mouth expansion (Fig. 1). However, their relatively small size has led to the intriguing hypothesis that cranial muscles are insufficient to produce all of the power for suction expansion (11, 12) and that some of the power required for suction feeding comes from the large axial muscles that typically power swimming (8, 13). In fish, the axial muscles have the potential to generate mouth expansion by elevating the neurocranium and retracting the pectoral girdle, motions that can be transmitted via linkages to the rest of the cranial skeleton (14, 15). How much of suction expansion power is generated by the axial muscles remains unknown because we have no measurements of the actual power required for this rapid, dynamic event.Open in a separate windowFig. 1.Muscles of mouth expansion in largemouth bass. Cranial (sternohyoideus, levator arcus palatini, dilator operculi, levator operculi) and axial (epaxialis, hypaxialis) muscles may contribute power to suction expansion, based on their anatomy and published muscle activity patterns.The power muscles must produce to expand the mouth can be calculated as the product of the rate of volume change and the pressure inside the mouth cavity at any given moment in time (16, 17). Although the pressure in the mouth cavity has been measured during suction expansion in many fish species, similar time-resolved recordings of mouth volume present a formidable challenge. The mouth cavity has a complex, 3D shape and motion, and this internal space is not visible with external light video. The only existing volume data are from estimates and models (18, 19), but it is now possible to measure mouth volume directly with X-ray reconstruction of moving morphology (XROMM) (20). In this study, we used XROMM to produce precise and accurate 3D animations of the bones surrounding the mouth cavity, and then measured the instantaneous volume of this cavity throughout the strike with a dynamic digital endocast (Fig. 2). The resulting volume measurements have high temporal resolution and can be combined with synchronous pressure measurements to measure how much power is required for suction expansion (16, 17).Open in a separate windowFig. 2.Skeletal motions of suction expansion increase mouth cavity volume. Lateral (Left) and rostral (Right) views of an XROMM animation with the dynamic digital endocast at (A) the onset of a strike, (B) maximum mouth volume, and (C) the endocast alone at maximum mouth volume. Only the left-side bones were animated with XROMM and fit with the endocast; endocast volume was doubled to reflect the volume of the whole mouth cavity (shown by dashed outlines in B and C).Our goal was to determine whether the suction feeding of largemouth bass capturing elusive prey is indeed powered by axial swimming muscles, or whether cranial muscle power alone is sufficient. We first measured how much power largemouth bass used to expand their mouth cavities during live suction-feeding strikes. We then compared that suction expansion power to the maximum power that the cranial muscles of these fish were capable of generating. Suction expansion powers exceeding the power capacity of the cranial muscles would indicate that the axial muscles are essential for this powerful feeding behavior.     

Novel concept for the epaxial/hypaxial boundary based on neuronal development

Trunk muscles in vertebrates are classified as either dorsal epaxial or ventral hypaxial muscles. Epaxial and hypaxial muscles are defined as muscles innervated by the dorsal and ventral rami of spinal nerves, respectively. Each cluster of spinal motor neurons passing through dorsal rami innervates epaxial muscles, whereas clusters traveling on the ventral rami innervate hypaxial muscles. Herein, we show that some motor neurons exhibiting molecular profiles for epaxial muscles follow a path in the ventral rami. Dorsal deep-shoulder muscles and some body wall muscles are defined as hypaxial due to innervation via the ventral rami, but a part of these ventral rami has the molecular profile of motor neurons that innervate epaxial muscles. Thus, the epaxial and hypaxial boundary cannot be determined simply by the ramification pattern of spinal nerves. We propose that, although muscle innervation occurs via the ventral rami, dorsal deep-shoulder muscles and some body wall muscles represent an intermediate group that lies between epaxial and hypaxial muscles.     

Epaxial muscle fiber architecture favors enhanced excursion and power in the leaper Galago senegalensis

Galago senegalensis is a habitual arboreal leaper that engages in rapid spinal extension during push‐off. Large muscle excursions and high contraction velocities are important components of leaping, and experimental studies indicate that during leaping by G. senegalensis, peak power is facilitated by elastic storage of energy. To date, however, little is known about the functional relationship between epaxial muscle fiber architecture and locomotion in leaping primates. Here, fiber architecture of select epaxial muscles is compared between G. senegalensis (n = 4) and the slow arboreal quadruped, Nycticebus coucang (n = 4). The hypothesis is tested that G. senegalensis exhibits architectural features of the epaxial muscles that facilitate rapid and powerful spinal extension during the take‐off phase of leaping. As predicted, G. senegalensis epaxial muscles have relatively longer, less pinnate fibers and higher ratios of tendon length‐to‐fiber length, indicating the capacity for generating relatively larger muscle excursions, higher whole‐muscle contraction velocities, and a greater capacity for elastic energy storage. Thus, the relatively longer fibers and higher tendon length‐to‐fiber length ratios can be functionally linked to leaping performance in G. senegalensis. It is further predicted that G. senegalensis epaxial muscles have relatively smaller physiological cross‐sectional areas (PCSAs) as a consequence of an architectural trade‐off between fiber length (excursion) and PCSA (force). Contrary to this prediction, there are no species differences in relative PCSAs, but the smaller‐bodied G. senegalensis trends towards relatively larger epaxial muscle mass. These findings suggest that relative increase in muscle mass in G. senegalensis is largely attributable to longer fibers. The relative increase in erector spinae muscle mass may facilitate sagittal flexibility during leaping. The similarity between species in relative PCSAs provides empirical support for previous work linking osteological features of the vertebral column in lorisids with axial stability and reduced muscular effort associated with slow, deliberate movements during anti‐pronograde locomotion.     

Distribution Pattern of Muscle Fiber Types in the Perivertebral Musculature of Two Different Sized Species of Mice

Many physiological parameters scale with body size. Regarding limb muscles, it has been shown that the demands for relatively faster muscles, less postural work, and greater heat production in small mammals are met by lower proportions of Type I and conversely higher proportions of Type II fibers. To investigate possible adaptations of the perivertebral musculature, we investigated the proportion, spatial distribution, and cross‐sectional area (csa) of the different muscle fiber types in the laboratory and harvest mouse. Serial cross sections from the posterior thoracic to the lumbo‐sacral region were prepared and Type I, IIA, and IIB fibers identified using enzymehistochemistry. The general distribution of Type I and IIB fibers, as well as the more or less equal distribution of IIA fibers, resembles the pattern found in other mammals. However, the overall proportion of Type I fibers was very low in the laboratory mouse and particularly low in the harvest mouse. Muscular adaptations to a small body size were met primarily by increased Type IIA fiber proportions. Thereby, not all muscles or muscle regions similarly reflected the expected scaling effects. However, our results clearly show that body size is a critical factor when fiber‐type proportions are compared among different sized mammals. Anat Rec, 293:446–463, 2010. © 2010 Wiley‐Liss, Inc.