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.
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.
The purpose of this study is to describe basicranial and brain growth in sub‐adult cotton‐top tamarin (Saguinus oedipus) and compare their growth with greater bushbabies (Otolemur spp.) based on computed tomographic (CT) imaging. Bilateral synchondroses (alisphenoid‐basisphenoid synchrondrosis, ABS) have been identified within the middle cranial fossa of bushbabies which indicate active growth centers at this stage of development. In Saguinus, the ABS fuses relatively earlier and is oriented more anteriorly than in Otolemur. In this study, we used micro‐computed tomography (CT) and imaging software (Amira) to study heads of Saguinus and Otolemur that died of natural causes at two ages: near birth and at approximately one‐month postnatal age. Using Amira, the endocranial contour of crania were manually segmented throughout serial slices, in order to generate a three‐dimensional view of an endocast. This allowed a comparison of brain shape differences between ages in each species. In both species, the occipital lobe is proportional broader and more posteriorly projected at one‐month of age. In addition, the endocast of both species are more complex in contour in the older specimens (i.e., surfaces were more rounded at birth). In Otolemur, the cerebellum and the temporal lobes are more inferiorly positioned in the older animal. In contrast, in Saguinus, the cerebellum becomes less pronounced due to a relative overgrowth of the cerebrum. Also, in Saguinus the temporal lobes are more laterally projecting and anteriorly displaced at one‐month. These results are consistent with the hypothesis that the ABS fuses early in primates, and bone modeling has a primary role in accommodating postnatal shape changes in the brain. However, we note that the ABS is oriented differently (more anteriorly) in the monkey, associated with the relatively anterior displacement of the temporal lobe. Support or Funding Information NSF # BCS‐1830894, BCS‐1830919, BCS‐0959438
Objectives:The aim of the present study is to broaden our knowledge of the ontogeny of cranial base cartilaginous joints in primates. Materials and Methods:A 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.Results: Our 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 sphenooccipital 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.Discussion: These 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.
It has been hypothesized that the human sphenoid bone is uniquely truncated, which in turn contributes to a reduction of forward midfacial growth. If so, the perinatal fusion of the intrasphenoidal synchondrosis (ISS) in humans may contribute to midfacial reduction. However, there is a lack of detailed knowledge on sphenoid development of non‐human primates. In this study, orientation and direction of growth of basicranial interface with the midface of late prenatal and early postnatal sphenoid development was examined in ontogenetic samples of primates including three species of monkeys (n = 25) and four species of lemurs and bushbabies (strepsirrhines; n= 28). Micro‐computed tomographic (CT) and histological methods were used to track cross‐sectional age changes in the sphenoid bone. In monkeys (Saguinus spp.), histological findings indicated the number of proliferating chondrocytes is reduced across age leading to a reduction in absolute anteroposterior length of the proliferating zone. Preliminary data from micro‐CT reconstructions suggest that absolute length of the ISS decreases more rapidly in monkeys than in strepsirrhines. Measurements of presphenoid (PS) and basisphenoid (BS) length indicate that in strepsirrhines, these bones grow similarly to one another as cranial length increases. In contrast, in monkeys, the PS increases at a faster pace (i.e. higher linear regression line slopes) than the BS. However, unlike humans, the monkeys studied have prolonged postnatal patency of the ISS. Thus, the reduced midfacial projection in humans and these monkeys cannot be explained by the timing of ISS fusion alone. Dichotomous growth patterns of the cranial base and midface among primates suggest different patterns of regional integration of the cranium. In particular, our results suggest that in monkeys, integration of the midface is stronger with the anterior compared to the posterior portion of the sphenoid bone. In strepsirrhines by comparison, growth of the midface progressively deviates from that of the sphenoid bone over time. Support or Funding Information NSF; grant numbers BCS‐1830894, BCS‐1830919, BCS‐0959438
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