Morphogenesis of the cranium of Cavia porcellus L. I: Introduction, classification and descriptive part

The craniogenesis of Cavia porcellus has been investigated in 7 embryos of different ages. From the developmental stage of 36 mm CRL, a reconstruction of the chondrocranium is described. As there is still a gap in the tectum posterius, the foramen magnum is not closed posteriorly. The course of the notochord is retrobasilar at the beginning, more rostrally it runs intrabasilar. After ossification, the place where the notochord enters the basioccipital is marked by a cavity. This cavity is not identical with the posterior basicranial fenestra. The laminae alares build up strong paracondylar processes. The auditory capsule is connected with the occipital region only by the exoccipitocapsular commissure, but there is no supraoccipitocapsular commissure. The fossa subarcuata is pierced by a subarcuate foramen. The very short lamina parietalis is not in contact with the orbital wing as there is no orbitoparietal commissure. The processus recessus divides the perilymphatic foramen into fenestra rotunda and aquaeductus cochleae. The suprafacial commissure arises from the upper margin of the canalicular part of the auditory capsule, but it does not reach the superior surface of the cochlear part at this stage. The tegmen tympani is well developed. The foramen singulare is not yet separated from the inferior acoustic foramen. At the stage of 36 mm CRL there is no septum spirale cartilagineum. Mm. tensor tympani et stapedius are developed in the typical way. The auditory capsule is connected with the basal plate by the anterior basicochlear and the alicochlear commissures. The floor of the orbitotemporal region is incomplete, the temporal wings are small. The alicochlear commissure, the alar process, the anterior basicochlear commissure, and the basal plate surround the carotid foramen, but there is no blood vessel passing through it. The temporal wing is at the beginning of ossification and shows a fissura ovalis for the mandibular nerve. Although the hypophysial canal is still present, there are no structures passing through it. There is no foramen rotundum. The orbital wing is still cartilagineous. The basal plate and the pre- and postoptic roots border the optical foramen. The straight muscles of the eyeball are attached to the ala hypochiasmatica which projects from the postoptic root. The interorbital septum is absent. The ophthalmic artery, which instead of the obliterated internal carotid artery, contributes to the circulus arteriosus cerebri is well developed. There is no orbitonasal commissure . The epiphanial foramina are present.(ABSTRACT TRUNCATED AT 400 WORDS)     

The development of the chondrocranium of the lacertid lizard,Acanthodactylus boskiana

The trabeculae cranii are at first quite separate from each other, after few days their anterior two fifths are connected by a trabecular plate which is obliterated throughout development. The paired origin of the parachordal plate is not observed. The fused posterior orbital cartilages chondrify in the form of a wide short plate, traversed by the oculomotor and trochlear nerves. The basicranial fenestra and fenestra ovalis are formed by the degeneration of pre-existing cartilage. The cochlear portion is completely fused with the parachordal plate from the very beginning. The elements of the pterygoquadrate are fused together. The quadrate and Meckel's cartilage are in close contact from the very beginning. While the lower part of the interorbital septum is derived from the trabecula communis, its upper part is derived from the anterior orbital cartilages. The lateral parts of the fused posterior orbital cartilages give rise to most of the taeniae and pilae of the orbitotemporal region. There is only one commissure between the auditory capsule and parachordal plate. A cartilaginous connection between the distal portion of the columella auris and ceratohyal persists for some time. The parietotectal and paranasal cartilages are fused together from the very beginning. The processus paroticus originates from the columella auris. In the fully formed stage the notochord is completely embedded in the occipital condyle. The union between the condyle and odontoid process persists. The auditory capsules and occipital arches contribute to the formation of the tectum synoticum plus posterius. The prefacial commissure and facial foramen lie in front of the cochlear portion. The columella auris possesses a processus internus (connected with the quadrate), but the processes a dorsalis has completely disappeared. The orbitotemporal region is quite complete. A medial fenestra is formed in the planum supraseptale. A fenestra is observed in each of the interorbital and nasal septa. The lamina transversalis anterior is fused with the parietotectal cartilage. A complete zona annularis is present. The outer wall of the paranasal cartilage is perforated by a large fenestra lateralis. The parietotectal and paranasal cartilages and the posterior process of the lamina transversalis anterior contribute to the formation of the concha nasalis. There is a contact between the planum antorbitale and nasal septum. The pterygoid process has disappeared. The common characters of the lacertid chondrocranuium are deduced.     

The Evolutionary Origin and Homologues of the Supracochlear Lamina: a Contribution to our Knowledge of Mammalian Ancestry

In cetaceans, each otic capsule is bound anteriorly to the remainder of the endocranium by an aliform structure called the supracochlear lamina. This lamina has been established here as the homologue of the sphenocochlear commissure of other mammals. Most researchers believe that these two structures arose within mammals. However, a comparative study involving data from both extant and extinct craniates suggests that the supracochlear lamina and the sphenocochlear commissure have a long premammalian history. The conclusion is that the lower of the two pharyngeal segments at the upper end of the mandibular branchial arch first became incorporated in the endocranium, constituting the cartilago trabecularis in the embryos of jawed craniates. The distal, or posterior, extremity of the trabecular cartilage projected outwardly to form the basitrabecular process. This process, which when ossified is called the processus basipterygoideus, functioned as a jaw support. Later, one more jaw support, termed the basivincular, evolved immediately in front of the basipterygoid process. Both these supports for the upper jaw existed in the piscine forerunners of the tetrapods. Subsequently, in the lineages leading to mammals, the basivincular jaw support became the processus alaris to which is attached an upper jaw endoskeletal remnant, called the ala temporalis. The basipterygoid jaw support, however, vanished as a consequence of the evolution of an exoskeletal joint system for the jaws of mammals. Yet the basipterygoid process persisted and as the sphenocochlear commissure or the supracochlear lamina assumed the new function of supporting the cochlear part of the auditory capsule.     

A detailed redescription of the mesoderm/neural crest cell boundary in the murine orbitotemporal region integrates the mammalian cranium into a pan-amniote cranial configuration

The morphology of the mammalian chondrocranium appears to differ significantly from those of other amniotes, since the former possesses uniquely developed brain and cranial sensory organs. In particular, a question has long remained unanswered as to the developmental and evolutionary origins of a cartilaginous nodule called the ala hypochiasmatica. In this study, we investigated the embryonic origin of skeletal elements in the murine orbitotemporal region by combining genetic cell lineage analysis with detailed morphological observation. Our results showed that the mesodermal embryonic environment including the ala hypochiasmatica, which appeared as an isolated mesodermal distribution in the neural crest-derived prechordal region, is formed as a part of the mesoderm that continued from the chordal region during early chondrocranial development. The mesoderm/neural crest cell boundary in the head mesenchyme is modified through development, resulting in the secondary mesodermal expansion to invade into the prechordal region. We thus revealed that the ala hypochiasmatica develops as the frontier of the mesodermal sheet stretched along the cephalic flexure. These results suggest that the mammalian ala hypochiasmatica has evolved from a part of the mesodermal primary cranial wall in ancestral amniotes. In addition, the endoskeletal elements in the orbitotemporal region, such as the orbital cartilage, suprapterygoid articulation of the palatoquadrate, and trabecula, some of which were once believed to represent primitive traits of amniotes and to be lost in the mammalian lineage, have been confirmed to exist in the mammalian cranium. Consequently, the mammalian chondrocranium can now be explained in relation to the pan-amniote cranial configuration.     

Individual anatomical variability of the head of the caudate nucleus and of the putamen in man

Individual variabilities in form, size and position of the nucleus caudatus head and the putamen have been studied in the horizontal section cutting across the inferior edge of the interventricular foramen (Monro) and the posterior commissure of the cerebrum in 70 mature persons died from various diseases not connected with disorders in the brain. Variability in length, width and position of these strial structures have been estimated taking into account the size of the intercommissural lines. The investigation has demonstrated that with an increasing distance between the anterior and posterior commissures of the cerebrum, the length and width of the nucleus caudatus head and those of the putamen increase; these nuclei are observed to be pushed off the median line and approach towards the level of the anterior cerebral commissure.     

Interhemispheric connections through the pallial commissures in the brain of Podarcis hispanica and Gallotia stehlinii (Reptilia,Lacertidae)

The cells-of-origin and the mode and site of termination of the interhemispheric connections passing through the anterior and posterior pallial commissures in the telencephalon of two lizards (Podarcis hispanica and Gallotia stehlinii) were investigated by studying the anterograde and retrograde transport of unilaterally injected horseradish peroxidase. The commissural projections arise mainly from pyramidal cells in the medial, dorsomedial, and dorsal cortices (medial subfield). Additionally some non-pyramidal neurons in the medial and dorsal cortices contribute to the commissural system. Medial cortex neurons project to the contralateral anterior septum through the anterior pallial commissure. The dorsomedial cortex projects contralaterally via the anterior pallial commissure to the dorsolateral septum and to the medial, dorsomedial, and dorsal cortices. The projection to the medial cortex terminates in two bands at the inner and outer border, respectively, of the cell layer; the projection to the dorsomedial and dorsal cortex ends in a zone in layer 1 which previously has been described to be Timm-negative, and in a diffuse band in the inner half of layer 3. The medial subfield of the dorsal cortex projects through the anterior pallial commissure to the dorsomedial and dorsal cortices with a similar pattern of termination to that found for the dorsomedial cortex. The posterior pallial commissure contains only the projections from the ventral cortex to its contralateral counterpart and to the ventral part of the caudal medial cortex. The similarities found between this commissural system and the mammalian hippocampal interhemispheric connections are discussed.     

On the origin of the so-called Meckelian ossicles in the nasal skull of odontocetes

Although Cave (1987) accepts the theory that the Meckelian ossicles originate from the maxilloturbinals, evidence given in his study in fact supports the opinion of Klima and van Bree (1985) that the Meckelian ossicles arise from elements of the nasal floor, solum nasi, of the embryonic nasal capsule, in particular from the lamina transversalis anterior and the cartilago paraseptalis.     

Anuran postnasal wall homology: An experimental extirpation study

The nasal placode was extirpated unilaterally in Gosner stage 18–20 embryos of Rana sylvatica, R. palustris and R. pipiens, in order to test alternative proposed schemes of homology for the ethmoidal attachment of the palatoquadrate in anurans and urodeles. Absence of the nasal sac has no pronounced effect on the formation of larval chondrocranial structures. In contrast, in metamorphosed animals the lamina orbitonasalis and inferior prenasal process are the only nasal capsule structures present on the operated side. The medial nasal branch of the deep ophthalmic nerve passes forward over the dorsal surface of the lamina orbitonasalis, rather than through an orbitonasal foramen. Comparison with previous experimental work on urodeles supports the traditional homology of the anuran lamina orbitonasalis with the antorbital process of urodeles and other vertebrates. J. Morphol. 238:343–353, 1998. © 1998 Wiley-Liss, Inc.     

Age-Related Changes of Elements in the Anterior Commissures and the Relationships Among their Elements

To elucidate compositional changes of the anterior commissure with aging, the authors investigated age-related changes of elements in the anterior commissures and the relationships among their elements. After ordinary dissection at Nara Medical University was finished, the anterior commissures were resected from 45 subjects, ranging in age from 70 to 101 years. The subjects consisted of 22 men and 23 women. After ashing with nitric acid and perchloric acid, the element content of the anterior commissures was determined by inductively coupled plasma-atomic emission spectrometry. The seven element contents of Ca, P, S, Mg, Zn, Fe, and Na did not change significantly in the anterior commissures with aging. Regarding the relationships among their element contents, significant correlations were found among the contents of Ca, Mg, Zn, and Na in the anterior commissures. The gender difference that the Zn content was significantly higher in men than in women was found in the anterior commissure.     

Development of midline cell types and commissural axon tracts requires Fgfr1 in the cerebrum

The adult cerebral hemispheres are connected to each other by specialized midline cell types and by three axonal tracts: the corpus callosum, the hippocampal commissure, and the anterior commissure. Many steps are required for these tracts to form, including early patterning and later axon pathfinding steps. Here, the requirement for FGF signaling in forming midline cell types and commissural axon tracts of the cerebral hemispheres is examined. Fgfr1, but not Fgfr3, is found to be essential for establishing all three commissural tracts. In an Fgfr1 mutant, commissural neurons are present and initially project their axons, but these fail to cross the midline that separates the hemispheres. Moreover, midline patterning defects are observed in the mutant. These defects include the loss of the septum and three specialized glial cell types, the indusium griseum glia, midline zipper glia, and glial wedge. Our findings demonstrate that FGF signaling is required for generating telencephalic midline structures, in particular septal and glial cell types and all three cerebral commissures. In addition, analysis of the Fgfr1 heterozygous mutant, in which midline patterning is normal but commissural defects still occur, suggests that at least two distinct FGF-dependent mechanisms underlie the formation of the cerebral commissures.     

Ontogeny of the partial secondary wall of the otoccipital region of the endocranium in prehatching Alligator mississippiensis (Archosauria, Crocodylia)

The ontogeny of the posterior otic and anterior occipital portions of the neural endocranium of prehatching Alligator mississippiensis was investigated by reconstruction from sectioned material. In Stage 6 of this species, in which the endochondral ossification of the otoccipital region of the neural endocranium is only in its very early stage, two bony outgrowths-laminae-are present at the external wall of the posterior portion of the neural endocranium. The anterior lamina arises from the external surface of the basal plate at the level of the posterior margin of the subcapsular process; the posterior lamina arises from the external surface of that portion of the pila occipitalis that forms the posteroventral wall of the metotic fissure. During ontogeny, both laminae lying in the anteroposterior sequence ossify in membrane, fuse together, grow laterodorsally, and fuse with the lateral wall of the lateral semicircular canal and the crista parotica. This lamina forms a new, secondary wall enclosing the posterior section of the otic capsule and contains the large external jugular foramen (or foramen vagi) in its basal portion. The laminae, designated lamina juxtaotica anterior and posterior (lamina juxtaotica when fused together), have not been recorded previously in crocodylians and are absent in all other Recent reptiles. From the functional point of view, the juxtaotic lamina 1) forms the margins of the external jugular foramen, and 2) forms the floor of the posterior section of the Eustachian tube. In birds, the structure called the metotic cartilage, which arises in ontogeny as an independent element, has a similar position as the juxtaotic lamina. However, the two structures differ in their developmental origins and their relation to the Eustachian tube and the ramus hyomandibularis of the facialis nerve. Moreover, there is no external jugular foramen in birds.     

A mode of arthropod brain evolution suggested by Drosophila commissure development

The evolutionary origin of the tritocerebral neuromere, which is a brain segment located at the junction between the supra- and subesophageal ganglia in most mandibulates (arthropods such as crustaceans and insects), is a subject rich in contentious debate. Various models have argued that the tritocerebrum came from a segmental nerve cord ganglia that was recruited into the head during the course of arthropod evolution. However, despite much thought on the subject, the origin of the tritocerebrum remains obscure. Here I describe the development of the tritocerebral commissure in Drosophila and demonstrate that the tritocerebral and mandibular commissures actually form as one commissure and then separate in a manner very similar to how the anterior and posterior commissures of a ventral nerve cord neuromere form. I propose that the tritocerebral neuromere originated from the splitting of an ancestral neuromere located in the anterior subesophageal ganglion into distinct tritocerebral and mandibular neuromeres. Also, I discuss the problem of arthropod brain neuromere homology in reference to this hypothesis.     

The midline glial cells are required for regionalization of commissural axons in the embryonic CNS of Drosophila

 The ventral nerve cord of arthropods is characterised by the organisation of major axon tracts in a ladder-like pattern. The individual neuromeres are connected by longitudinal connectives whereas the contra-lateral connections are brought about through segmental commissures. In each neuromere of the embryonic central nervous system (CNS) of Drosophila an anterior and a posterior commissure is found. The development of these commissures requires a set of neurone-glia interactions at the midline. Here we show that both the anterior as well as the posterior commissures are subdivided into three axon-containing regions. Electron microscopy of the ventral nerve cord of mutations affecting CNS midline cells indicates that the midline glial cells are required for this subdivision. In addition the midline glial cells appear required for a crossing of commissural growth cones perpendicular to the longitudinal tracts, since in mutants with defective midline glial cells commissural axons frequently cross the midline at aberrant angles. Received: 6 July 1997 / Accepted: 27 August 1997     

Commissure formation in the embryonic insect brain

The primary axon scaffold of the insect brain is established early in embryogenesis and comprises a preoral protocerebral commissure, a postoral tritocerebral commissure and longitudinal fiber pathways linking the two. In both grasshopper and fly its form is approximately orthogonal and is centered around the stomodeum. We show how pioneer fibers from the protocerebrum and tritocerebrum cross the brain midline directly via their respective commissures. The deutocerebrum, however, lacks its own commissure and we describe how deutocerebral pioneers circumnavigate the gut to cross the midline either via the protocerebral commissure or the tritocerebral commissure. In contrast to all other commissures of the central nervous system, the protocerebral commissure persists, albeit in reduced form, in the commissureless mutation in the fly. Besides the com gene, a further, as yet unidentified, mechanism must regulate this commissure. The formation of the tritocerebral commissure involves labial, a member of the Hox gene group. Genetic rescue experiments in labial mutants reveal that the formation of this commissure can be rescued by all other Hox genes except Abdominal-B. However, only in the labial and Deformed null mutants are the commissures associated with the respective expression domains (tritocerebral, mandibular, respectively) absent. This suggests that the molecular mechanisms regulating postoral brain commissure formation are distinct from those in the neuromeres of the ventral nerve cord.     

Age at maturity in cavies and guinea-pigs (Cavia aperea and Cavia aperea f. porcellus): influence of social factors

Age at maturity, a particularly important parameter in the life history of small mammals, contributes greatly to fitness. Social influences on age at maturity have been demonstrated for altricial rodents, in particular, mice. Nothing is known about such effects in precocial small mammals. Wild cavies Cavia aperea are born in a highly precocial state and mature early in life, briefly after weaning. We investigated whether the wild cavy C. aperea and the domestic guinea-pig Cavia aperea f. porcellus reach maturity earlier in the presence of adults of the opposite sex. Juvenile females kept in pairs without males showed first vaginal opening (=oestrus) when 59 days old in cavies and at about 40 days in the guinea-pig. However, in the company of adult males, cavy females kept in pairs reached maturity when about 30 days old, and guinea-pig females when 26 days old. Most cavy females experienced successful pregnancy following first vaginal opening. In cavies, female mass at birth and at first oestrus was not correlated with age at first oestrus. In guinea-pigs, birth mass predicted age at maturity only when a male was present. The growth rate from birth to first oestrus related to age at first oestrus. In the wild cavy, the presence of a male appeared to influence maturation more between days 25 and 30 than earlier in life. Male C. aperea matured and had fully descended testes when about 65–70 days old. All male cavies produced abundant motile sperm from day 75. First successful copulations occurred at about the same age. Surprisingly, the priming effect of the presence of an adult male on female maturation proved stronger in these highly precocial caviomorphs than in altricial rodents investigated so far.     

On the separation of functions mediated by the AV3V region

Knife-cuts were used to separate the disruptive effects on fluid balance that are produced by electrolytic lesions of the anteroventral third ventricle (AV3V) region. It was observed that vertical cuts of the dorsal stalk of the subfornical organ (SFO) produced none of these effects. Horizontal cuts between the SFO and the anterior commissure produced neither of the acute effects of AV3V lesions (adipsia and diuretic weight loss) but they did mimic AV3V lesions in disrupting drinking responses to peripherally injected angiotensin and hypertonic saline. In contrast, horizontal cuts between the anterior commissure and the organum vasculosum of the lamina terminalis (OVLT) did not reduce drinking responses to angiotensin but they did cause a large weight loss during the 24 hours following surgery. It is suggested that these ventral cuts severed neural connections between the medial septum and the ventral medial preoptic area in producing the large weight loss. Together with findings from other experiments, these findings support the hypothesis that distinct neural elements mediate the various functions that are disrupted by lesions of the AV3V region.     

Fascicle switching generates a chiasmal neuroarchitecture in the embryonic central body of the grasshopper Schistocerca gregaria

The central body is a prominent neuropilar structure in the midbrain of the grasshopper and is characterized by a fan-shaped array of fiber columns, which are part of a chiasmal system linking anterior and posterior commissures. These columns are established during embryogenesis and comprise axons from cell clusters in the pars intercerebralis, which project to the central body via the so-called w, x, y, z tracts. Up to mid-embryogenesis the primary axon scaffold in both the brain and ventral nerve cord comprises a simple orthogonal arrangement of commissural and longitudinal fiber pathways. No chiasmata are present and this pattern is maintained during subsequent development of the ventral nerve cord. In the midbrain, individual axons entering the commissural system from each of the w, x, y, z tracts after mid-embryogenesis (55%) are seen to systematically de-fasciculate from an anterior commissure and re-fasciculate with another more posterior commissure en route across the midline, a feature we call "fascicle switching". Since the w, x, y, z tracts are bilaterally symmetrical, fascicle switching generates chiasmata at stereotypic locations across the midbrain. Choice points for leaving and entering fascicles mark the anterior and posterior positions of each future column. As the midbrain neuropil expands, the anterior and posterior groups of commissures condense, so that the chiasmata spanning the widening gap between them become progressively more orthogonally oriented. A columnar neuroarchitecture resembling that of the adult central body is already apparent at 70% of embryogenesis.     

The development of the septum primum relative to atrial septation in the mouse heart

The septum primum in the mouse originates as a thickened primordium with a straight rather than a sickle-shaped ventral border. It is covered on its ventral border by anterior cushion material which is continuous over the roof of the atrium with the principal anterior cushion mass. A process of cavitation thins the septum primum and precedes actual fenestration. This process shifts the membranous septum to the left thereby providing room for the septum secundum to overlap on the right side. The septum primum cannot contact the posterior cushion until closure of the sinus venosus gutter which is described. The closure of the interatrial foramen, later the foramen primum, is accomplished by cell growth of the anterior cushion material. The ventral thick border of the septum primum contributes to the ventral limbus and the caudal thickened boundary of the fossa ovalis with some contribution from the left venous valve. These boundaries as well as the membranous portion of the interatrial septum are derived from the same primordium, namely the septum primum.     

Early development of chondrocranium in the tailed frog Ascaphus truei (Amphibia: Anura): Implications for anuran palatoquadrate homologies

Chondrocranial development in Ascaphus truei was studied by serial sectioning and graphical reconstruction. Nine stages (21–29; 9–18 mm TL) were examined. Mesodermal cells were distinguished from ectomesenchymal (neural crest derived) cells by retained yolk granules. Ectomesenchymal parts of the chondrocranium include the suprarostrals, pila preoptica, anterior trabecula, and palatoquadrate. Mesodermal parts of the chondrocranium include the orbital cartilage, posterior trabecula, parachordal, basiotic lamina, and otic capsule. Development of the palatoquadrate is as follows. The pterygoid process first connects with the trabecula far rostrally; their fusion progresses caudally. The ascending process connects with a mesodermal bar that extends from the orbital cartilage to the otic capsule, and forms the ventral border of the dorsal trigeminal outlet. This bar is the “ascending process” of Ascaphus adults; it is a neurocranial, not palatoquadrate structure. The basal process chondrifies in an ectomesenchymal strand running from the quadrate keel to the postpalatine commissure. Later, the postpalatine commissure and basal process extend anteromedially to contact the floor of the anterior cupula of the otic capsule, creating separate foramina for the palatine and hyomandibular branches of the facial nerve. Based on these data, and on comparison with other frogs and salamanders, the anuran anterior quadratocranial commissure is homologized with the pterygoid process of salamanders, the anuran basal process (=“pseudobasal” or “hyobasal” process) with the basal process of salamanders, and the anuran otic ledge with the basitrabecular process of salamanders. The extensive similarities in palatoquadrate structure and development between frogs and salamanders, and lacking in caecilians, are not phylogenetically informative. Available information on fossil outgroups suggests that some of these similarities are primitive for Lissamphibia, whereas for others the polarity is uncertain. J. Morphol. 231:63-100, 1997. © 1997 Wiley-Liss, Inc.