The brain of the common vampire bat, Desmodus rotundus murinus (Wagner, 1840): a cytoarchitectural atlas.

The vampire bat, Desmodus rotundus, is exceptionally agile and stealthy in nature. Feeding at night on cattle blood, it is a known scourge carrying rabies. It is endowed with a very high neocortical volume among bats, acute olfactory capabilities and an accessory olfactory system. These characteristics have resulted into an impressive number of neuroanatomical investigations except a long due atlas on its brain. This study presents a cytoarchitectural atlas of the brain of the common vampire, Desmodus rotundus murinus, in the frontal plane, serially between the olfactory bulb and the medulla oblongata. Twenty six selected sections are presented, each separated by about 300 to 560 microns. The atlas figures show lugol fast blue-cresyl echt violet stained hemisections with their matching half in a labeled line drawing. About 595 discrete brain structures (some repeating) have been identified. This study is likely to provide the accurate localization of nuclear groups, whole structures, fiber tracts, and interconnections to facilitate future neuroanatomical and neurophysiological investigations on the vampire brain.

The brain of the common vampire bat, Desmodus rotundus murinus (Wagner, 1840): a cytoarchitectural atlas / O cérebro do morcego vampiro comum, Desmodus rotundus murinus (Wagner, 1840): um atlas citoarquitetural

The vampire bat, Desmodus rotundus, is exceptionally agile and stealthy in nature. Feeding at night on cattle blood, it is a known scourge carrying rabies. It is endowed with a very high neocortical volume among bats, acute olfactory capabilities and an accessory olfactory system. These characteristics have resulted into an impressive number of neuroanatomical investigations except a long due atlas on its brain. This study presents a cytoarchitectural atlas of the brain of the common vampire, Desmodus rotundus murinus, in the frontal plane, serially between the olfactory bulb and the medulla oblongata. Twenty six selected sections are presented, each separated by about 300 to 560 microns. The atlas figures show lugol fast blue-cresyl echt violet stained hemisections with their matching half in a labeled line drawing. About 595 discrete brain structures (some repeating) have been identified. This study is likely to provide the accurate localization of nuclear groups, whole structures, fiber tracts, and interconnections to facilitate future neuroanatomical and neurophysiological investigations on the vampire brain.

O morcego vampiro, Desmodus rotundus, é excepcionalmente ágil e furtivo. Alimentando-se à noite do sangue de gado, é um conhecido flagelo portador da raiva. Entre os morcegos, apresenta um alto volume neocortical, capacidades olfatórias agudas e um sistema ofatório suplementar. Estas características têm suscitado um número impressionante de estudos neuroanatômicos, no entanto, não foi produzido ainda um atlas do cérebro desta espécie. O presente estudo apresenta, assim, um atlas citoarquitetural do cérebro do vampiro comum, Desmodus rotundus murinus, no plano frontal, serialmente entre o bulbo ofatório e a medula oblongata. Vinte e seis seções selecionadas são aqui apresentadas, cada uma separada por em torno de 300 a 560 mícrones. As figuras do atlas mostram hemisseções manchadas com lugol violeta de cresilo, com a sua respectiva metade apresentada numa figura rotulada. Em torno de 595 estruturas cerebrais discretas (algumas repetidas) foram identificadas. Este estudo proverá a localização precisa de grupos nucleares, estruturas inteiras, tratos de fibras, e interconexões para facilitar futuras investigações neuroanatômicas e neurofisiológicas realizadas no cérebro do morcego vampiro.

Histochemical localization of enzymes and lipids in the ovary of a vespertilionid bat, Scotophilus heathi, during the reproductive cycle.

The present study describes seasonal changes in delta5 3beta hydroxysteroid dehydrogenase (3beta-HSD), glusose-6 phosphates dehydrogenase (G-6-PD), and lipids in the ovary of a vespertilionid bat, Scotophilus heathi. Total lipids and 3beta-HSD activity are restricted to thecal and interstitial cells of the ovary. The total lipids, 3beta-HSD, and G-6-PD significantly increase during recrudescence, and remain high during winter dormancy and breeding as compared to the other reproductive phases. High incidence of lipids and enzyme activity in interstitial cells during the breeding period and at the time of ovulation clearly suggests that these cells are actively involved in steroidogenesis. A decline in enzymes and lipid activity during winter dormancy, which correlates with the declining levels of steroidogenesis, might be the factors responsible for prolonged survival of the Graafian follicle in the ovary of S. heathi.

Histochemical localization of enzymes and lipids in the ovary of a vespertilionid bat, Scotophilus heathi, during the reproductive cycle

O presente estudo descreve as mudanças sazonais na D5 3b hidroxiesteróide desidrogenase (3b-HSD), glicose-6 fosfato desidrogenase (G-6-PD), e lipídios no ovário de um morcego vespertilionidae, Scotophilus heathi. As atividades totais dos lipídios e do 3b-HSD estão restritas às células tecais e intersticiais do ovário. Os lipídios, 3b-HSD e G-6-PD totais, aumentaram significantemente durante a recrudescência, e permaneceram elevados durante a dormência de inverno e o período de acasalamento, quando comparados a outras fases reprodutivas. A alta incidência de atividade de lipídios e enzimas nas células intersticiais durante o período de acasalamento e durante o período de ovulação sugere claramente que estas células estão ativamente envolvidas na esteroidogênese. O declínio da atividade dos lipídios e enzimas durante a dormência de inverno, o qual se correlaciona com os níveis decrescentes da esteroidogênese, podem ser o fator responsável pela longa sobrevivência do folículo de De Graaf no ovário do S. heathi.

Observations on the vomeronasal organ of prenatal Tarsius bancanus borneanus with implications for ancestral morphology.

Adult primates have at least five known phenotypes of vomeronasal organ (VNO), ranging from the typical morphology seen in most other mammals to complete absence. With such morphological disparity, the phylogenetic value and any inferences on ancestral VNO morphology of the primate VNO are left uncertain. The present study investigated the VNO of embryonic and fetal Tarsius bancanus borneanus (n = 4) in comparison with prenatal specimens from four other species of primates in an effort to clarify adult morphological variations. In all except one of the fetal primates, the VNO communicated to the nasopalatine duct. One exception occurred in the largest fetal Tarsius (25 mm crown-rump length), in which the VNO communicated with the nasal cavity alone. The vomeronasal neuroepithelium was well differentiated from a thinner, non-sensory epithelium in all Tarsius and New World monkeys studied, as well as late embryonic and fetal Microcebus myoxinus. In anterior sections, this neuroepithelium was found in a more superior location in Tarsius and New World monkeys compared with Microcebus myoxinus. In all primates, masses of cell bodies were found superior to the VNO, intermingled with nerve fibres. These morphologically resembled luteinizing hormone-releasing hormone neurons described in other mammals, including humans, suggesting that a primitive association of these neurons with the VNO may exist in all primate taxa. The present study revealed that prenatal similarities exist in Tarsius and New World primates in VNO epithelial morphology. However, these are transient stages of morphology. If tarsiers and anthropoids do represent a clade (Haplorhini), then the atypical morphology seen in adult tarsiers and New World monkeys probably represents the adult VNO morphology of a haplorhine common ancestor.

Size of the vomeronasal organ in wild Microtus with different mating strategies.

Most studies on mammalian vomeronasal organ (VNO) have been on laboratory-bred animals. Our present study examines the VNO in wild-caught meadow voles (Microtus pennsylvanicus: n=16) and prairie voles (M. ochrogaster: n=15). These species vary in their mating strategies and degree of parental care by males. M. ochrogaster exhibits pair bonding and more paternal care compared to M. pennsylvanicus, a promiscuous species. We hypothesize that sexual dimorphism will occur in the promiscuous species based on previous studies which suggest that those who exhibit more aggressive or masculine behavior have larger VNOs. Our results support our original finding that VNOs are not different in size in wild Microtus spp. that vary in male parental tendencies. However, the present study also indicates that M. pennsylvanicus, the species exhibiting more disparate parental tendencies, exhibited larger VNOs in females than males. This is the reverse of previous findings on rats, and we hypothesize that this difference may be due to mate selectivity and/or maternal aggression.

Human pineal luteinizing hormone receptors.

The presence of luteinizing hormone receptors in human pineal glands from five females and three males, ranging in age from 61-89 yr, was examined by in situ hybridization and immunocytochemistry. The results demonstrated the presence of these receptors at the mRNA and protein levels in all the pineal glands examined. Pineal gland luteinizing hormone receptors could potentially be involved in the regulation of melatonin synthesis.

Anatomical position of the vomeronasal organ in postnatal humans.

In the last decade or so, there has been a renewed interest in the adult human vomeronasal organ (VNO). Studies have yielded sometimes disparate findings about the microscopic structure of the organ and its supporting tissues. Such varied descriptions may be due to examination of different regions of the VNO, individual variation of VNOs among humans, or the presence of multiple, non-homologous structures that bear false resemblance to the human VNO. A histological description of the spatial relationship of the human VNO to other nasal septal elements is needed to ensure that all investigators are examining the same regions and homologous structures. Histologically sectioned nasal septa from, 22 human cadavers (1 child, 21 adults) were examined grossly and by light microscopy for the VNO. Using histological sections, the position of the VNO relative to other structures was estimated. Sections containing the VNO were retrospectively compared to scaled photographic slides of the unsectioned septa to identify surface landmarks. Human VNOs varied in anteroposterior and superoinferior position relative to the anterior nasal spine and the nasal cavity floor. In the absence of a visible duct opening, the only reliable surface marker, no consistent surface markings were noted for precise location. VNOs were frequently found superior to swellings associated with the paraseptal and/or septal cartilages. Such findings demonstrate that the human VNO is positionally variable, which may have contributed to previous conflicting findings on presence versus absence. Furthermore, our findings support recent suggestions that the VNO may have been misidentified by some investigators, and that its opening can be easily confused with other structures.

The human vomeronasal organ. III. Postnatal development from infancy to the ninth decade.

The large literature on the human vomeronasal organ (VNO) offers little consensus as to its persistence in the adult. We have already documented the existence of the VNO from embryonic day 33 through the neonatal stages. This has now been extended to human adults: 27 cadaver nasal septa, aged 2-86 y, were either dissected or decalcified, serially sectioned, stained and examined. The consistent presence of the VNO is reported as a homologue, in the form of a duct-like structure on the nasal septum at all ages. Also reported are size variability, pronounced bilateral asymmetry, a nonchemosensory pseudostratified ciliated epithelium with considerable structural variation and generally without medial-lateral differentiation, nasal septal glands opening into the VNO lumen, a lack of correlation between postnatal age and VNO size, visualisation of the human VNO with certainty by histological means alone, and a minute opening as its only visible surface feature. The human VNO is a discrete structure that should not be confused with the nasopalatine fossa, the septal mucosal pits or VNO openings.

Reappraisal of the vomeronasal system of catarrhine primates: ontogeny, morphology, functionality, and persisting questions.

The vomeronasal organ (VNO) is a chemosensory organ that functions in sociosexual communication in many vertebrates. In strepsirhine primates and New World monkeys, the bilateral VNOs are traditionally understood to exist as a well-developed chemosensory epithelial unit. In contrast, the VNOs of catarrhine primates are thought to be absent or exist only as reduced epithelial tubes of uncertain function. However, the VNO of New World monkeys shows substantial variation in the extent of sensory epithelium. Recent findings that the chimpanzee (Pan troglodytes) possesses a VNO similar to humans suggest the variability of the VNO among haplorhine primates may be more extensive than previously thought, and perhaps more at par with that observed in chiropterans. The atypical histologic structure and location of the human/chimpanzee VNO suggest accessory glandular secretion and transport functions. Other catarrhine primates (e.g., Macaca spp.), may truly be characterized by VNO absence. Unique aspects of facial growth and development in catarrhine primates may influence the position or even presence of the VNO in adults. These recent findings demonstrate that previous investigations on some catarrhine primates may have missed the VNO and underestimated the extent of variability. As an understanding of this variation increases, our view of VNO functionality and associated terminology is changing. Further investigations are needed to consider phylogenetic implications of VNO variability and the association of craniofacial form and VNO anatomic position in primates.

The existence of the vomeronasal organ in postnatal chimpanzees and evidence for its homology with that of humans.

It is currently thought that New World monkeys, prosimians, and humans are the only primates to possess vomeronasal organs (VNOs) as adults. Recent studies of the human VNO suggest that previous investigations on Old World primates may have missed the VNO. We examined nasal septa from the chimpanzee (Pan troglodytes) grossly and histologically for comparison with nasal septa from humans, Old World monkeys (Macaca fascicularis, M. nemistrina) and prosimian primates (Microcebus murinus, Otolemur garnettii). Grossly, chimpanzees had depressions on the nasal septum similar to fossae reported anterior to the VNO openings in humans. Histologically, chimpanzees and humans had bilateral epithelial tubes which were above the superior margin of the paraseptal cartilages (vomeronasal cartilage homologue). The epithelial tubes had a homogeneous ciliated epithelium. These structures were thus positionally and structurally identical to the human VNO and unlike the well-developed prosimian VNOs which were surrounded by vomeronasal cartilage. Macaques had no structures which resembled the VNO of either the prosimians or humans. The results demonstrate that the VNO is present postnatally in the chimpanzee and is almost identical to the human VNO in its anatomical position and histological structure. This in turn suggests that the reported absence of the VNO in at least some adult Old World primates is artifactual, and that further study may provide evidence for its existence in other species.

The human vomeronasal organ. Part II: prenatal development.

During the 20th century, the human vomeronasal organ (VNO) has been controversial regarding its structure, function, and even identity. Despite reports that provide evidence for its presence throughout prenatal and postnatal ontogeny, some studies and numerous textbooks declare its absence in late fetal and postnatal humans. To that end, the present study was designed to establish firmly whether the human VNO is homologous with that of other mammals and whether it degenerates (partially or completely) or persists throughout prenatal development. Fifty human embryos and fetuses (33 d to 32 wk fertilisation age) and 2 neonates were examined by light microscopy. Four embryonic primates (mouse lemurs) were examined for a comparison of VNO embryogenesis. The presence or absence and structural characteristics of the VNO and supporting tissues are described. The first appearance of the VNO was in the form of bilateral epithelial thickenings of the nasal septum, the vomeronasal primordium. The primordia invaginated between 37 and 43 d of age and formed the tubular VNO. The tubular VNO was located dorsally at a variable distance from, but was always spatially separated from the paraseptal cartilages. The mouse lemurs examined in this study and other reports from the literature indicate that the human VNO resembles that of primates having functional VNOs until just after a tubular VNO is formed. Examination of the VNO and adjacent tissues suggested that the VNO may lose receptor cells and corresponding vomeronasal nerves and become a ciliated, pseudostratified epithelium between approximately 12 and 14 wk of age. Our findings indicate the prenatal human VNO goes through 3 successive stages: early morphogenesis, transformation (of the epithelium), and growth. These observations indicated that (1) all embryonic humans develop a vomeronasal organ which is homologous with the VNOs of other mammals, but which has become displaced and highly variable in relative location during embryogenesis; (2) the human vomeronasal organ does not degenerate prenatally, but very likely loses the functional components of the vomeronasal complex of other mammals; and (3) the remnant of the human VNO persists until birth and beyond.

Right-sided aorta: a cadaver report and brief discussion of human aortic arch anomalies.

We observed an unusual right-sided aorta during routine laboratory dissection. The short aortic arch passed to the right side of the esophagus and trachea and had four branches, from proximal to distal: left common carotid, right common carotid, right subclavian, left subclavian arteries. The ligamentum arteriosum connected the pulmonary trunk to the left subclavian artery and lay to the left of the esophagus and trachea. The left recurrent laryngeal nerve passed under the ligamentum arteriosum while the right recurrent laryngeal nerve passed under the aortic arch. The descending thoracic aorta was situated near the midline, anterior to the vertebral bodies; consequently, the right posterior intercostal arteries were shorter than normal. The large veins of the thorax and the other thoracic organs appeared normal.

Comparative morphology and histochemistry of glands associated with the vomeronasal organ in humans, mouse lemurs, and voles.

The vomeronasal organ (VNO) is a chemosensory structure of the vertebrate nasal septum that has been recently shown to exist in nearly all adult humans. Although its link to reproductive behaviors has been shown in some primates, its functionality in humans is still debated. Some authors have suggested that the human VNO has the capacity to detect pheromones, while others described it as little more than a glandular pit. However, no studies have utilized histochemical techniques that would reveal whether the human VNO functions as a generalized gland duct or a specialized chemosensory organ. Nasal septal tissue from 13 humans (2-86 years old) were compared to that of two adult lemurs (Microcebus murinus) and eight adult voles (four Microtus pennsylvanicus and four Microtus ochrogaster). Sections at selected intervals of the VNO were stained with periodic acid-Schiff (PAS), alcian blue (AB), AB-PAS, and PAS-hematoxylin procedures. Results revealed typical well-developed VNOs with tubuloacinar glands in Microtus and Microcebus. VNO glands were AB-negative and PAS-positive in voles and mouse lemurs. Homo differed from Microtus and Microcebus in having more branched, AB and PAS-positive glands that emptied into the VNO lumen. Furthermore, the human VNO epithelium had unicellular mucous glands (AB and PAS-positive) and cilia, similar to respiratory epithelia. These results demonstrate unique characteristics of the human VNO which at once differs from glandular ducts (e.g., cilia) and also from the VNOs of mammals possessing demonstrably functional VNO.

The endotheliochorial interhemal membrane of the Indian musk shrew, Suncus murinus: an ultrastructural study.

Even though the chorioallantoic placenta of Suncus has been previously investigated with light and electron microscopy, controversies related to its structure still remain. To resolve these, Suncus murinus placentae from several (early and late limb bud, advanced pregnancy, and full term) were examined by electron microscopy. The interhemal membrane of Suncus comprises a maternal endothelium with basal lamina, syncytial trophoblast with its basal lamina, fetal mesenchyme, and fetal capillary endothelium. Layering of these components remain unchanged throughout gestation. The most striking feature of the interhemal membrane is the hypertrophied mesenchymal and maternal epithelial layers. The syncytiotrophoblast develops into a sieve-like transtrophoblastic spongy layer bearing numerous processes of the hypertrophied maternal endothelium. Mesenchymal cells intervene amidst the fetal endothelium displaying a high protein synthesizing activity. The interhemal membrane of Suncus is confirmed to be endotheliochorial.

Human olfactory bulb: aging of glomeruli and mitral cells and a search for the accessory olfactory bulb.

The aims of this study on the human olfactory bulb were two. First morphometry of the bulbs revealed marked declines during aging in the numbers of mitral cells and glomeruli, the bulb's principal integrative and relay elements. Numbers of glomeruli and mitral cells in each bulb of the young adult human were found to be approximately 8,000 and 40,000, respectively; these numbers declined steadily with age at an approximate rate of 10% per decade, so that in the ninth and tenth decades less than 30% of these elements remain in place. Such a marked decline with aging is suggested to underlie in part the decline in olfactory abilities (odor detection and identification) of humans with aging. In a separate study a systematic search for presence of an accessory olfactory bulb in the adult and aging bulbs was undertaken. No positive evidence for such an organized formation was found in the various regions of the adult bulbs of different age groups. The implications of these negative findings for the recent theories on human vomeronasal function and pheromonal perception are discussed.

Vomeronasal organ in bats and primates: extremes of structural variability and its phylogenetic implications.

The mere appearance of a tubular, epithelially-covered, bilateral structure, no matter how minuscule, on the anteroventral nasal septum of tetrapods, is generally called the vomeronasal organ (of Jacobson). However, considering the functionality of this chemosensory structure, the presence of a non-cilated (microvillar) neuroepithelium (and not just any odd type of epithelium) encased in a variously shaped vomeronasal cartilage, along with vomeronasal nerve bundles and above all an accessory olfactory bulb connected to the limbic vomeronasal amygdala, are the absolute essential neurostructural characteristics and anatomic requirement for a functional VNO and the accessory olfactory system in any tetrapod. The distribution of the vomeronasal organ is reported here in two mammalian orders: Chiroptera and Primates. An impressive data pool on the vomeronasal organ of bats is now available, pointing to the fact that at this time bats may be the only group in which this organ system is extremely variable, ranging from total absence (even in the embryo) to spectacular development with numerous intervening stages in different chiropteran species. Of the eighteen bat families, only one family of New World leaf-nosed bats, family Phyllostomidae, exhibits functional vomeronasal organs. The vespertilionid bat Miniopterus, and the mormoopid bat Pteronotus, present exceptions to this rule. Among Primates, very few species have been rigorously studied. As a result, developmental variability of the vomeronasal organ is almost unknown; either the vomeronasal organ is well developed (such as in New World monkeys) or absent (as in Old World monkeys and great apes) in the adult. The concept whether adult humans or embryonic and fetal forms are endowed with this so-called sixth sense, is a controversial one and is under intense study in our laboratory and by others. The general phylogenetic implications based on our cladistic analysis of bats are that the vomeronasal organ complex has evolved several times. Among the prosimians and platyrrhine primates, the organ is well developed, although to a varying degree. Among catarrhine primates, its loss has occurred only once, as it is generally absent in the adult forms.

Structure and diversity in mammalian accessory olfactory bulb.

The accessory olfactory bulb (AOB) is the first neural integrative center for the olfactory-like vomeronasal sensory system. In this article, we first briefly present an overview of vomeronasal system organization and review the history of the discovery of mammalian AOB. Next, we briefly review the evolution of the vomeronasal system in vertebrates, in particular the reptiles. Following these introductory aspects, the structure of the rodent AOB, as typical of the well-developed mammalian AOB, is presented, detailing laminar organization and cell types as well as aspects of the homology with the main olfactory bulb. Then, the evolutionary origin and diversity of the AOB in mammalian orders and species is discussed, describing structural, phylogenetic, and species-specific variation in the AOB location, shape, and size and morphologic differentiation and development. The AOB is believed to be absent in fishes but present in terrestrial tetrapods including amphibians; among the reptiles AOB is absent in crocodiles, present in turtles, snakes, and some lizards where it may be as large or larger than the main bulb. The AOB is absent in bird and in the aquatic mammals (whales, porpoises, manatees). Among other mammals, AOB is present in the monotremes and marsupials, edentates, and in the majority of the placental mammals like carnivores, herbivores, as well as rodents and lagomorphs. Most bat species do not have an AOB and among those where one is found, it shows marked variation in size and morphologic development. Among insectivores and primates, AOB shows marked variation in occurrence, size, and morphologic development. It is small in shrews and moles, large in hedgehogs and prosimians; AOB continues to persist in New World monkeys but is not found in the adults of the higher primates such as the Old World monkeys, apes, and humans. In many species where AOB is absent in the adult, it often develops in the embryo and fetus but regresses in later stages of development. Finally, new areas in vomeronasal system research such as the diversity of receptor molecules and the regional variation in receptor neuron type as well as in the output neurons of the AOB and their projection pathways are briefly discussed. In view of the pronounced diversity of size, morphologic differentiation, and phylogenetic development, the need to explore new functions for the vomeronasal system in areas other than sexual and reproductive behaviors is emphasized.

Subisthmic accessory thyroid gland in man: a case report and a review of thyroid anomalies.

Morphological variations of the thyroid gland are common and generally occur superior to the gland, reflecting its developmental origin. In this report we describe an accessory lobe located inferior to both lateral lobes and the isthmus. The accessory lobe was supplied by a branch of the right inferior thyroid artery and its vein drained via the plexus thyroideus impar. A discussion of thyroid anomalies is presented and a system for classifying variations of thyroid anatomy is proposed.