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Abstract ObjectivesThe aim of the present study is to broaden our knowledge of the ontogeny of cranial base cartilaginous joints in primates. Materials and MethodsA cross‐sectional age sample of 66 specimens from four platyrrhine and three strepsirrhine genera were studied using microcomputed tomography, histology, and immunohistochemistry. Specimens were segmented, reconstructed, and measured using Amira software. Ontogenetic scaling of palatal, presphenoid, and basisphenoid length relative to cranial length was examined using standardized major axis regression. After histological sectioning, selected specimens were examined using immunohistochemistry of antibodies to proliferating cell nuclear antigen. ResultsOur results support the hypothesis that the presphenoid in platyrrhines grows more rapidly compared with strepsirrhines, but this study establishes that most or all of this growth discrepancy occurs prenatally, and mostly at the presphenoseptal synchondrosis (PSept). All species have prolonged patency (here meaning absence of any bony bridging across the synchondrosis) of the intrasphenoidal and spheno‐occipital synchondroses (ISS). However, immunohistochemical results suggest growth is only rapid throughout infancy, and mitotic activity is slowing during juvenile ages. The same is indicated for the PSept. DiscussionThese results demonstrate that platyrrhines and strepsirrhines do not follow the pattern of early fusion of ISS seen in humans. In addition, these primates have a more prolonged patency and growth at PSept compared with humans. Finally, results reveal that in bushbabies and tamarins, as in humans, synchondroses remain cartilaginous for a prolonged period after chondrocyte proliferation has slowed or ceased. In light of these results, it is time to reassess related processes, such as differences in timing of brain expansion. 

Abstract Nasal turbinals, delicate and complex bones of the nasal cavity that support respiratory or olfactory mucosa (OM), are now easily studied using high resolution micro‐computed tomography (μ‐CT). Standard μ‐CT currently lacks the capacity to identify OM or other mucosa types without additional radio‐opaque staining techniques. However, even unstained mucosa is more radio‐opaque than air, and thus mucosal thickness can be discerned. Here, we assess mucosal thickness of the nasal fossa using the cranium of a cadaveric adult dog that was μ‐CT scanned with an isotropic resolution of 30 μm, and subsequently histologically sectioned and stained. After co‐alignment of μ‐CT slice planes to that of histology, mucosal thickness was estimated at four locations. Results based on either μ‐CT or histology indicate olfactory mucosa is thicker on average compared with non‐olfactory mucosa (non‐OM). In addition, olfactory mucosa has a lesser degree of variability than the non‐OM. Variability in the latter appears to relate mostly to the varying degree of vascularity of the lamina propria. Because of this, in structures with both specialized vascular respiratory mucosa and OM, such as the first ethmoturbinal (ET I), the range of thickness of OM and non‐OM may overlap. Future work should assess the utility of diffusible iodine‐based contrast enhanced CT techniques, which can differentiate epithelium from the lamina propria, to enhance our ability to differentiate mucosa types on more rostral ethmoturbinals. This is especially critical for structures such as ET I, which have mixed functional roles in many mammals. 

Abstract Living primates show a complex trend in reduction of nasal cavity spaces and structures due to moderate to severe constraint on interorbital breadth. Here we describe the ontogeny of the posterior end of the primate cartilaginous nasal capsule, the thimble shaped posterior nasal cupula (PNC), which surrounds the hind end of the olfactory region. We used a histologically sectioned sample of strepsirrhine primates and two non‐primates (Tupaia belangeri,Rousettus leschenaulti), and histochemical and immunohistochemical methods to study the PNC in a perinatal sample. At birth, most strepsirrhines possess only fragments of PNC, and these lack a perichondrium. Fetal specimens of several species reveal a more complete PNC, but the cartilage exhibits uneven or weak reactivity to type II collagen antibodies. Moreover, there is relatively less matrix than in the septal cartilage, resulting in clustering of chondrocytes, some of which are in direct contact with adjacent connective tissues. In one primate (Vareciaspp.) and both non‐primates, the PNC has a perichondrium at birth. In older, infantVareciaandRousettus, the perichondrium of the PNC is absent, and PNC fragmentation at its posterior pole has occurred in the former. Loss of the perichondrium for the PNC appears to precede resorption of the posterior end of the nasal capsule. These results suggest that the consolidation of the basicranial and facial skeletons happens ontogenetically earlier in primates than other mammals. We hypothesize that early loss of cartilage at the sphenoethmoidal articulation limits chondral mechanisms for nasal complexity, such as interstitial expansion or endochondral ossification. 

Abstract Cranial synchondroses are cartilaginous joints between basicranial bones or between basicranial bones and septal cartilage, and have been implicated as having a potential active role in determining craniofacial form. However, few studies have examined them histologically. Using histological and immunohistochemical methods, we examined all basicranial joints in serial sagittal sections of newborn heads from nine genera of primates (five anthropoids, four strepsirrhines). Each synchondrosis was examined for characteristics of active growth centers, including a zonal distribution of proliferating and hypertrophic chondrocytes, as well as corresponding changes in matrix characteristics (i.e., density and organization of Type II collagen). Results reveal three midline and three bilateral synchondroses possess attributes of active growth centers in all species (sphenooccipital, intrasphenoidal, presphenoseptal). One midline synchondrosis (ethmoseptal) and one bilateral synchondrosis (alibasisphenoidal synchondrosis [ABS]) are active growth centers in some but not all newborn primates. ABS is oriented more anteriorly in monkeys compared to lemurs and bushbabies. The sphenoethmoidal synchondrosis (SES) varies at birth: in monkeys, it is a suture‐like joint (i.e., fibrous tissue between the two bones); however, in strepsirrhines, the jugum sphenoidale is ossified while the mesethmoid remains cartilaginous. No species possesses an SES that has the organization of a growth plate. Overall, our findings demonstrate that only four midline synchondroses have the potential to actively affect basicranial angularity and facial orientation during the perinatal timeframe, while the SES of anthropoids essentially transitions toward a “suture‐like” function, permitting passive growth postnatally. Loss of cartilaginous continuity at SES and reorientation of ABS distinguish monkeys from strepsirrhines. 

Abstract Previous descriptive work on deciduous dentition of primates has focused disproportionately on great apes and humans. To address this bias in the literature, we studied 131 subadult nonhominoid specimens (including 110 newborns) describing deciduous tooth morphology and assessing maximum hydroxyapatite density (MHD). All specimens were CT scanned at 70 kVp and reconstructed at 20.5–39 μm voxels. Grayscale intensity from scans was converted to hydroxyapatite (HA) density (mg HA/cm³) using a linear conversion of grayscale values to calibration standards of known HA density (R²= .99). Using Amira software, mineralized dental tissues were captured by segmenting the tooth cusps first and then capturing the remainder of the teeth at descending thresholds of gray levels. We assessed the relationship of MHD of selected teeth to cranial length using Pearson correlation coefficients. In monkeys, anterior teeth are more mineralized than postcanine teeth. In tarsiers and most lemurs and lorises, postcanine teeth are the most highly mineralized. This suggests that monkeys have a more prolonged process of dental mineralization that begins with incisors and canines, while mineralization of postcanine teeth is delayed. This may in part be a result of relatively late weaning in most anthropoid primates. Results also reveal that in lemurs and lorises, MHD of the mandibular first permanent molar (M₁) negatively correlates with cranial length. In contrast, the MHD of M₁positively correlates with cranial length in monkeys. This supports the hypothesis that natural selection acts independently on dental growth as opposed to mineralization and indicates clear phylogenetic differences among primates. 

Abstract Nasal anatomy in rodents is well-studied, but most current knowledge is based on small-bodied muroid species. Nasal anatomy and histology of hystricognaths, the largest living rodents, remains poorly understood. Here, we describe the nasal cavity of agoutis ( Dasyprocta spp.), the first large-bodied South American rodents to be studied histologically throughout the nasal cavity. Two adult agoutis were studied using microcomputed tomography, and in one of these, half the snout was serially sectioned and stained for microscopic study. Certain features are notable in Dasyprocta . The frontal recess has five turbinals within it, the most in this space compared to other rodents that have been studied. The nasoturbinal is particularly large in dorsoventral and rostrocaudal dimensions and is entirely non-olfactory in function, in apparent contrast to known muroids. Whether this relates solely to body size scaling or perhaps also relates to directing airflow or conditioning inspired air requires further study. In addition, olfactory epithelium appears more restricted to the olfactory and frontal recesses compared to muroids. At the same time, the rostral tips of the olfactory turbinals bear at least some non-olfactory epithelium. The findings of this study support the hypothesis that turbinals are multifunctional structures, indicating investigators should use caution when categorizing turbinals as specialized for one function (e.g., olfaction or respiratory air-conditioning). Caution may be especially appropriate in the case of large-bodied mammals, in which the different scaling characteristics of respiratory and olfactory mucosa result in relative more of the former type as body size increases. 

The sphenoid bone articulates with multiple basicranial, facial, and calvarial bones, and in humans its synchondroses are known to contribute to elongation of the skull base and possibly to cranial base angulation. Its early development (embryological, early fetal) has frequently been studied in a comparative context. However, the perinatal events in morphogenesis of the sphenoid have been explored in very few primates. Using a cross-sectional age sample of non-human primates (n=39; 22 platyrrhines; 17 strepsirrhines), we used microcomputed tomographic (µCT) and histological methods to track age changes in the sphenoid bone. In the midline, the sphenoid expands its dimensions at three growth centers, including the sphenooccipital, intrasphenoidal (ISS) and presphenoseptal (PSept) synchondroses. Bilaterally, the alisphenoid is enlarged via appositional bone growth that radiates outward from cartilaginous parts of the alisphenoid during midfetal stages. The alisphenoid remains connected to the basitrabecular process of the basisphenoid via the alibasisphenoidal synchondrosis (ABS). Reactivity to proliferating cell-nuclear antigen is observed in all synchondroses, indicating active growth perinatally. Between mid-fetal and birth ages in Saguinus geoffroyi , all synchondroses decrease in the breadth of proliferating columns of chondrocytes. In most primates, the ABS is greatly diminished by birth, and is likely the earliest to fuse, although at least some cartilage may remain by at least one-month of age. Unlike humans, no non-human primate in our sample exhibits perinatal fusion of ISS. A dichotomy among primates is the orientation of the ABS, which is more rostrally directed in platyrrhines. Based on fetal Saguinus geoffroyi specimens, the ABS was initially oriented within a horizontal plane, and redirects inferiorly during late fetal and perinatal stages. These changes occur in tandem with forward orientation of the orbits in platyrrhines, combined with downward growth of the midface. Thus, we postulate that active growth centers direct the orientation of the midface and orbit before birth. 

Diffusible iodine-based contrast-enhanced computed tomography (diceCT) has emerged as a viable tool for discriminating soft tissues in serial CT slices, which can then be used for three-dimensional analysis. This technique has some potential to supplant histology as a tool for identification of body tissues. Here, we studied the head of an adult fruit bat ( Cynopterus sphinx ) and a late fetal vampire bat ( Desmodus rotundus ) using diceCT and µCT. Subsequently, we decalcified, serially sectioned and stained the same heads. The two CT volumes were rotated so that the sectional plane of the slice series closely matched that of histological sections, yielding the ideal opportunity to relate CT observations to corresponding histology. Olfactory epithelium is typically thicker, on average, than respiratory epithelium in both bats. Thus, one investigator (SK), blind to the histological sections, examined the diceCT slice series for both bats and annotated changes in thickness of epithelium on the first ethmoturbinal (ET I), the roof of the nasal fossa, and the nasal septum. A second trial was conducted with an added criterion: radioopacity of the lamina propria as an indicator of Bowman’s glands. Then, a second investigator (TS) annotated images of matching histological sections based on microscopic observation of epithelial type, and transferred these annotations to matching CT slices. Measurements of slices annotated according to changes in epithelial thickness alone closely track measurements of slices based on histologically-informed annotations; matching histological sections confirm blind annotations were effective based on epithelial thickness alone, except for a patch of unusually thick non-OE, mistaken for OE in one of the specimens. When characteristics of the lamina propria were added in the second trial, the blind annotations excluded the thick non-OE. Moreover, in the fetal bat the use of evidence for Bowman’s glands improved detection of olfactory mucosa, perhaps because the epithelium itself was thin enough at its margins to escape detection. We conclude that diceCT can by itself be highly effective in identifying distribution of OE, especially where observations are confirmed by histology from at least one specimen of the species. Our findings also establish that iodine staining, followed by stain removal, does not interfere with subsequent histological staining of the same specimen.