Regional changes in vertebra morphology during ontogeny reflect the life history of Atlantic cod (Gadus morhua L.)

This study examined vertebra formation, morphology, regional characters, and bending properties of the vertebral column of Atlantic cod throughout its life cycle (0–6 years). The first structure to form was the foremost neural arch, 21 days post hatching (dph), and the first vertebra centrum to form – as a chordacentrum – was the 3rd centrum at 28 dph. Thereafter, the notochord centra developed in a regular sequence towards the head and caudal fin. All vertebrae were formed within 50 dph. The vertebral column consisted of 52 (± 2) vertebrae (V) and could be divided into four distinct regions: (i) the cervical region (neck) (V1 and V2), characterized by short vertebra centra, prominent neural spines and absence of articulations with ribs; (ii) the abdominal region (trunk) (V3–V19), characterized by vertebrae with wing‐shaped transverse processes (parapophyses) that all articulate with a rib; (iii) the caudal region (tail) (V20–V40), where the vertebra centra have haemal arches with prominent haemal spines; (iv) the ural region (V41 to the last vertebra), characterized by broad neural and haemal spines, providing sites of origin for muscles inserting on the fin rays – lepidotrichs – of the tail fin. The number of vertebrae in the cervical, abdominal and caudal regions was found to be constant, whereas in the ural region, numbers varied from 12 to 15. Geometric modelling based on combination of vertebra lengths, diameters and intervertebral distances showed an even flexibility throughout the column, except in the ural region, where flexibility increased. Throughout ontogeny, the vertebra centra of the different regions followed distinct patterns of growth; the relative length of the vertebrae increased in the cervical and abdominal regions, and decreased in the caudal and ural regions with increasing age. This may reflect changes in swimming mode with age, and/or that the production of large volumes of gametes during sexual maturation requires a significant increase in abdominal cavity volume.     

Notochord segmentation may lay down the pathway for the development of the vertebral bodies in the Atlantic salmon

This study indicates that the development of the vertebrae in the Atlantic salmon requires the orchestration of two sources of metameric patterning, derived from the notochord and the somite rows, respectively. Before segmentation of the salmon notochord, chordoblasts exhibit a well-defined cell axis that is uniformly aligned with the cranio-caudal axis. The morphology of these cells is characterised by a foot-like basal projection that rests on the notochordal sheath. Notochordal segments are initially formed within the chordoblast layer by metameric change in the axial orientation of groups of chordoblasts. This process results in the formation of circular bands of chordoblasts, with feet perpendicular to the cranio-caudal axis, the original chordoblast orientation. Each vertebra is defined by two such chordoblast bands, at the cranial and caudal borders, respectively. Formation of the chordoblast segments closely precedes formation of the chordacentra, which form as calcified rings within the adjacent notochordal sheath. Sclerotomal osteoblasts then differentiate on the surface of the chordacentra, using them as foundations for further vertebral growth. Thus, the morphogenesis of the rudiments of the vertebral bodies is initiated by a generation of segments within the chordoblast layer. This dual segmentation model for salmon, in which the segmental patterns of the neural and haemal arches are somite-derived, while the vertebral segments seem to be notochord-derived, contrasts with current models for avians and mammals.     

From somites to vertebral column.

We report on the development and differentiation of the somites with respect to vertebral column formation in avian and human embryos. The somites, which are made up of different compartments, establish a segmental pattern which becomes transferred to adjacent structures such as the peripheral nervous system and the vascular system. Each vertebra arises from three sclerotomic areas. The paired lateral ones give rise to the neural arches, the ribs and the pedicles of vertebrae, whereas the vertebral body and the intervening disc develop from the axially-located mesenchyme. The neural arches originate from the caudal half of one somite, whereas the vertebral body is made up of the adjacent parts of two somites. Interactions between notochord and axial mesenchyme are a prerequisite for the normal development of vertebral bodies and intervening discs. The neural arches form a frame for the neural tube and spinal ganglia. The boundary between head and vertebral column is located between the 5th and 6th somites. In the human embryo, proatlas, body of the atlas segment, and body of the axis fuse to form the axis.     

Osteophytes: The product of convergent evolution

The very reasonable suggestion, that diarthrodial joint and juxta-discal (vertebral centra-marginal) bony overgrowths (referred to as osteophytes) have different etiologies, has eluded previous confirmation. The prevailing perspective is that diarthrodial osteophytes represent the product of compressive forces and that those on the margins of vertebral centra result from traction and therefore are enthesial in derivation. If diarthrodial joint osteophytes result from intrinsic pressures, any surface responses would require transcortical nutritional support, easily recognized by en face microscopic examination. This contrasts with enthesially derived growth, the surface of which is characterized by Sharpey's fiber insertions. These are recognized as inverted cones with a central protrusion on examination of related bone surfaces. We hypothesize that diarthrodial and disc-adjacent osteophytes have a different pathophysiology, distinguishable on the basis of microscopic surface appearance. We pursued microscopic examination of the surfaces of osteophytes present on diarthrodial joints (hip, knee, elbow, costovertebral) and vertebrae (cervical, thoracic, and lumbar) from the CAL Milano Cemetery Skeletal Collection for presence of transcortical channels and the inverted cones of Sharpey's fiber insertions. Examination of 22 diarthrodial joint osteophytes reveals the presence solely of transcortical channels, while examination of 35 vertebral centra marginal osteophytes reveals the presence only of inverted cones. Findings are independent of age, gender, joint affected, position in the spinal column and osteophyte “severity.” It is now evidenced that all osteophytes are not created equal. Diarthrodial joint osteophytes are endochondrally derived; vertebral centra osteophytes, enthesial in derivation. Different pathophysiology at least partially explain the clinical character of these processes.     

Histology-based morphology of the neurocentral synchondrosis in Alligator mississippiensis (Archosauria, Crocodylia)

Morphology of the neurocentral synchondroses--thin cartilaginous layers between centra and neural arches--are documented in the extant crocodilian, Alligator mississippiensis (Archosauria, Crocodylia). Examination of dry skeletons demonstrates that neurocentral suture closure occurs in very late postnatal ontogeny (after reaching sexual maturity and/or body size ca. 40% from the upper range). Before sexual maturity (body length (BL) ≥ ca. 1.80 m), completely fused centra and neural arches are restricted to the caudal vertebral series. In contrast, the presacral vertebrae often remain unfused throughout postnatal ontogeny, retaining open sutures in very mature individuals (BL ≥ 2.80 m). These unfused centra and neural arches are structurally supported by the relatively large surface area of the neurocentral junctions, which results from primarily horizontal (mediolateral) increases with strong positive allometry. Cleared and stained specimens show that the cartilaginous neurocentral synchondrosis starts to form after approximately 40 embryonic days. Histological examination of the neurocentral junction in dorsal and anterior caudal vertebrae of six individuals (BL = 0.28-3.12 m) shows : (1) neurocentral fusion is the result of endochondral ossification of the neurocentral synchondrosis, (2) the neurocentral synchondrosis exhibits bipolar organization of three types of cartilaginous cells, and (3) complex neurocentral sutures (i.e., curved, zigzagged, and/or interdigitated boundaries) come from clumping of bone cells of the neural arches and centra into the neurocentral synchondrosis. The last two morphological features can be advantageous for delaying neurocentral fusion, which seems to be unique in crocodilians and possibly their close relatives, including nonavian dinosaurs and other Mesozoic archosaurs.     

Role of somite patterning in the formation of Weberian apparatus and pleural rib in zebrafish

In the vertebrate body, a metameric structure is present along the anterior–posterior axis. Zebrafish tbx6^−/− larvae, in which somite boundaries do not form during embryogenesis, were shown to exhibit abnormal skeletal morphology such as rib, neural arch and hemal arch. In this study, we investigated the role of somite patterning in the formation of anterior vertebrae and ribs in more detail. Using three-dimensional computed tomography scans, we found that anterior vertebrae including the Weberian apparatus were severely affected in tbx6^−/− larvae. In addition, pleural ribs of tbx6 mutants exhibited severe defects in the initial ossification, extension of ossification, and formation of parapophyses. Two-colour staining revealed that bifurcation of ribs was caused by fusion or branching of ribs in tbx6^−/−. The parapophyses in tbx6^−/− juvenile fish showed irregular positioning to centra and abnormal attachment to ribs. Furthermore, we found that the ossification of the distal portion of ribs proceeded along myotome boundaries even in irregularly positioned myotome boundaries. These results provide evidence of the contribution of somite patterning to the formation of the Weberian apparatus and rib in zebrafish.     

Trajectory architecture of the trabecular bone between the body and the neural arch in human vertebrae

The cancellous structure of vertebrae has been studied to investigate the direction of trabeculae and thus the lines of stress. The trabecular bone of the pedicle, connecting the body to the lamina, differed in different regions of the vertebral column. At C2 level, it was found that trabeculae are involved in transfer of th column. At C2 level, it was found that trabeculae are involved in transfer of the compressive forces from the superior articular surface to the inferior articular process and body. Throughout the thoracic region, trabeculae in the pedicle were inclined anteriorly towards the body, indicating that compressive forces in the thoracic spine are transferred from the neural arch to the body. In the lower lumbar region, trabeculae run from the body towards the neural arch. Trabeculae in the thoracic transverse processes extend from the costal facet to the lamina, suggesting that weight brought by the ribs to the costotransverse articulations is transmitted to laminae through transverse processes.     

Developmental pathways of vertebral centra and neural arches in human embryos and fetuses

Summary The ossification pathways of both vertebral centra (i.e., vertebral bodies) and neural arches were studied in human embryos and fetuses (CR-length between 38 and 116 mm). A clearing and double-staining method for whole embryo or fetus, using alcian blue and alizarin red S, allowed an easy and precise detection of the morphology of the whole vertebral column and every single vertebra. Both cartilaginous and bony components were clearly visible. Different temporal and topographical patterns of ossification were shown for the centra and arches; the latter were respectively proximaldistal (i.e., bidirectional from a defined starting tract in T10-L1) and cranial-caudal (i.e., monodirectional). The patterns could be related to the morphogenetic processes of other structures (i.e., muscles and nerves). Moreover, the numerical survey of ossification centers provided a possible parameter for the determination of the fetal developmental age. This could be useful in the study of pathological conditions.     

Developmental Failure of Segmentation in a Caudal Vertebra of Apatosaurus (Sauropoda)

A vertebral element assigned to an Apatosaurus cf. ajax from the Late Jurassic Morrison Formation is described. The specimen exhibits an unusual morphology where two vertebrae are nearly seamlessly fused together, including the haemal arch that spans them. This morphology is thought be the result of a developmental abnormality. CT scans of the specimen reveal a thin zone of dorsoventral thickening between the two neural arches consistent with cortical bone. Contrast in internal morphology differentiates the anterior and posterior vertebral bodies with the anterior expressing greater porosity, which increased accommodation for barite‐rich calcite precipitation. No vacuities are observed to suggest the former presence of an intervertebral disk or intervertebral joints: the absence of an intervertebral disc or intervertebral joints is indicative of a condition known as block vertebra. Block vertebrae occur with the loss, or inhibition, of somitocoele mesenchyme early in embyogenesis (i.e., during resegmentation of the somites responsible for the formation of the affected vertebra). The derivatives of somitocoele mesenchyme include the intervertebral disc and joints. Although vertebral paleopathologies are not uncommon in the fossil record, this specimen is the first recognized congenital malformation within Sauropoda. Anat Rec, 297:1262–1269, 2014. © 2014 Wiley Periodicals, Inc.     

Development and evolution of the notarium in Pterosauria

The notarium is the structure formed by fusion of the dorsal vertebrae which occurred independently in pterosaurs and birds. This ankylosis usually involves two to six elements and in many cases, also includes the last cervical vertebra. Fusion can occur in different degrees, uniting the vertebral centra, the neural spines, the transverse processes, the ventral processes, or a combination of these sites. A detailed assessment of the fusion process of pterosaur dorsal vertebrae is still lacking. Here we identify the fusion sequence of pterosaur notarial elements, demonstrating the order of ossification in vertebral bodies and neural spines based on fossils and extant birds. In both Pterosauria and Aves, the notarium generally develops in a antero-posterior direction, but the actual order of each fusion locus may present slight variations. Based on our data, we were able to identify seven developmental stages in the notarium formation, with broad implications for the prediction of ontogenetic stages for the Pterosauria. In addition, we report the occurrence of a notarium in Ardeadactylus longicollum (Kimmeridgian, Southern Germany), the oldest occurrence of this structure in pterosaurs.     

Vertebral pattern variation in the North Sea harbor porpoise (Phocoena phocoena) by computed tomography

Vertebral series in the harbor porpoise (Phocoena phocoena) include cervical, thoracic, lumbar, and caudal. In contrast to studying skeletons from museums, in which small bones can be missed, evaluation of full body computed tomography (CT) scans provides an overview of the vertebral column, while maintaining interrelationship of all structures. The aim of this study was to document variations in vertebral patterning of the harbor porpoise via evaluation of CT images of intact stranded harbor porpoises. The harbor porpoises were divided into age classes, based on developmental stage of reproductive organs on postmortem examination and closure of proximal humeral physis on CT. Numbers of vertebrae per series, fusion state of the syncervical, type of first hemal arch, number of double articulating ribs, and floating ribs were recorded based on CT images. Included in the study were 48 harbor porpoises (27 males and 21 females), which were divided in two age classes (27 immatures and 21 adults). Total vertebral count varied from 63 to 68 with vertebral formula range C7T12-14L12-16Cd29-33. Twenty-five different vertebral formulas were found, of which C7T13L14Ca30 was the most common (n = 8, 17%). Thoracic vertebrae with six, seven, or eight double articulating ribs and zero, one, or two vertebrae with floating ribs were seen. Four different fusion states of the syncervical and four types of hemal arches were recognized. This study showed a great variation in vertebral patterning in the harbor porpoise, with homeotic and meristic variation in the thoracic, lumbar, and caudal vertebral series.     

Radiographic and Magnetic Resonance Imaging Identification of Thoracolumbar Spine Variants with Implications for the Positioning of the Conus Medullaris in Rhesus Macaques

The anatomy of the vertebral column in mammals may differ between species and between subjects of the same species, especially with regards to the composition of the thoracolumbar spine. We investigated, using several noninvasive imaging techniques, the thoracolumbar spine of a total of 44 adult rhesus macaques of both genders. Radiographic examination of the vertebral column showed a predominant spine phenotype with 12 rib‐bearing thoracic vertebrae and 7 lumbar vertebrae without ribs in 82% of subjects, whereas a subset of subjects demonstrated 13 rib‐bearing thoracic vertebrae and 6 lumbar vertebrae without ribs. Computer tomography studies of the thoraco‐lumbar spine in two cases with a pair of supernumerary ribs showed facet joints between the most caudal pair of ribs and the associated vertebra, supporting a thoracic phenotype. Magnetic resonance imaging (MRI) studies were used to determine the relationship between the lumbosacral spinal cord and the vertebral column. The length of the conus medullaris portion of the spinal cord was 1.5 ± 0.3 vertebral units, and its rostral and caudal positions in the spinal canal were at 2.0 ± 0.3 and 3.6 ± 0.4 vertebral units below the thoracolumbar junction, respectively (n = 44). The presence of a set of supernumerary ribs did not affect the length or craniocaudal position of the conus medullaris, and subjects with13 rib‐bearing vertebrae may from a functional or spine surgical perspective be considered as exhibiting12 thoracic vertebrae and an L1 vertebra with ribs. Anat Rec, 300:300–308, 2017. © 2016 Wiley Periodicals, Inc.     

The locomotor system of the ocean sunfish Mola mola (L.): role of gelatinous exoskeleton,horizontal septum,muscles and tendons

Adult ocean sunfish are the heaviest living teleosts. They have no axial musculature or caudal fin. Propulsion is by unpaired dorsal and anal fins; a pseudocaudal fin (‘clavus’) acts as a rudder. Despite common perception, young sunfish are active predators that swim quickly, beating their vertical fins in unison to generate lift‐based propulsion and attain cruising speeds similar to salmon and marlin. Here we show that the thick subcutaneous layer (or ‘capsule’), already known to provide positive buoyancy, is also crucial to locomotion. It provides two compartments, one for dorsal fin musculature and one for anal fin muscles, separated by a thick, fibrous, elastic horizontal septum that is bound to the capsule itself, the roof of the skull and the dorsal surface of the short vertebral column. The compartments are braced sagittally by bony haemal and neural spines. Both fins are powered by white muscles distributed laterally and red muscles located medially. The anal fin muscles are mostly aligned dorso‐ventrally and have origins on the septum and haemal spines. Dorsal fin muscles vary in orientation; many have origins on the capsule above the skull and run near‐horizontally and some bipennate muscles have origins on both capsule and septum. Such bipennate muscle arrangements have not been described previously in fishes. Fin muscles have hinged tendons that pass through capsular channels and radial cartilages to insertions on fin rays. The capsule is gelatinous (89.8% water) with a collagen and elastin meshwork. Greasy in texture, calculations indicate capsular buoyancy is partly provided by lipid. Capsule, septum and tendons provide elastic structures likely to enhance muscle action and support fast cruising.     

Characteristic intraepidermal nerve fibre endings of the intervibrissal fur in the mystacial pad of the rat: morphological details revealed by intravital methylene blue staining and the zinc iodide-osmium tetroxide technique

The gross anatomical features of human cervical vertebrae during the fetal-neonatal period were investigated in order to develop morphological standards for the individual ossification centres for use in forensic and anthropological osteology. It was found that the morphology of the cervical vertebral arches and the centra cannot be used for the determination of fetal age although the dens of the axis displays some developmental differences which may be useful for the determination of fetal maturity.     

The cat vertebral column: stance configuration and range of motion

This study examined the configuration of the vertebral column of the cat during independent stance and in various flexed positions. The range of motion in the sagittal plane is similar across most thoracic and lumbar joints, with the exception of a lesser range at the transition region from thoracic-type to lumbar-type vertebrae. The upper thoracic column exhibits most of its range in dorsiflexion and the lower thoracic and lumbar in ventroflexion. Lateral flexion is limited to less than 5° at all segments. The range in torsion is almost 180° and occurs primarily in the midthoracic region, T4-T11. Contrary to the depiction in most atlases, the standing cat exhibits several curvatures, including a mild dorsiflexion in the lower lumbar segments, a marked ventroflexion in the lower thoracic and upper lumbar segments, and a profound dorsiflexion in the upper thoracic (above T9) and cervical segments. The curvatures are not significantly changed by altering stance distance but are affected by head posture. During stance, the top of the scapula lies well above the spines of the thoracic vertebrae, and the glenohumeral joint is just below the bodies of vertebrae T3-T5. Using a simple static model of the vertebral column in the sagittal plane, it was estimated that the bending moment due to gravity is bimodal with a dorsiflexion moment in the lower thoracic and lumbar region and a ventroflexion moment in the upper thoracic and cervical region. Given the bending moments and the position of the scapula during stance, it is proposed that two groups of scapular muscles provide the major antigravity support for the head and anterior trunk. Levator scapulae and serratus ventralis form the lateral group, inserting on the lateral processes of cervical vertebrae and on the ribs. The major and minor rhomboids form the medial group, inserting on the spinous tips of vertebrae from C4 to T4. It is also proposed that the hypaxial muscles, psoas major, minor, and quadratus lumborum could support the lumbar trunk during stance. Received: 2 January 1997 / Accepted: 23 September 1997     

Vertebral microanatomy in squamates: structure, growth and ecological correlates

The histological study of vertebrae in extant squamates shows that the internal vertebral structure in this group differs from that of other tetrapods. Squamate vertebrae are lightly built and basically composed of two roughly concentric osseous tubes--one surrounding the neural canal and the other constituting the peripheral cortex of the vertebra--connected by few thin trabeculae. This structure, which characteristically evokes that of a tubular bone, results from a peculiar remodelling process characterised by an imbalance between local bone resorption and redeposition; in both periosteal and endosteo-endochondral territories, bone is extensively resorbed but not reconstructed in the same proportion by secondary deposits. This process is particularly intense in the deep region of the centrum, where originally compact cortices are made cancellous, and where the endochondral spongiosa is very loose. This remodelling process starts at an early stage of development and remains active throughout subsequent growth. The growth of squamate centra is also strongly asymmetrical, with the posterior (condylar) part growing much faster than the anterior (cotylar) part. Preliminary analyses testing for associations between vertebral structure and habitat use suggest that vertebrae of fossorial taxa are denser than those of terrestrial taxa, those in aquatic taxa being of intermediate density. However, phylogenetically informed analyses do not corroborate these findings, thus suggesting a strong phylogenetic signal in the data. As our analyses demonstrate that vertebrae in snakes are generally denser than those of lizards sensu stricto, this may drive the presence of a phylogenetic signal in the data. More comprehensive sampling of fossorial and aquatic lizards is clearly needed to more rigorously evaluate these patterns.