Homo and Macaca 1

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-growing 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 determined. 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, several 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. (fig. la). Small, isolated spots of resorp- These transient resorptive spots apparent- tion occur in relation to the sutures, how- ly undergo constant change in location and ever, and function in adjustments of in- extent according to the configuration and ternal surface contour during active sutural the growth activity of the underlying bone growth. A broad, distinctive zone of brain. Frequent reversals are observed in resorption is characteristically present on 360 HERMAN S. DUTERLOO AND DONALD H. ENLOW

Fig. 2 This composite diagram illustrates the various regional remodeling changes that take place in the occipital area of the Rhesus monkey skull. Diagram A shows the area analyzed in B. Dia- gram B is an interpretation of regional growth directions occurring in the occipital fossa. The endocranial zone around the foramen magnum is resorptive; the contralateral ectocranial (ventral) surfaces are depository. Ventrally-moving cortical drift produces coordinated downward-directed growth. Simultaneously, the foramen itself becomes enlarged by this same process. A schematized illustration of this growth movement is shown in diagram C. the meningeal surface surrounding the separates the external depository from the perimeter of the foramen magnum (fig. 6). endocranial resorptive growth fields. In The cortical linings of the sigmoid sulcus three of the older specimens studied, a thin and the vermian sulcus are similarly sur- layer of surface bone had been deposited face resorptive in nature, and the greater over the resorptive growth fields lining the part of the occipital segment of the clivus meningeal side of the occipital bone. This is also marked by endocranial surface re- addition increased the thickness of the cor- sorption during its period of active growth. tex itself following the earlier period of ac- The placement of the reversal line that sep- tive cranial growth. arates the depository from the resorptive The sizeable endocranial resorptive zone parts of the clivus is variable but most fre- surrounding the foramen magnum and quently occurs slightly below the spheno. which extends superiorly onto the occipital occipital synchondrosis. The ectocranial portion of the clivus functions to lower surfaces of the cortex encircling the fora- this entire area and to move it anteriorly men magnum and that part of the occipital during continued growth. A process of di- bone adjacent to the pharynx are uniform- rect cortical growth (drift) is necessarily ly surface-depository in type. A circumspi- required here since the placement of su- nal reversal line, quite constant in occur- tures is such that these changes could not rence and placement, is present on the be produced by sutural growth. Thus, the crest of the foramina1 rim and thereby combination of resorption on the endocra- CRANIAL GROWTH IN HOMO AND MACACA 36 1 + the brain, including the hypophysis, olfac- tory bulbs, temporal lobes, cerebellum, and the auditory apparatus. In addition, major vessels and nerves pass through the floor. a situation that does not exist in the roof. The placement and the orientation of sutures in the cranial floor is such that the process of sutural bone growth cannot in itself entirely accommodate the extent of expansion required since many divergent t growth directions are involved. Further, a decreasing gradient of growth is involved as the midventral axis of the cranial base is approached. These multiple factors represent the functional basis for the marked differences in growth processes that characterize the cranial floor and roof, respec- tively (Enlow, ’68a). In figure la, note that a number of small, scattered resorptive areas characterize the meningeal surfaces of the anterior cranial floor, the prefrontal region of the forehead, and the anteroinferior depression of the middle cranial fossa. All of these regions are isolated, confined “cul de sacs” that re- quire an ectocranial mode of direct cortical drift. Sutures do not occur in most parts ++ of these separate fossae, and growth there- Fig. 3 This schematic diagram illustrates re- fore cannot take place in a manner com- modeling differences in the nuchal region of the parable to that in the skull roof. Transient occipital bone of Macaca (top) and Homo (bot- spots of endocranial resorption function to tom). Note the extensive resorptive area (-) on enlarge each fossa and to move the floor the external (cutaneous) surface of the flattened monkey occipital squama. In man, this compara- in an ectocranial direction as the ventral ble surface is entirely depository. Resorption on parts of the brain simultaneously increase the internal (meningeal) surface of this bone in in size. The variable resorptive patches also the monkey is limited to a distinctive zone sur- provide localized cortical remodeling ad- rounding the foramen magnum. In man, resorption on meningeal surfaces is much more exten- justments required to accommodate the sive and includes the entire cortical lining of the differential gradient of growth between the occipital fossa. See text for further description midventral part of the floor and its more and discussion. lateral regions associated with the hemispheres. This pattern, further, makes pos- nial surface and deposition on the ecto- sible the adjustments required in sustain- cranial side (1) moves the entire area in- ing the positions of vessels and nerves pass- feriorly; (2) enlarges the basal portion of ing through the cortex, a function that the posterior cranial fossa in a posterior di- could not be carried out if the sutural rection; (3) moves the clivus anteriorly; growth process represented the sole mech- and (4) proportionately enlarges the lu- anism of growth expansion. men of the foramen magnum itself (fig. 2). The cortical lining of the pituitary fossa In contrast to the smooth, even-con- is depository, although zones of surface re- toured endocranial surface of the skull sorption occur on the clinoid processes and roof, the internal topography of the cranial within the nearby optic foramina (fig. la). floor is complex and irregular. A number As previously mentioned, the sphenoidal of partially isolated compartments are pres- part of the clivus is depository. Thus, the ent that house the various ventral parts of prominent, medial elevation that comprises 362 HERMAN S. DUTERLOO AND DONALD H. ENLOW this general region, and which separates regional fields participate in a coordinated, the left and right middle cranial fossae, composite pattern of growth that utilizes grows in a superior direction as the entire different parts of several different bones. area itself becomes displaced inferiorly by The sizeable, irregular region of surface the expanding brain. This upward mode of resorption that occurs on the greater part growth not only functions to enlarge the of the external cortex lining the temporal median elevation but also to sustain its fossa involves portions of the temporal, position in relation to the slower-growing parietal, frontal and sphenoid bones (figs. midventral part of the brain as the lateral la,b,c). This variable resorptive area serves bony areas associated with the hemispheres as a growth pivot that adjusts the changing descend to a proportionately greater extent. contour bridging the bulging lateral cra- The longitudinal growth of this region is nial wall with the medially tapering de- provided, in part, by the spheno-occipital pression just behind the orbital rim. As the synchondrosis, the sphenoidal synchondro- protruding, convex lateral wall is carried sis, and the sphenoethmoidal juncture. ectocranially by displacement associated The prominent petrous elevation within the with expansion of the brain, sutural bone cranial cavity, like the midline sphenoidal growth simultaneously enlarges the cover- elevation, also has a depository type of age of the bones involved. A differential surface. This serves to proportionately en- extent of growth occurs, however, so that large the convex partition that separates the concave anteroinferior region, located the concave middle and posterior cranial within the temporal fossa, necessarily ro- fossae as all continue to expand simulta- tates inward to adjust its relative position neously. in response to the outward carry of the The surface of the cortex lining of each whole bones. Thus, as these bones all be- auditory canal is resorptive, and a reversal come displaced ectocranially in company line occurs at the rim of the meatus. The with the cerebrum, that portion located external side of the petrous portion of the within the fossa maintains contact with its temporal bone, like the outer surfaces of own slower-growing, smaller, anterior part the adjacent squamous part, is depository of the brain by means of a growth move- in nature. Similarly, the contiguous phar- ment in a medial (inward) direction. This yngeal side of the occipital and the sphe- remodeling adjustment requires a resorp- noid bones are of a depository surface type. tive cortical surface on the external side The orbit, zygomatic arch, and the tem- of the bone, a feature that differs from the poral fossa. Growth of these topographi- remodeling pattern found in the human cally complex, contiguous regions of the skull (see later discussion). skull involves a correspondingly complex Cortical remodeling changes on the pos- pattern of remodeling in order to produce terior side of the lateral orbital rim and on the proportionate enlargement of each in both sides of the zygomatic arch are es- relation to the others. In figures la and lb, sentially identical to those found in the note that large fields of periosteal resorp- human facial skeleton. The entire medial tion occur on the posterior side of the mas- surface of the arch as well as the posterior sive lateral orbital rim, on the medial side side of the orbital rim are characteristi- of the zygomatic arch, and on the surface cally resorptive. This contributes to a move- lining the temporal fossa. Although these ment of the rim in a progressively antero- resorptive areas are all directly continuous lateral course, and a movement of the arch with each other, their regional remodeling in a direct lateral direction. The cortex in functions during growth are quite differ- both regions is composed of typical endo- ent. Note that the reversal lines that sepa- steal bone tissue of a compacted cancellous rate these various resorptive fields from type (fig. 7). Note that the contralateral adjacent depository surfaces cross those surfaces in both regions (the anterolateral sutures present rather than follow them. side of the rim and the lateral surface of Each individual bone thus does not behave the arch) are depository in nature. This re- as an isolated growth unit that is essen- modeling combination, like the others de- tially independent of the rest. Rather, these scribed above, follows the principle dealing CRANIAL GROWTH IN HOMO AND MACACA 363 with “surfaces facing toward and away The pterygoid processes. The two plates from the direction of growth,” as previously that form the walls of each pterygoid fossa defined. are oriented so that their outer sides face The lengthening of the zygomatic arch anteriorly, which is the direction of pro- is produced largely by bone additions with- gressive growth. These external surfaces in the zygomaticotemporal suture (Gans are depository, while the cortical lining and Sarnat, ’51). As the horizontal dimen- within the fossa itself is resorptive. As the sion of the cranial cavity expands, concur- cranial floor elongates, the relative posi- rent deposition of bone in the suture pro- tions of the adjacent forward-facing ptery- portionately lengthens this zygomatic goid plates are thereby maintained by a bridge between the temporal and the malar proportionate anterior growth movement. bones. The point of union between the arch It is noted that the directly contiguous and the cranium is characterized by a re- maxillary tuberosity (posterior surface of versal line that separates the resorptive the maxillary corpus) grows in a posterior field on the medial side of the arch from- direction. The maxilla and the pterygoid the depository field on the lateral surface plates, separated only by the narrow ptery- of the temporal squama. gomaxillary fissure, thus grow toward each The lining of the orbital cavity is marked other. However, the entire maxilla becomes by a sizeable resorptive region that occu- displaced (carried) in an anterior course pies the lateral half of the thin, single- as it grows posteriorly, thereby sustaining layered roof and the superior half of the a constant positional relationship with the lateral wall. The contralateral endocranial pterygoid processes. side, which forms the lateral part of the DISCUSSION floor in the anterior cranial fossa, is depository. This remodeling combination Three basic modes of growth are opera- tive during the postnatal enlargement moves the entire superolateral portion of of the neurocranium in both man and the the orbit, which lacks sutures this re- in Rhesus monkey. First, increases in some gion, in a lateral direction as the cranial linear dimensions of individual bones in fossa, the zygomatic arch, and the zygo- the skull roof and cranial floor are pro- matic process of the frontal bone all grow duced by continued additions of new bone simultaneously in a corresponding direc- at either sutures or synchondroses. Second, tion. With the exception of the diminutive surface remodeling, involving differential lacrimal bone, the remainder of the bony deposition and resorption of bone according orbital lining is depository. The lacrimal to local directions of growth, occurs on vir- itself functions as an adjustment linkage tually all endosteal and periosteal surfaces, between the differentially growing bones both on the internal and external sides of that surround it (Enlow, ’68a). A converse the cranium. This functions to adjust the arrangement of resorption and deposition regional shape of each growing bone and occurs in the medial portions of the orbit to produce proportionate changes (de- and the anterior cranial fossa, in contrast creases as well as increases) in regional to the lateral parts just described. The orbi- size. Third, all of the bones become dis- tal side is depository and the opposite en- placed as they enlarge, thereby expanding docranial surface is irregularly resorptive. their spatial relationships to one another. Thus, the various cortical surfaces that Because of different morphological factors form both sides of the orbit follow the rule in the cranial floor as compared with the in which surfaces facing away from the calvaria, the combinations of these three growth direction are resorptive. The entire basic growth processes are correspondingly orbit grows and moves in a combined an- different in the two regions. The predomi- terior and lateral course as the frontal lobe nant mode of calvarial enlargement in- of the cerebrum expands in a correspond- volves sutural growth with only relatively ing direction. Except for its superolateral minor surface remodeling changes, primar- surface, which is resorptive, the cortical ily in regions just adjacent to sutures. In lining of the orbit faces these directions. the more complex cranial floor, however, a 364 HERMAN S. DUTERLOO AND DONALD H. ENLOW decreasing gradient of sutural growth takes face resorption are found in the frontal and place. This is accompanied by a much more prefrontal regions, the anteroventral part widespread occurrence of regional remodel- of the middle cranial fossa, variable por- ing which serves to expand the various en- tions of the floor in the occipital area, and docranial fossae, stabilize the passage of a prominent region surround the foramen vessels and nerves during skeletal growth, magnum. Thus, smaller and separate zones and to provide differential degrees of en- of resorption characterize the cranial floor largement among the different parts of the of the monkey while a continuous resorp- braincase on its ventral side. Because of tion-deposition interface occurs in the hu- differences in the proportions and rates of man cranium. It is noted, however, that growth in the cranial floor of Macaca as these are differences in relative extent rath- compared with Homo, corresponding dif- er than basic pattern, since the underlying ferences in respective remodeling patterns sequence of remodeling changes and the also occur. anatomical factors that predispose them The endocranial side of the human neu- are comparable. Because of differences in rocranium is characterized by a distinctive the proportions of the various parts of the circumcranial reversal lime that separates brain in these two species, related differ- the growth fields of the skull roof from ences in the extent of coverage by resorp- those in the floor (Enlow, '68a). This long tive and depository endocranial surfaces line completely encircles the cranium at a exist, even though the plan of remodeling level approximately midway across the in- itself is essentially similar. In the human ner aspect of the forehead and continues cranial floor, the cerebral lobes markedly around the lateral and posterior internal overhang the midventral cranial base, both walls of the skull. The meningeal surface anteroposteriorly and laterally. The floor of the bony cortex above this line is de- of the anterior cranial fossa (and the orbi- pository, while the surface below it is large- tal roof) is thereby situated much lower in ly resorptive in nature. This arrangement relation to the sphenoid than the more ele- is associated with differences in mode of vated and convex frontal floor in Macaca. growth in the two general areas, as out- The human forehead is proportionately lined above. In the monkey, a continuous larger, much higher, and it is more verti- circumcranial reversal line does not occur cally disposed. The floor of the middle cra- as such. Rather, a number of smaller but nial fossa of man is depressed in config- discontinuous resorptive regions are pres- uration, and the ectocranial petrous pyra- ent. Scattered patches of endocranial sur- mid is largely incorporated within its bony

Fig. 4 In these diagrams, key differences between man (right) and monkey (left) in the orientation of the cranial floor (b) and forehead (d) are schematized. The relative size and placement of the orbital region (c, shaded area) in relation to the size of the cranium is shown. Note the differences in the inclination of the foramen magnum (a) and the anterior cranial fossa (arrows), and the degree of flexure of the cranial base (b). CRANIAL GROWTH IN HOMO AND MACACA 365 cortex. This arrangement is in contrast to factors is directly related to a much more that found in the monkey. The human pos- extensive distribution of surface resorption terior cranial fossa is also much deeper as on the meningeal side of the bony cortex compared with the relatively flat occipital lining the human cranial floor as a whole. fossa of the monkey. It is suggested that This results in a differentially greater ex- the combination of these morphological tent of outward cortical drift (direct growth movement) of the bony plates involved, a process that accompanies the limited extent of growth expansion by sutures and synchondroses. These same remodeling differences, also, are apparently associated with the greater downward angulation of the cranial base flexure in man as compared with the monkey (fig. 4). This in turn is related to the more upright posture of the human skeletal frame and the verti- cal disposition of the facial complex. A number of close similarities as well as differences exist in the complex remodeling patterns of the orbit in these two primates (fig. 5). These patterns are associated with the comparative anatomical placement of the orbits and their enclosing rims in relation to the anterior cranial fossa above and behind each orbit as well as the protruding muzzle below and in front of them. As in most other regions of the craniofacial skeleton, the basic plan of remodeling is more or less comparable in both species. The medial (nasal) wall and the floor of the orbital cavity are depository in both species, and the lateral half of the inferior- anterior surface of the rim and the lacrimal Fig. 5 In the top diagram, the frontal cerebral lobes (shaded area) of man extend over the or- area are resorptive. The lateral half of the bits (heavy dashed line). The orbits are oriented cortical lining of the domed roof is also in a parallel fashion, and a diminished supra- resorptive, but the extent is proportionately orbital ridge grows slightly forward (dark stippled arrows). The anterior surface of the lateral orbi- much larger in the monkey and occupies tal rim, however, is resorptive and grows back- the entire length of the cavity. In man, this ward (white arrows). The lateral post-orbital resorptive field is restricted to the anterior surfaces are depository and grow laterally. These part located deep to the overhanging supra- multiple growth directions result in a flat, squared appearance of the whole region in the human orbital ridges. However, the essential simi- face. The growth of the comparable area in the larity in overall remodeling patterns pro- monkey differs (bottom diagram). The frontal duces growth movements that carry the hu- lobes of the cerebral hemispheres are much less man and monkey orbits in a predominantly bulbous, and the orbits have a laterally oblique orientation. In contrast to the human skull, note anterior and slightly lateral course. The that the anterior part of the monkey orbit is not overlying floor of the anterior cranial fossa covered by the frontal lobe. The supraorbital ridge moves in a corresponding direction, al- grows forward and laterally. The lateral orbital though the more restricted, upward-sloping ridges are depository on their anterior facing surfaces and resorptive (white arrows) on their pos- floor of the monkey does not descend to the terior facing side. The lateral orbital rim of the level that occurs in man. As a result, the monkey drifts laterally and anteriorly. The adja- orbits in the monkey lie anterior to an cent temporal region is resorptive. See text for a obliquely oriented frontal region, while in correlative discussion of relationships between these anatomical factors and the growth proc- the human skull they are situated almost esses associated with them. directly beneath the frontal area (see pre- 366 HERMAN S. DUTERLOO AND DONALD H. ENLOW

Fig. 6 Section through the occipital bone of Macaca mulatta, x 30. The meningeal surface (top) is resorptive from reversal R1 to R?. RI is the circumspinal reversal line on the rim of the foramen magnum. Rz is the internal (meningeal) occipital reversal line. Area A is composed of endosteally formed bone. Note the many replacement osteons and resorption spaces. Area B is lamellar bone deposited by the periosteum on the ventral (ectocranial) surface. In area C, periosteally formed bone has been laid down over a previously formed layer of endosteal bone. In man, the reversal line Rz is not present, but reversal line R1 characteristically occurs. Fig. 7 This section is a part of the posterior-facing cortex of the lateral orbital rim from a young growing monkey (x 30). The surface is resorptive from the left border of the picture to the reversal line (R). The comparable surface in man is depository. This difference contributes to the morphoge- netic basis for the anatomical differences in this area between the human and monkey skulls. See the text for descriptions. vious descriptions concerning correspond- extent of upward and forward rotation of ing differences in growth changes). This the upper human face in conjunction with situation, together with the circumstances the marked anterior positioning of the fore- in the following paragraph, appear to be head. As a result, the human lateral orbital directly related to the more prognathic fa- rim is distinctively upright as compared cial profile of Macaca in comparison with with the sloping nature of this region in the that of man. monkey. A distinct difference in the growth pat- The large resorptive region on the lat- tern of the external part of the protruding eral side of the monkey skull, within the lateral orbital rim occurs between these large temporal fossa and posterior to the two species. In the monkey, the anterolat- lateral orbital rim, is entirely absent in era1 surface is entirely depository, while a man. This is related to the much less mas- resorptive periosteal surface is characteris- sive development of the temporal lobe of tic in the human skull. The posterior-facing the monkey cerebrum, a feature which re- surface of the lateral orbital rim (within quires a medial direction of bone growth the temporal fossa) is resorptive in Macaca to adjust the position of the bony wall in but is depository in man. These differing response to the generalized ectocranial di- growth patterns are adapted to the greater rection of calvarial displacement. The tem- CRANIAL GROWTH IN HOMO AND MACACA 367 poral fossa in the monkey is, correspond- Enlow, D. H., and S. Bang 1965 Postnatal ingly, relatively large. Because of the more growth and remodeling of the human maxilla. prognathic facial contour in Macaca, the Amer. J. Orthodont., 51: 446-464. Gans, B. J., and B. G. Sarnat 1951 Sutural zygomatic arch is relatively long as com- facial growth of the Macaca rhesus monkey; pared with the arch in the proportionately a gross and serial roentgenographic study by shorter and more upright face of man. A means of metallic implants, Amer. J. Ortho- much wider temporal fossa, also, is a fea- dont., 37: 827-841. ture of the monkey skull related to his Massler, M., and I. Schour 1941 The growth pattern of the cranial vault in the albino rat more massive jaw musculature. as measured by vital staining with alizarin red S. Anat. Rec., 110: 83-101. LITERATURE CITED Moore, A. W. 1949 Head growth of the ma- Brodie, A. G. 1941 On the growth pattern of caque monkey as revealed by vital staining, the human head from the third month to the embedding and undecalcsed sectioning. Amer. eighth year of life. Am. J. Anat., 68: 209-262. J. Orthodont., 35: 654-671. DuBrul, E. L., and H. Sicher 1954 The Adaptive Moss, M. L. 1962 The functional matrix. In: Chin. Charles C Thomas, Springfield, Illinois. Vistas in Orthodontics. B. S. Kraus and R. A. Enlow, D. H. 1963 Principles of Bone Remodel- ing. Charles C Thomas, Springfield, Illinois. Riedel, eds. Lea and Febiger, Philadelphia, pp. 85-98. 1966 A comparative study of facial growth in Homo and Macaca. Am. J. Phys. Scott, J. H, 1967 Dento-facial development and Anthrop., 24: 293-308. growth. Pergamon Press Ltd., Oxford, England. 1968a The Human Face. An account of Vilmann, H. 1968 The growth of the parietal the postnatal growth and development of the bone in the albino rat studied by roentgen- craniofacial skeleton. Hoeber Medical Division, cephalometry and vital staining. Arch. Oral Harper and Row, New York. Biol., 13: 887-902. -- 1968b Wolffs law and the factor of Weidenreich, F. 1941 The brain and its role in architectonic circumstance. Amer. J. Orthodont., the phylogenetic transformation of the human 54: 803-822. skull. Trans. Amer. Phil. SOC.,31: 321-442. Enlow, D. H., and D. B. Harris 1964 A study of Weinmann, J. P., and H. Sicher 1955 Bone and the postnatal growth of the human mandible. Bones. Second edition. C. V. Mosby Co., St. Amer. J. Orthodont., 50: 25-50. Louis.