A Comparative Study- of Cranial Growth in Homo and Macaca 1 HERMAN S. DUTERLO02 AND DONALD H. ENLOW Department of Anatomy and Center for Human Growth and Development, The University of Michigan, Ann ATbOr, Michigan ABSTRACT This study deals with the postnatal growth and remodeling changes that take place in the cranial bones of Macaca mulatta. Multiple ground sections were prepared throughout each component bone from the calvaria and cranial floor of young, rapidly growing specimens having primary or mixed dentition. These sections were then analyzed for (1) the different types of inward-growing and outward-grow- ing bone tissues present, and (2) the distribution of resorptive and depository periosteal and endosteal surfaces. Using this information, the remodeling history of each bone was reconstructed and the overall growth pattern of the cranium as a whole was de- termined. The growth changes that characterize the brain case of the monkey were then compared and contrasted with those in Homo. While a number of distinct similarities were observed in their respective growth and remodeling processes, sev- eral marked differences were also found. These occurred largely in certain parts of the cranial floor and they appeared to be associated with corresponding differences in the size, configuration, and disposition of the brain in the two species and also with factors related to body posture and facial prognathism. The purposes of this study are (1) to de- 1). Overall growth and remodeling pat- scribe and illustrate the postnatal remodel- terns for all of the bones in relation to each ing processes that take place in the cra- other were then analyzed. These interpre- nium of Macaca mulatta, (2) to interpret tations are based largely on three basic these processes according to the morpho- principles of bone growth that have been logical and functional factors that are re- utilized in preceding reports (Enlow, ’68a). lated to them, and (3) to compare growth They are briefly summarized below. changes in the cranium of the Rhesus Surfaces facing toward and away fTom monkey with those that characterize the the direction of growth. Those surfaces of human skull. This study is a sequel to a bone, both endosteal and periosteal, which previous reports dealing with the growth are oriented so that they face toward the of the human facial skeleton (Enlow and growth direction receive new bone deposi- Harris, ’64; Enlow and Bang, ’65) and tion. Conversely, those particular surfaces comparative studies of facial growth be- that face away from this direction are re- tween the human and the monkey (En- sorptive. A cortical plate undergoes direct low, ’66, ’68b). growth mouement (a process termed “drift”) by the combination of new bone MATERIALS AND METHODS addition on one side and removal from the Multiple ground sections were prepared contralateral side. An analysis of the dis- from each of the component bones in the tribution of resorptive and depository sur- cranial roof and floor. Dried skulls from 15 face types provides a basis for interpreting well preserved specimens having either the behavior of all the regional parts of a primary or mixed dentition were used. The bone duxing continued enlargement. Any sections were analyzed for the detailed given bone has a characteristic pattern in arrangement of both resorptive and de- the arrangement of these two types of sur- pository surfaces on all endosteal and faces, and the composite of all the cortical periosteal sides of the cortex in each of the changes that correspondingly take place individual bones. Using this information, represent the process of remodeling which the inward and outward directions of cor- 1 Supported in part by USPHS grant DE-02272. tical growth movements were determined 2 Present Address : Department of Orthodontics, School of Dentistry, University of Nymegen, Nymegen, and mapped for each bone as a whole (fig. The Netherlands. AM. J. ANAT., 127: 357-368. 357 358 HERMAN S. DUTERLOO AND DONALD H. ENLOW Fig. 1 The detailed distribution of resorptive and depository surfaces in the monkey skull are mapped in this diagram. Ectocranial and endocranial periosteal surfaces that undergo progressive resorption during growth are indicated by dark stippling. Depository surfaces are indicated by light stippling. A. inner aspect of the cranial floor; B. ventrolateral aspect; C. lateral aspect. Note the widespread occurrence of surface-resorptive growth fields in the occipital and temporal areas, within the orbit, on the cranial floor, on the posterior oral side of the hard palate, and within the pterygoid fossa. produces the proportionate expansion of portionate increases or decreases which the bone as a whole. function locally to sustain the overall con- Relocation. As a new bone continues to figuration of the entire bone. be deposited on a given surface, the other Displacement. Two basic types o€ regional parts of that bone necessarily be- growth movement are involved in skeletal come altered in their relative locations. In enlargement. As described above, actual order to maintain proportionate positions, cortical movement occurs as a result of these parts simultaneously undergo actual drift; i.e., deposition and resorption on op- growth movements that serve to place them posite sides of the same cortical plate. In in a succession of new locations as the addition, whole bones become passively whole bone continues to enlarge. This fac- moved or carried (“displaced) as a con- tor of relocation is a major feature of bone sequence of the enlargement of a group of growth, and it underlies the process of re- bones in relation to each other. Thus, the modeling itself. Thus, a bone does not grow floor of the cranium grows downward (to- simply by continued apposition at one or ward its articulation with the atlas), but two major “centers” of growth. Rather, all becomes correspondingly displaced in an parts of the whole bone are involved in opposite, superior direction. The progres- regional cortical changes that provide pro- sive increase in the mass of soft tissues CRANIAL GROWTH IN HOMO AND MACACA 359 that house the bones is believed to con- their structure, and former localized areas tribute directly to these complex move- of resorption have become covered by thin ments by displacement (Moss, ’62). layers of more recently deposited periosteal bone. OBSERVATIONS The growth pattern of the occipital bone Growth patterns in the differs from that of the other calvarial ele- cranium of macaca ments. The flattened portion which forms The calvaria. The greater part of the the floor and a part of the wall in the pos- external (cutaneous) side of the frontal terior cranial fossa is typically thin. It is and parietal bones, and also a portion of composed of a single layer of lamellar bone the squamous portion of the temporal, is containing a few small diploic spaces. In characterized by a uniformly depository figure lb, note that a large zone of external type of periosteal surface (fig. lb). The resorption is present in the nuchal region, inner periosteal (meningeal) surface ad- and that the remainder of the cutaneous jacent to the brain is similarly of a deposi- side is depository. This remodeling pattern tory nature. The cortex is usually com- provides a means of calvarial adjustment posed of a single layer of lamellar bone adapted to the differential extent of expan- tissue. Where large diploic spaces occur, sion by the various parts of the underlying the cortex is arranged into two tables, and brain. Because the cerebral hemispheres the resulting endosteal surfaces are resorp- enlarge to a greater degree than the more tive. inferiorly located cerebellum, the superior The outward growth movement of the part of the occipital bone necessarily be- calvaria is believed to be produced largely comes displaced in an ectocranial direction by passive displacement in conjunction to a proportionately greater extent than with sutural bone growth rather than di- does the more basal region adjacent to the rect cortical drift (Massler and Schour, cerebellum. The combination of external ’41; Vilmann, ’68). The process of new resorption and endocranial deposition in bone deposition on the external and inter- the latter area functions to move its cortex nal periosteal surfaces of these bones is not in an endocranial manner as the superior concerned primarily with the direct en- (squamous) part of the bone is carried largement of the brain case, but rather outward with the expanding cerebrum with proportionate increases in the thick- (fig. 2). The effective result is a “rotation” ness of the bony wall itself and with ad- of the bone, so that as the whole bone be- justments in its curvature as the whole comes displaced ectocranially, the basal cranium enlarges. A variable distribution part simultaneously pivots inward to sus- of external surface resorption has been ob- tain its contact with the slower-growing served near the lambdoidal and sagittal cerebellum (fig. 3). Although a small sutures. The walls in the suture areas are range of variation was found in the place- much thicker than the remainder of the ment of the reversal line that separates the bones, and these scattered patches of ex- resorptive from the depository growth fields ternal resorptive remodeling reduce cortical involved, only one specimen showed a total thickness as the regions involved become absence of a resorptive area. One other in- successively relocated away from the thick- dividual had several scattered patches of er suture areas during continued growth. surface resorption rather than a single, On the meningeal side of the cortex, varia- large resorptive field. ble and scattered resorption patches were The meningeal side of the squamous also found immediately adjacent to the part of the occipital is characterized by a various sutures and expand the concave predominantly depository type of surface contour of the internal cortical surface.