In the present study, we have examined the postnatal growth dynamics of the human facial skeleton and mandible through the analysis of the bone modelling activity (Fig. 5). The bone modelling patterns obtained in this work reflect the distribution of forming and resorbing fields but without distinguishing between active or resting fields. A bone modelling map incorporating the distribution of the growth fields as well as the state (active or resting) and the rate of the cellular activity would be extremely valuable to understand the bone growth dynamics. Further research is needed to develop non-destructive methods to obtain this information. In spite of this lack of information, the interpretation of the bone modelling maps obtained in this work allowed us to approach the main, general, hypothetical growth dynamics that characterize the subadult and adult human facial skeleton and mandible. The bone modelling patterns from all specimens show a general downward-forward growth vector. However, there are ontogenetic differences in the distribution of growth fields that demonstrate postnatal changes in the bone growth dynamics. Integration of the modelling data from the different anatomical elements informs us about the general growth dynamics of the whole skull and its relationships with ontogenetic postnatal changes of the craniofacial system.
Bone growth dynamics in the subadult face and mandible
The modelling pattern of the face and the mandible from the subadult specimens established here is similar to the pattern described by Enlow & Hans (1996). The facial skeleton is characterized by depository surfaces in the upper (supraorbital region) and middle face (orbital and nasal regions) and bone resorption fields in the lower face (nasomaxillary region). According to this map, the upper and the middle face grow in a lateral and forward direction, whereas the zygomatic region grows laterally and is relocated posteriorly, in agreement with the resorbing surfaces present at the orbital margins. The lower face shows a large bone resorption field related to the formation of the canine fossa – a depression on the external surface of the maxillary bone region specific to Homo sapiens (Enlow & Hans, 1996). As reported by Enlow & Hans (1996), resorption in the nasomaxillary region occurs simultaneously with bone formation in the posterior region of the face (specifically in the craniofacial sutures) and in the nasal cavity floor and palate. Consequently, the lower face shows a downward or vertical growth related to the formation of the canine fossa and the increase in height of the nasal cavity (Kurihara et al. 1980; Enlow & Hans, 1996; McCollum & Ward, 1997).
The mandible pattern is characterized by depository surfaces in the symphyseal region and the anterior corpus, whereas the posterior region of the corpus and the ramus show a complex pattern of resorption and formation fields. According to these data, the mandible shows a forward growth associated to the deposition in the symphysis and the corpus, as well as to the lengthening of the posterior region of the corpus. At the same time, the ramus and the molar region of the corpus show a mainly lateral growth, together with a downward growth of the ramus and a posterior relocation of the condyle and coronoid region. It is worth mentioning that the symphyseal region presents a human-specific resorption field in the alveolar component of the buccal side related to the dental movements, the mental growth, and ultimately the development of the human chin (Enlow & Hans, 1996).
As a whole, the bone modelling pattern indicates that the subadult facial skeleton and mandible grow following a downward-forward vector. As we mentioned before, this general pattern agrees with the results of Enlow & Hans (1996), albeit with some differences. In opposition to Enlow & Hans (1996), the lingual side of the corpus shows resorption fields in the sublingual fossa and in the region anterior to the mandibular foramen, and formation in the submandibular fossa. Our modelling map also suggests a more marked lateral growth of the molar region in the mandibular corpus and ramus than in Enlow & Hans (1996) model. Other differences regarding the extension of the resorbing surfaces in the buccal side of the ramus could be considered artefacts due to the variability of the distribution of modelling fields observed in the human mandible (Enlow & Harris, 1964; Kurihara et al. 1980; Hans et al. 1995).
Our analyses also reveal variability in the distribution of the modelling fields mainly observed in the anterior lower face and in the mandibular ramus. In the anterior face, variability in the distribution and the extension of the resorption fields of the anterior face agrees with the modelling data provided by Kurihara et al. (1980) for humans up to 14 years old, but disagrees with the mainly depository anterior lower face observed by McCollum (2008). As mentioned by Kurihara et al. (1980) and later by McCollum (2008), variability in the modelling maps from this facial region could be due to morphological variations associated to different geographical origin. Variability in the mandible ramus involves the extension and location of the resorption fields in the coronoid and the condyle neck, due to lateral adjustments while growing upward and relocating posteriorly. Besides these two main areas, some variability is also observed in the buccal symphyseal region previously reported by Kurihara et al. (1980). In the mandibular corpus, individual 126 shows in the submandibular fossa a modelling pattern that resembles that established by Enlow & Hans (1996) but opposite to the general pattern obtained in the present work.
Bone growth dynamics in the adult face and mandible
In the present study, we have established for the first time, to our knowledge, the bone modelling pattern of the face and the mandible from adult humans. The facial pattern is mainly depository with resorption surfaces restricted to the nasal region, the canine fossae, and the inferior margin of the zygomatic region. Resorption at the nasal region could be associated to the increase in height of the nasal aperture (McCollum, 2008) and the forward projection of this region (Bastir, 2008). The resorption fields in the area of the canine fossae are likely related to the development of this specific feature of Homo sapiens. In the zygomatic region, resorption surfaces would reflect the complex growth dynamics associated to the mechanical strains of the masticatory force (Herring, 1993; Lieberman et al. 2000, see references therein). The increase of the bone formation surfaces that characterized the adult modelling map leads us to hypothesize that the adult face shows downward and forward growth directions with the main emphasis in the horizontal direction, in agreement with morphometric data obtained in previous work (Bastir, 2008). However, more data, particularly on the modelling processes at the nasomaxillary complex, are needed to fully understand the downwards movements of the lower face during adulthood.
In the adult mandible, the symphysis and the anterior region of the corpus are mainly depository, with resorbing surfaces restricted to the alveolar component of the buccal side of the symphysis. This modelling field distribution is similar to that observed in subadult specimens and reflects the growth dynamics associated to dental movements and also to the development of this particular feature of Homo sapiens (Enlow & Hans, 1996). Resorption fields are also present in the lingual side of the symphysis. These fields are located in sites related to the attachments of the gastricus, genioglossus, geniohyoideus, and the anterior part of the mylohyoideus muscles. The pattern of the posterior region of the corpus and the ramus differs greatly from the subadult patterns established in the present and in previous works (Kurihara et al. 1980; Enlow & Hans, 1996). The buccal side shows resorption fields covering the posterior region of the corpus and the anterior region of the ramus, whereas the resorption fields of the lingual side are located in the submandibular fossa of the corpus, and in the coronoid region and the lower half (gonial area) of the ramus. This map indicates a forward growth direction of the symphysis and a lateral growth of the molar region of the corpus, whereas the anterior region of the ramus grows in a posterior and medial direction. The posterior region of the ramus experiences complex growth dynamics characterized by a lateral growth of the gonial area, a medial growth of the mandibular notch area, and a lateral and medial growth of the condyle area. These growth directions indicate that the lower part of the ramus is taking or maintaining a vertical position while the upper area increases in width and grows backwards.
The modelling pattern of the facial skeleton and the mandible varies less in adult than in subadult specimens. Variability is observed in the extension of the resorption fields of the anterior nasomaxillary region and the mandibular ramus, as observed in subadults. Following the previous interpretations for subadult specimens (Kurihara et al. 1980; Enlow & Hans, 1996; McCollum, 2008), we hypothesize that these variations could respond to individual differences in morphological characteristics.
Postnatal changes in the growth dynamics of the human face
According to the data obtained in the present study, the facial skeleton and mandible from subadult and adult specimens show a general downward and forward growth, in agreement with Enlow & Hans (1996). Both groups also show a marked spatial gradient of the variability in the modelling field distribution from the anterior region of the maxilla with high variability to the almost constant upper facial regions in the proximity of the neurocranium. However, bone modelling patterns differ between both age groups. Subadult specimens show a marked downward growth direction, whereas adults are characterized by a forward direction. The interpretation of these ontogenetic changes within the craniofacial biology context allows us to approach how different skeletal components interact to maintain the functional and structural balance, but increase in size during the postnatal development (Moss & Young, 1960; Enlow & Hans, 1996).
During the subadult stage, the facial skeleton experiences a downward growth and a forward displacement, while the maxilla increases in length. This growth and displacement of the facial block is accompanied by an upward maxillary rotation (airorhynchy) due to the higher bone growth in the craniofacial sutures that attach the midface to the basicranium than in the anterior region of the maxilla (Enlow and Bang, 1965; Björk & Skieller, 1976; Bromage, 1989; Enlow & Hans, 1996; McCollum & Ward, 1997). Rotation of the premaxilla would be balanced by a downward rotation through compensatory resorption activity in the external surfaces of the anterior region of the maxilla (Björk, 1969; Björk & Skieller, 1976, 1983; see also Bromage, 1989; McCollum & Ward, 1997 and references therein). The resulting downward growth vector contributes to the characteristic facial retraction of Homo sapiens (Bromage, 1989; Enlow & Hans, 1996). Simultaneously, the mandible is displaced forward and downward to compensate the displacements of the maxilla and to maintain the occlusal plane (Enlow & Hans, 1996). The forward displacement of the face becomes balanced through the growth of the posterior region of the mandibular corpus, whereas the vertical growth is compensated by the increase in height of the ramus and, particularly, the condyle (Enlow & Hans, 1996). During this displacement, the mandibular corpus increases in width in the anterior region, whereas the molar region and the ramus show a lateral drift. The lateral drift and the vertical growth of the ramus have been related to the growth of the basicranium to keep the mandible in contact with the neurocranium through the temporomandibular joint.
With adulthood, the modelling pattern changes, reflecting the biological changes that occurred during the craniofacial development. The most important differences are observed in the anterior region of the face, where the resorbing surfaces that occupy the subadult nasomaxillary region become restricted to the canine fossa in adults. This increase of the bone formation fields in adult specimens suggests a mainly forward growth of the whole facial skeleton with an increase in the height of the nasal region. The mandible responds to these changes and shows bone modelling differences located mainly in the ramus. Complex growth dynamics in this mandibular region show a lateral and medial growth that maintains the vertical position and the contact with the neurocranium through the temporomandibular joint (Enlow & Hans, 1996). As well, the ramus increases in a way highly similar to the nasomaxillary region, whereas the whole mandible grows with the main forward direction accompanying the anterior region of the face growth.
To understand the biological meaning of these modelling changes, we need to consider several parallel developmental events that occur in the craniofacial system. The growth and development of each craniofacial bone should be analysed as part of the integrated complex system influenced by multifactorial processes involving genetic and epigenetic factors (Moss & Young, 1960; Atchley & Hall, 1991; Enlow & Hans, 1996; Lieberman et al. 2002). Early in the ontogeny, the craniofacial growth is characterized by the increase in the size of the brain, the growth of both the cranial base and the neurocranium, and the flexion of the cranial base. During the rapid expansion of the brain, the neurocranium enlarges mainly from deposition within the cranial sutures, as well as expanding through modelling activity, with bone deposition in the ectocranial surface and bone resorption in the endocranial surface (Duterloo & Enlow, 1970; Enlow & Hans, 1996). The basicranium also increases in length and breadth through the modelling mechanism and the sutural bone formation (Enlow & Hans, 1996: Opperman, 2000). These cranial dynamics, and particularly the cranial base flexure, influence the size and projection of the facial skeleton that shows the main downward growth as inferred from the bone modelling data obtained in the present and previous studies (e.g. Lieberman et al. 2000; Bastir et al. 2010). The mandible also shows a downward growth direction that increases in height as it grows forward in order to maintain the occlusal plane with the maxilla. As well, the lateral growth of the ramus inferred in the present work indicates how the ramus grows to maintain contact with the cranial base through the temporomandibular joint.
Critical changes occur in the human skull at around 14 years of age and new relationships emerge among craniofacial components. The brain, having reached 95% of the total size by age 6 years, reaches its final brain size at an average age of 14.5 years in males and 11.5 years in females (Giedd et al. 1999, 2006; Lenroot & Giedd, 2006, 2010). In the second decade of the postnatal development, the growth of the cranial base ceases and most occipital bone sutures fuse, whereas the sphenoid bone sutures fuses in the first decade (Madeline & Elster, 1995,b; Lingawi, 2012). The calvarial sutures also fuse completely at 20–30 years old (Vijay Kumar et al. 2012). However, most facial sutures remain patent until late adulthood, e.g. the frontomaxillary, nasomaxillary and zygomaticomaxillary, which start to fuse until the 7th or 8th decade of life (Rice, 2008). Interestingly, the facial skeleton continues growing into adulthood, whereas the neurocranium and cranial base by that time have already stopped growing (Bastir et al. 2006; Edwards et al. 2007; Holton & Franciscus, 2008). Reduction of the resorption fields in the adult anterior face could be indicating that this continue growth of the face occurs with a mainly forward direction. Thus, the retracted facial skeleton – a defining characteristic of Homo sapiens – is established in the subadult period (e.g. Moss & Young, 1960; Lieberman et al. 2002; Holton et al. 2010). The mandible also responds to these developmental changes, as reflected in its modelling pattern observed mainly in the ramus. As the neurocranium and basicranium stop growing, the distance between the mandible fossae becomes established and the condyles would adapt to this distance, changing the growth of the condyles to maintain the contact with the neurocranium through the temporomandibular joint (Enlow & Hans, 1996). The increase in height of the ramus also responds to the vertical growth of the nasomaxillary region in order to maintain the occlusal plane.
The particular features of the modelling pattern of the adult face and mandible could be related to the increase of the volume of the oro-naso-pharyngeal cavities. This hypothesis would agree with the relationship established between the growth and development of the craniofacial complex and the nasal respiratory function (Moss & Young, 1960; Moss, 1962; Klein, 1986; Hall, 2005a; Chinn et al. 2006; Rosas et al. 2006; Weinstein, 2008; Gungora & Turkkahramanb, 2009). Moreover, it has been proposed that the bone growth of the facial skeleton and particularly the nasomaxillary complex and the mandible are related via physiological factors to the general body size or the metabolic requirements (Hall, 2005b; Rosas et al. 2006; Bastir, 2008 and references therein). In agreement, we hypothesize that, once the growth of the neurocranium and cranial base ceases, the forward growth direction of the adult human face indicates an increase of airway dimensions – the oro-naso-pharyngeal cavities – to maintain the integration between airway, relative body and lung size due to the augmented energy requirements (Henry & Rees, 1991; Rosas & Bastir, 2002; Rosas et al. 2006).
In conclusion, our results demonstrate postnatal changes in the hypothetical growth dynamics of the facial skeleton and the mandible from a mainly downward direction in subadults to a mainly forward direction in adults. We hypothesize that these changes are related to biological events occurring in the craniofacial system, such as cessation of the brain growth, fusion of the craniofacial sutures, growth of the cranium and cranial base, as well as flexion of the cranial base. During adulthood, a new relationship among skeletal elements of the skull emerges and growth dynamics change, stressing the forward growth of the face. We hypothesize that the adult growth of the face is related to the increase of the airway dimensions (the nasal and oral cavities) to cope with the physiological demands.