Craniofacial levels and the morphological maturation of the human skull

Abstract

It is well known that the human skull achieves adult size through a superior-inferior gradient of maturation. Because the basicranium matures in size before the face, it has been suggested that the form of the basicranium might have ontogenetic knock-on effects on that of the face. However, although sequential spatially organized maturation of size is well described in the cranium, the maturation of skull shape is not. Knowledge of the maturation of shape is important, nevertheless, because it is claimed that the early determination of the spatial configuration of basicranial components, where the facial skeleton attaches, is relevant in the spatio-temporal ontogenetic cascade from basicranium to face. This paper examines the ontogeny of various components of the human skull in 28 individuals from the longitudinal Denver Growth Study. Sixty-six landmarks and semilandmarks were digitized on 228 X-rays and analysed using geometric morphometric methods. Bootstrapped confidence intervals for centroid size support previous studies suggesting a supero-inferior gradient of growth maturation (size over time), while developmental maturation (shape over time) is more complex. A sequence of shape maturation is described, in which the earliest structure to mature in shape was the midline cranial base (7-8 years), followed by the lateral cranial floor (11-12), midline neurocranium (9-10) and facial and mandibular structures (15-16). The absolute ages of shape maturation of the latter three depended on the criterion of maturity used, which was not the case for the basicranial components. Additionally, ontogenetic dissociations were found between the maturation of size and shape of the midline cranial base and lateral floor, possibly underlining its role as structural 'interface' between brain and facial ontogeny. These findings imply potential for bidirectional developmental influences between the lateral cranial floor and the face until about 11-12 years. The findings are discussed with regard to their relevance for palaeoanthropology and especially the evolutionary and developmental bases of skull morphological variation.

Fig. 1

Craniofacial levels of skull development. The lines connecting the origin schematically indicate the hypothesized (Buschang et al. 1983; Enlow & Hans, 1996) differences in maturation of the various craniofacial levels; they do not imply ontogenetic shape trajectories, which would be multivariate and curvilinear. The temporal sequence of morphological maturation shows that the neurobasicranial complex reaches adult shape earlier than the ethmomaxillary complex and the mandible.

Fig. 2

(A) Lateral radiograph indicating the equiangular fan at the neurocranium and the equidistant combs across the basicranium and the face. The intersections of the fan/comb lines with the anatomical structures define semilandmarks. (B) Procrustes fit and slid semilandmarks. (C) Consensus configuration and landmark numbers.

Fig. 3

Maturation patterns of (A) the neurobasicranial and (B) the ethmomaxillary complex. In the inset graphs centroid size and shape (Procrustes) distances to adults are plotted. The significances of the differences in size and shape between the subadults and adults are shown on the bars beneath these graphs, in which dashed lines indicate significant differences from adult. These indicate the immature portions of the ontogenetic trajectories, solid lines the mature ones (absence of significant differences). The reference and transformation grids for the relevant landmark configurations are shown beneath each graph. Squares indicate midline basicranial structures while filled dots indicate lateral basicranial structures.

Fig. 4

Maturation patterns of (A) the mandible and (B) the midline cranial base. The differences in size and shape between the subadults and the adults are given. In the inset graphs centroid size and shape (Procrustes) distances to adults are plotted. The significances of the differences in size and shape between the subadults and adults are shown on the bars beneath these graphs in which dashed lines indicate significant differences from adult. These indicate the immature portions of the ontogenetic trajectories, solid lines the mature ones (absence of significant differences). The reference and transformation grids for the relevant landmark configurations are shown beneath each graph. Note the ontogenetic dissociation in the midline cranial base between the achievement of adult size (by G7) and adult shape (by G4).

Fig. 5

Maturation patterns of (A) the lateral cranial floor and (B) the midline neurocranium. In the inset graphs centroid size and shape (Procrustes) distances to adults are plotted. The significances of the differences in size and shape between the subadults and adults are shown on the bars beneath these graphs in which dashed lines indicate significant differences from adult. These indicate the immature portions of the ontogenetic trajectories, solid lines the mature ones (absence of significant differences). The reference and transformation grids for the relevant landmark configurations are shown beneath each graph. Note the ontogenetic dissociation in the lateral cranial floor between the achievement of adult size (in G8) and adult shape (in G6).