Contributions of placodal and neural crest cells to avian cranial peripheral ganglia

The method of embryonic tissue transplantation was used to confirm the dual origin of avian cranial sensory ganglia, to map precise locations of the anlagen of these sensory neurons, and to identify placodal and neural crest-derived neurons within ganglia. Segments of neural crest or strips of presumptive placodal ectoderm were excised from chick embryos and replaced with homologous tissues from quail embryos, whose cells contain a heterochromatin marker. Placode-derived neurons associated with cranial nerves V, VII, IX, and X are located distal to crest-derived neurons. The generally larger, embryonic placodal neurons are found in the distal portions of both lobes of the trigeminal ganglion, and in the geniculate, petrosal and nodose ganglia. Crest-derived neurons are found in the proximal trigeminal ganglion and in the combined proximal ganglion of cranial nerves IX and X. Neurons in the vestibular and acoustic ganglia of cranial nerve VIII derive from placodal ectoderm with the exception of a few neural crest-derived neurons localized to regions within the vestibular ganglion. Schwann sheath cells and satellite cells associated with all these ganglia originate from neural crest. The ganglionic anlagen are arranged in cranial to caudal sequence from the level of the mesencephalon through the third somite. Presumptive placodal ectoderm for the VIIIth, the Vth, and the VIIth, IXth, and Xth ganglia are located in a medial to lateral fashion during early stages of development reflecting, respectively, the dorsolateral, intermediate, and epibranchial positions of these neurogenic placodes.     

A fate-map for cranial sensory ganglia in the sea lamprey

Cranial neurogenic placodes and the neural crest make essential contributions to key adult characteristics of all vertebrates, including the paired peripheral sense organs and craniofacial skeleton. Neurogenic placode development has been extensively characterized in representative jawed vertebrates (gnathostomes) but not in jawless fishes (agnathans). Here, we use in vivo lineage tracing with DiI, together with neuronal differentiation markers, to establish the first detailed fate-map for placode-derived sensory neurons in a jawless fish, the sea lamprey Petromyzon marinus, and to confirm that neural crest cells in the lamprey contribute to the cranial sensory ganglia. We also show that a pan-Pax3/7 antibody labels ophthalmic trigeminal (opV, profundal) placode-derived but not maxillomandibular trigeminal (mmV) placode-derived neurons, mirroring the expression of gnathostome Pax3 and suggesting that Pax3 (and its single Pax3/7 lamprey ortholog) is a pan-vertebrate marker for opV placode-derived neurons. Unexpectedly, however, our data reveal that mmV neuron precursors are located in two separate domains at neurula stages, with opV neuron precursors sandwiched between them. The different branches of the mmV nerve are not comparable between lampreys and gnatho-stomes, and spatial segregation of mmV neuron precursor territories may be a derived feature of lampreys. Nevertheless, maxillary and mandibular neurons are spatially segregated within gnathostome mmV ganglia, suggesting that a more detailed investigation of gnathostome mmV placode development would be worthwhile. Overall, however, our results highlight the conservation of cranial peripheral sensory nervous system development across vertebrates, yielding insight into ancestral vertebrate traits.     

The early development of cranial sensory ganglia and the potentialities of their component cells studied in quail-chick chimeras

The quail-chick marker system has been used to study the early developmental stages of the ganglia located along cranial nerves VII, IX, and X. The streams of neural crest cells arising from the rhombencephalic-vagal neural crest were followed from the onset of their migration up to the localization of crest cells in the trunk and root ganglia of these nerves. It was shown that two different populations of crest cells are segregated early as a result of morphogenetic movements in the hypobranchial region. The dorsal population gives rise to the root ganglia of nerves IX and X located close to the encephalic vesicles, where the crest cells differentiate both into neurons and into glia. In contrast, the ventral stream of neural crest cells contributes together with cells from epibranchial placodes to the trunk ganglia (geniculate, petrous, and nodose ganglia) of cranial nerves VII, IX, and X. The successive steps of the invasion of the placodal anlage by crest cells can be followed owing to the selective labeling of the neural crest cells. It appears that the latter give rise to the satellite cells of the geniculate, petrous, and nodose ganglia while the large sensory neurons originate from the placodes. The nodose ganglion has been the subject of further studies aimed to investigate whether neuronal potentialities can be elicited in the neural crest-derived cells that it contains. The ability to label selectively either the neurons or the glia by the quail nuclear marker made this investigation possible in the particular case of the nodose ganglion whose neurons and satellite cells have a different embryonic origin. By the technique already described (N. M. Le Douarin, M. A. Teillet, C. Ziller, and J. Smith, 1978, Proc. Nat. Acad. Sci. USA75, 2030–2034) of back-transplantation into the neural crest migration pathway of a younger host, it was shown that the presumptive glial cells of the nodose ganglion are able to remigrate when transplanted into a 2-day chick host and to differentiate into autonomic structures (sympathetic ganglion cells, adrenomedullary cells, and enteric ganglia). It is proposed as a working hypothesis that neuronal potentialities contained in the neural crest cells which invade the placodal primordium of the nodose ganglion are repressed through cell-cell interactions occurring between placodal and crest cells.     

A comparative analysis of internal cranial anatomy in the hylobatidae

Craniometric studies on the hylobatids using external metrics (Creel and Preuschoft, 1976 , 1984 ) sorted hylobatid populations into primary species groupings which are in accordance with the four currently recognized generic‐level groupings. The goal of the current study was to assess the relative orientations of the orbits, palate, and basioccipital clivus among the hylobatid genera in an effort to further clarify whether the lesser apes differ significantly in these internal cranial features and how that variation patterns across the groups. Nine angular variables quantifying orbital, palatal, and basioccipital clivus orientations were measured on lateral view radiographs of adults representing three of the four hylobatid genera: Hylobates; Nomascus; and, Symphalangus. The interspecific adult hylobatid means for the angular variables were analyzed using t‐test contrasts. The total sample was further subjected to discriminant function analysis (DFA) to test for the ability of craniofacial angular variables to distinguish the hylobatid genera from one another. The three hylobatid genera displayed significant morphological differentiation in orbital, palatal, and posterior skull base orientations. Normal, jackknifed, and cross‐validation DFA procedures correctly identified the hylobatids 50–100% of the time. The observed morphological patterns generally mapped onto the findings of earlier external craniometric hylobatid studies and suggest concordance between specific internal and external cranial features. This article is the first comprehensive study of variation in internal cranial anatomy of the Hylobatidae and includes the first published craniofacial angular data for Nomascus. Am J Phys Anthropol 143:250–265, 2010. © 2010 Wiley‐Liss, Inc.     

Development of cranial parasympathetic ganglia requires sequential actions of GDNF and neurturin

The neurotrophic factors that influence the development and function of the parasympathetic branch of the autonomic nervous system are obscure. Recently, neurturin has been found to provide trophic support to neurons of the cranial parasympathetic ganglion. Here we show that GDNF signaling via the RET/GFR(alpha)1 complex is crucial for the development of cranial parasympathetic ganglia including the submandibular, sphenopalatine and otic ganglia. GDNF is required early for proliferation and/or migration of the neuronal precursors for the sphenopalatine and otic ganglia. Neurturin exerts its effect later and is required for further development and maintenance of these neurons. This switch in ligand dependency during development is at least partly governed by the altered expression of GFR(&agr;) receptors, as evidenced by the predominant expression of GFR(&agr;)2 in these neurons after ganglion formation.     

Fluorescence of catecholamines in nerve structures of cranial cervical ganglia transferred to striated muscle

In order to form additional innervation sources of the organs, a possibility to preserve the structure of the cranial cervical node transferred on the musculus sterno-mastoideus has been tried. During this manipulation most of neurocytes die. Along the periphery and on the caudal pole of the node a part of cells remain alive. At first the structure and metabolism of these cells is disturbed. However, beginning from the end of the first month after the transfer, the remained cells and the processes formed by them accumulate catecholamines. By the second--third, and especially by the end of the first month after the transfer, the remained cells and the processes sound. A suggestion is made on a possibility to use these neurocytes for creating additional sources of the organs' innervation.     

Gene expression profiling of cranial sensory ganglia that transmit food intake stimuli

Peripheral cranial sensory nerves projecting into the oral cavity receive food intake stimuli and transmit sensory signals to the central nervous system. They are derived from four cranial sensory ganglia, trigeminal, geniculate, petrosal, and nodose ganglia, each of which contains multiple kinds of sensory neurons with different cell morphologies and neuronal properties. We investigated the complex properties of these neurons from the viewpoint of gene expression using DNA microarrays. The 498 genes were selected from a total of 8,740 genes as showing tissue-dependent expression on the microarray by hierarchical cluster analysis, in which several genes known to be differentially expressed in cranial sensory ganglia are included. This suggests that DNA microarray cluster analysis revealed a number of characteristic genes for sensory neurons in these ganglia. Among the selected 498 genes, 44 genes are associated with neurotransmission, such as neuropeptides, their receptors, and vesicle transport, and 26 are ion channels regulating membrane potentials. The identification of a number of genes related directly to neural properties indicates that these sensory ganglia contain heterogeneous types of neurons with different neural properties.     

A comparative study of leukocyte counts and disease risk in primates

Little is known about how the risk of disease varies across species and its consequences for host defenses, including the immune system. I obtained mean values of basal white blood cells (WBC) from 100 species of primates to quantify disease risk, based on the assumption that higher baseline WBC counts will be found in species that experience greater risk of acquiring infectious disease. These data were used to investigate four hypotheses: disease risk is expected to increase with (1) group size and population density; (2) greater contact with soil-borne pathogens during terrestrial locomotion; (3) a slow life history; and (4) increased mating promiscuity. After controlling for phylogeny, WBC counts increased with female mating promiscuity, as reflected in discrete categories of partner number, relative testes mass, and estrous duration. By comparison, the social, ecological, and life-history hypotheses were unsupported in comparative tests. In terms of confounding variables, some WBC types were associated with body mass or activity period, but these variables could not account for the association with mating promiscuity. Several factors may explain why hypotheses involving social, ecological, and life-history factors went unsupported in these tests, including the role of behavioral counterstrategies to disease, restrictions on female choice of mating partners, and the effect of transmission mode on parasite strategies and host defenses.     

Intranuclear inclusion bodies within neurons of spinal and cranial ganglia in three cyprinid species

Summary A histological examination of 205 fish representing four cyprinid species from a site 2.5 miles north of Wheeling, West Virginia, on the Ohio River revealed large (2–4 m) cuboidal intranuclear inclusion bodies (NIB's) within neurons in the cranial and spinal ganglia of three species. Because the minnows had been caught during a yearly sampling of fish, an additional 63 minnows were taken the following year. Inclusions were again observed. The NIB's stain strongly with phloxine as well as with Mallory and Giemsa stains, appearing bright red or pink. Various histochemical tests indicated that the inclusions contain protein and lipid but no carbohydrates or nucleic acids. No heavy metals were detected by electron probe analysis. At the ultrastructural level the inclusions exhibit subunits resembling hexagons measuring 326–350 nm. Previously suggested causes for such inclusions include effects of viruses, aging, drugs, cellular transformation, and an altered metabolic state of affected cells.     

Neural crest and placode roles in formation and patterning of cranial sensory ganglia in lamprey

Vertebrates possess paired cranial sensory ganglia derived from two embryonic cell populations, neural crest and placodes. Cranial sensory ganglia arose prior to the divergence of jawed and jawless vertebrates, but the developmental mechanisms that facilitated their evolution are unknown. Using gene expression and cell lineage tracing experiments in embryos of the sea lamprey, Petromyzon marinus, we find that in the cranial ganglia we targeted, development consists of placode‐derived neuron clusters in the core of ganglia, with neural crest cells mostly surrounding these neuronal clusters. To dissect functional roles of neural crest and placode cell associations in these developing cranial ganglia, we used CRISPR/Cas9 gene editing experiments to target genes critical for the development of each population. Genetic ablation of SoxE2 and FoxD‐A in neural crest cells resulted in differentiated cranial sensory neurons with abnormal morphologies, whereas deletion of DlxB in cranial placodes resulted in near‐total loss of cranial sensory neurons. Taken together, our cell‐lineage, gene expression, and gene editing results suggest that cranial neural crest cells may not be required for cranial ganglia specification but are essential for shaping the morphology of these sensory structures. We propose that the association of neural crest and placodes in the head of early vertebrates was a key step in the organization of neurons and glia into paired sensory ganglia.     

Embryonic origin of substance P containing neurons in cranial and spinal sensory ganglia of the avian embryo

The ontogeny of the neurons exhibiting substance P-like immunoreactivity (SPLI) was examined in the spinal and cranial sensory ganglia of chick and quail embryos. It was shown that in dorsal root ganglia (DRG) virtually all neuronal somas occupying the mediodorsal (MD) region of the ganglia are SPLI-positive while the larger neurons of the lateroventral (LV) area are SPLI-negative. In the cranial nerve ganglia, both types of neurons coexist in the trigeminal ganglion but with a different distribution: small neurons with SPLI are proximal while large neurons without SPLI occupy the maxillomandibular and ophthalmic lobes. The distal ganglia of nerves VII and IX (i.e., geniculate, petrosal) do not show cell bodies with SPLI in the two species considered. A few of them only (about 12%) are found in the nodose (distal ganglion of nerve X). The proximal ganglia of nerves IX and X (i.e., superior-jugular complex) are composed of small neurons which virtually all exhibit SPLI. Chimaeric cranial sensory ganglia were constructed by grafting the quail hind-brain primordium into chick embryos. Revelation of SPLI was combined with acridine orange staining on the same sections in order to ascertain the placodal (chick host) or neural crest (quail donor) origin of the SP-positive neurons in each type of ganglion. We found that all the neurons showing SPLI are derived from the neural crest in the trigeminal and in the superior and jugular ganglia. In the geniculate, petrosal, and nodose all the neurons are derived from the placodal ectoderm. The small number of SPLI-positive cells of the nodose ganglia are not an exception to this rule. Therefore, generally speaking, the sensory neurons of the cranial ganglia that express the SP phenotype are derived from the crest, with the exception of some neurons present in the nodose of both quail and chick embryos and which are of placodal origin. The vast majority of placode-derived neurons do not have amounts of SP that can be detected under the conditions of the present study.     

A comparative and quantitative study of small intensely fluorescent (SIF) cells in the sympathetic ganglia of some small mammals

This comparative study of the number of SIF cells in the ganglions of the rat, cat, rabbit, mouse and hamster has confirmed that the mean number of SIF cells in the same ganglion of different species varies greatly, for instance in the superior cervical ganglion (SCG) of the rat and the cat, in the stellate ganglion of the cat and the mouse, or in the inferior mesenteric ganglion of the hamster and the other species. There is also considerable variability among individuals of the same animal species. In the SCG, the only ganglion for which there are data on the number of neurons, the ratio of SIF cells to neurons is around 1% in the rat, 0.2% in the rabbit, 0.3% in the mouse and 0.05% in the cat, i.e. a twenty-fold difference between the cat and the rat. Williams et al. (1975) distinguished type 1 SIF cells, corresponding to interneurons, from type 2, which are purely endocrine cells. Type 2 appears to be predominant in all ganglia, except the rabbit SCG where type 1 is highly predominant, and in all species, except the rat, in which this distinction is not applicable. The possible implications of these data on ganglionic functioning are discussed.     

Brain expansion and comparative prenatal ontogeny of the non-hominoid primate cranial base

The basicranium is the keystone of the primate skull, and understanding its morphological interdependence on surrounding soft-tissue structures, such as the brain, can reveal important mechanisms of skull development and evolution. In particular, several extensive investigations have shown that, across extant adult primates, the degree of basicranial flexion and petrous orientation are closely linked to increases in brain size relative to cranial base length. The aim of this study was to determine if an equivalent link exists during prenatal life. Specific hypotheses tested included the idea that increases in relative endocranial size (IRE5), relative infratentorial size (RIE), and differential encephalization (IDE) determine the degree of basicranial flexion and coronal petrous reorientation during non-hominoid primate fetal development. Cross-sectional fetal samples of Alouatta caraya (n=17) and Macaca nemestrina (n=24) were imaged using high-resolution magnetic resonance imaging (hrMRI). Cranial base angles (CBA), petrous orientations (IPA), base lengths, and endocranial volumes were measured from the images. Findings for both samples showed retroflexion, or flattening, of the cranial base and coronal petrous reorientation as well as considerable increases in absolute and relative brain sizes. Although significant correlations of both IRE5 and RIE were observed against CBA and IPA, the correlation with CBA was in the opposite direction to that predicted by the hypotheses. Variations of IDE were not significantly correlated with either angle. Correlations of IPA with IRE5 and RIE appeared to support the hypotheses. However, partial coefficients computed for all significant correlations indicated that changes to the fetal non-hominoid primate cranial base were more closely related to increases in body size than the hypothesized influence of relative brain enlargement. These findings were discussed together with those from a previous study of modern human fetuses.     

Distribution of substance P immunoreactive cell bodies and fibers in cranial sensory and autonomic ganglia of the chick

Substance P-immunoreactive neurons were demonstrated in chick embryonic and adult trigeminal ganglion and jugular-superior ganglionic complex using FITC-immunohistochemical methods. Both small-size and large ganglion cells exhibited SP immunoreactivity, without apparent changes during embryonic and post-hatching development. SP-positive fibers could be detected in a good number in the sympathetic cranial cervical ganglion, either during embryonic development or in adult chick. No immunoreactive perikarya were observed in this ganglion. In the ciliary ganglion, both choroidal and ciliary neurons were SP-negative, whereas SP immunoreactive fibers surrounded the perikarya of both cell populations.