The chondrocranial key: Fetal and perinatal morphogenesis of the sphenoid bone in primates

Nanami Mano,Jane Taylor,James J Cray,Lanre Oladipupo,Emily Durham,Valerie B Deleon,Rebecca Reynolds,Christopher Vinyard,Brody Wood,Timothy D Smith

doi:10.3897/vz.71.e65934

Abstract

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 inSaguinus 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 fetalSaguinus geoffroyispecimens, 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.

Highlights

The mammalian sphenoid ossifies within the center of the chondrocranium, the cartilaginous template for most bones of the basicranium the ethmoid bone, and nasal cartilages (Starck 1967)
Comparative histogenesis of the primate sphenoid bone during early to midfetal ontogeny The early fetal slow loris (Nycticebus coucang) has little ossification of the chondrocranium, which still possesses the cartilaginous precursors for the sphenoid bodies and for the alisphenoid (Fig. 1A)
The cartilage is dense with chondrocytes, virtually devoid of extracellular matrix

Summary

Introduction

The mammalian sphenoid ossifies within the center of the chondrocranium, the cartilaginous template for most bones of the basicranium the ethmoid bone, and nasal cartilages (Starck 1967). When it first ossifies, multiple ossification centers coalesce as two midline elements, the presphenoid and basisphenoid, and paired bilateral elements, the orbitosphenoids and alisphenoids (de Beer 1937). Many of the joints of the sphenoid bone are active “growth centers” that may affect the form of the cranium (Baume 1968; McBratney-Owen et al 2008). Histological evidence across age exists for humans, a few primates, and various non-primates (e.g., Baume 1968; Hoyte 1973; Melsen 1974, 1977; Heinkele et al 1989; Kjaer 1990)

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Conclusion