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The role of function in the development of human craniofacial form ФA perspective.

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THE ANATOMICAL RECORD 218:107-110 (1987)
The Role of Function in the Development of Human
Craniofac ial Form-A Perspective
M.R. KEAN AND P. HOUGHTON
Departments of Orthodontics (M.R.K.) and Anatomy [I? H.), Uniuersity of Otago,
P 0. Box 647, Ditnedin, New Zealand
ABSTRACT
As a n anatomical region the head combines great diversity of function with close integration of structure. Consequently no structural component has
autonomy of form. There is a sequence of maturation of functions and their related
structural components, and in this sequence the nervous system and its supportive
structures mature first. The nasal airway matures next in response to increasing
body mass, and the masticatory system constitutes the last major functional system
to reach maturity. The later the maturation of the function, the greater is the
requirement for its related morphology to adapt to preceding skeletal templates.
These matters of developmental sequence, and extrinsic as well as intrinsic craniofacial functions, are paramount considerations in interpreting the form of any
component of head anatomy.
Studies in craniofacial biology, whether developmental, structural, or functional, frequently fall within
a single conceptual framework: A discrete region is examined as though it were a n autonomous unit, and
without regard to the influence of other craniofacial
regions, or of the body as a whole. Studies of variation
isolated to the masticatory system, or the cranial vault,
are examples. Yet the subtle fact is that within the
functionally diverse yet structurally integrated architecture of the head, no component has autonomy; all are
influenced by the demands of other components. Furthermore, as some head components subserve wholebody functions, in any study of craniofacial structure
the relationship between the demands of the whole body
and the form of the head must be considered.
This paper presents a perspective on the form of the
craniofacial skeleton derived from the developmental
sequence of extrinsic and intrinsic functional demands
made on the head. Structurally the sequence is expressed as a series of templates. Later-maturing components adapt to preceding templates, which requires the
latest maturing structures to be the most adaptable.
Such a perspective begins with a consideration of the
developmental sequence within the head. Here the nervous system assumes priority. Soon after closure of the
neural tube in the fourth week of embryonic life, the
forebrain, midbrain, and hindbrain vesicles are recognizable. At this time brainstem flexures appear, and the
cranial nerves are starting to form. During the sixth
week the cranial base, which serves as a supportive
platform for the brain - and a suspensory beam for the
facial structures - begins to appear in cartilage. As
early as the sixth week the flexure of the base is apparent, mirroring the angulation ofthe brain. Over succeeding weeks of embryonic development the elements of the
base fuse, but remain permeated by canals and foramina
carrying cranial nerves and major blood vessels. Thus
0 1987 ALAN R. LISS, INC.
the supportive base develops in intimate and dependent
relationship with the nervous system, a relationship
seen a t its most complex in the course of the seventh
cranial nerve and its branches through the temporal
and sphenoid bones.
This developmental precocity of the nervous system is
matched by a cellular conservatism. With early completion of its cellular complement and a very limited capacity for regeneration and repair, the nervous system is
structurally the least modifiable of body systems. Any
substantive change in morphology of the cranial base,
including its flexure, would be undesirably disruptive to
the brain stem and emergent nerves. This overall stability of form of the cranial base during development has
been considered to be due to its being under “strong
genetic control” (van Limborgh, 1972; Glenister, 1976;
Simons and van Limborgh, 1979; Bromage, 1980; Hanken, 1983). However, in the light of the sequence of
tissue development, and evidence derived from experimental studies (Young, 1959; Moss, 1961; Schowing,
1968a,b; Moss et al., 1972; Greelen, 1973; Blechschmidt,
1976; Simons, 1979; Sarnat, 1982) this stability of form
should be ascribed to the influence of the nervous system. The subsequent growth of the base, involving no
significant change in flexure after the first year of postnatal life (Brodie, 1955; Knott, 1971; Riolo et al., 1974;
Broadbent et al., 1975; Lewis and Roche, 1977) and limited inferior cortical drift with a proportional increase
in length by growth at the transverse joints (Scott, 1958;
Enlow, 1982), requires minimal adjustment of the complex relationship between nerve tissue and the cartilage, and ultimately the bone, of the base.
Suspended from the anterior part of the base, the
central part of the upper facial skeleton varies in posiReceived December 15,1985; accepted January 13,1987.
108
M.R. KEAN AND P. HOUGHTON
tion according to the orientation of the base and the
length of its anterior part. For example, the upper face
is positioned more anteroinferiorly when suspended from
a n open than from a closed base (Enlow, 1982; Kean and
Houghton, 1982).But in addition, the upper face is influenced in shape and size by variation in volume of the
nasal airway. A functionally significant increase in airway volume is possible only through vertical development, increase in width of the airway being limited by
the general neurological constraints suggested above,
and particularly the positioning of the eyes. Longitudinal cephalometric studies (Riolo et al., 1974; Broadbent
et al., 1975) demonstrate that increase in height of the
airway is one of the major dimensional changes occurring in the face during maturation. The functional correlate of this is the increasing energy demand of the
growing body. Evidence for the direct association between body size and nasal airway height can be derived
from these cephalometric studies, which show that, on
average, the height of the nasal airway at maturity is
greater in males than in females, whereas until about
age 12 years nasal airway heights are similar, age for
age, for the two sexes. The reason why this should be so
lies neither in the nasal cavity nor the face, nor even in
the head, but in the greater respiratory needs of males,
in whom the greater functional demand is imposed on
the face by the body. Between 6 and 16 years muscle
mass increases about threefold in girls and fourfold in
boys (Malina, 1978), and from about 12 years the curve
for male muscle mass rises sharply, whereas that for
females is starting to flatten. That is, male and female
growth curves for muscle mass diverge from this age.
Similarly diverging growth curves for males and females are seen for vital capacity (Ferris et al., 1952;
Ferris and Smith, 1953). Airway enlargement is thus
appropriate to oxygen demand, and the extent to which
oxygen demand varies on average between males and
females, or between any two individuals during development or at maturity, determines the extent to which
the face develops vertically. Cross-sectional studies also
reveal a highly significant correlation between body
weight and nasal height in adults (Miyashita and Takahashi, 1971). Respiratory demand and the expansion
required of the airway are influenced by a complex interplay of factors, including inherited body size (particularly muscle mass), and environmental factors such as
diet, disease, altitude, and climate (Roberts, 1953; Heath
and Williams, 1981).
Although increase with maturation of the height of
the upper face is well documented, the significance of its
functional basis is not widely appreciated. Enlargement
of the nasal airway is obligatory as the body grows, and
as architectural substrate the airway, meeting an extrinsic demand, is a major influence on overall craniofacia1 form.
By contrast, the growth curves for the other component of upper facial height, the teeth and alveolus, unlike those for the airway, do not diverge significantly for
males and females with maturation (Riolo et al., 1974),
as there is no biological requirement for this either
within or beyond the head. And in absolute terms, a t
maturity the increase in height of the dentoalveolar
component of upper facial height has been only about
half that of the airway.
These upper facial growth changes, largely consequent on respiratory demand, lead inevitably to adjustments to the positioning of the maxillary dentition.
Continuing adaptation is thus required in the mandible,
particularly in the ramus and its related soft tissues, for
the form of the mandibular dentition and its supportive
bone has been determined at a n earlier stage of development and must in any case match the maxillary.
Thus, as the maxillary dentition shifts inferiorly with
enlargement of the airway during maturation, and the
occlusal plane and the body of the mandible align more
horizontally, mandibular angle lessens and the ramus
increases in height. Consistently, the more vertical the
ramus, the broader and higher it becomes, with larger
surface area; associated evidence of greater muscularity
is found in deeper, flattened temporal fossae with higher
temporal lines, and robust zygomatic arches (Sassouni,
1969; Houghton, 1978; Lavelle, 1979), these being the
compensatory muscular concomitants of the skeletal
changes. Hence, for a given cranial base morphology, a n
individual of large muscle bulk and large nasal airway,
requires that the process of adaptation of the masticatory system be carried further than in a small adult.
One skeletal manifestation of this is a lesser mandibular
angle in the more heavily muscled individual, this being
the biological basis of the observation in classical biometrics that at maturity, on average, males have smaller mandibular angles than females (Morant, 1936;
Hrdlicka, 1940).
The traditional view of the mandible as a third-order
lever during the power stroke, the condyles being stressbearing, survives through much debate (Hylander, 1975;
Gingerich, 1979; Moore, 1981; Moss, 1983) and is supported by a host of recent experimental biomechanical
studies (Hylander, 1979; Hylander and Bays, 1979;
Brehnan et al., 1981; Mongini et al., 1981; Standlee et
al., 1981; Hohl and Tucek, 1982). While the mechanical
efficiency of the maturing mandible decreases, the concept of efficiency or inefficiency of the mandibular lever
is one of physics rather than biology, relating to the
bony form alone. There is not a developmental or evolutionary set toward inefficiency, for the maturation of the
musculature proceeding concomitantly with the bony
change ensures biological efficiency.
The adaptation of the masticatory system to the templates of cranial base and airway in turn influences the
mature width of vault and face. The underlying cranial
base has two components in this dimension: the central
core penetrated by nerves and blood vessels; and lateral
regions related particularly to the masticatory apparatus. The width of the core is determined relatively early,
being related to the support required for the developing
brain whereas the width of the lateral regions, though
also providing support for the maturing hemispheres,
varies particularly with the degree of development of
the masticatory muscles whose maturation occurs much
later. Individuals with severe masticatory demands will
show hypertrophy of these muscles, and consequently a
wide area of attachment on the base, even in the presence of a mandible with a n open angle and of efficient
lever form. The face also is influenced by the development of the masticatory muscles behind the zygomatic
bone (Cachel, 1979); the “filling-out” and flattening of
the facial surface of the maxilla lateral to the airway is
DEVELOPMENT OF HUMAN CRANIOFACIAL FORM
an expression of greater buttressing for the zygomatic
bone and arch, and is thus a function of masticatory
development rather than directly a consequence of vertical development of the upper face, though the two are
associated. This influence of muscle development on the
cranial base and face is well demonstrated in cases of
unilateral trigeminal palsy, where there is reduced depth
of the pterygoid region, reduction in size of the corresponding pterygoid plate and fossa, and reduction in
width of the corresponding side of the face (Rogers, 1958).
The shape of the cranial vault has been ascribed to
variation in dimensions of the cranial base, long heads
being associated with long bases and round heads with
short bases (e.g., Lavelle, 1979; Enlow, 1982). However,
such direct expression of genetically determined brain
proportions tends to be obscured by the many other
influences on the vault (Buranarugsa and Houghton,
1981; Anderson and Popovich, 1983; Houghton and
Kean, 1986). For example, brain size, and thus vault
size, is influenced by nutrition (Brown, 1966; Israel,
1978; Metcoff, 1978). The flexure of brain stem and cranial base, or more distant influences such as body muscle mass and its determinants, influence vault form
through the masticatory system, with substantial temporalis muscles flattening the temporal fossae, and substantial pterygoid muscles widening the base. Thus,
while its early expansion may be dependent on growth
of the underlying brain, the final shape of the vault is
a n expression of a spectrum of influences. A sequence of
adaptations is apparent, the hemispheres of the brain
sometimes being required finally to adapt in form because of a sequence initiated by the primordial flexure
of the developing midbrain. However, unlike the situation with the attenuated nerves emerging from the
brainstem and passing through bony foramina, a gradual moulding of the hemispheres is physiologically
acceptable.
In this perspective of craniofacial form, the brain early
in development determines shape and size of the supportive cranial base. Subsequently the airway, constrained laterally by major sense organs, enlarges
vertically in harmony with the respiratory demand of
the body. The masticatory system, and specifically its
musculoskeletal component, adapts to the templates of
cranial base and airway, and in its turn influences the
form of the vault. This set of internal adaptations notwithstanding, the form and relationship between different parts of the head cannot be interpreted fully without
reference to the whole body.
From this perspective a holistic model emerges that
interprets the development of human craniofacial form
as the structural resultant of a predictable sequence of
functional demands. Crucial to a n appreciation of the
model is the realization that certain demands and influences beyond the head affect profoundly its overall form.
The significance of the model is that problems of head
morphology, or any component of it, may be pursued
deductively through studying the interaction of functional demand and structural maturation.
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