AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 86:75-80 (1991)
Effects of Age and Gender on the Location and Orientation of the Foramen Magnum in Rhesus Macaques (Macaca mulatta) ANNE V. MASTERS, DEAN FALK, AND TIMOTHY B. GAGE Department of Anthropology, State University of New York, Albany, New York 12222
KEY WORDS
Endocasts, Basicranium, Brainstem, Cranial capacity, Sexual dimorphism
ABSTRACT Endocasts from 378 rhesus macaque skulls from the Cay0 Santiago skeletal collection were measured to determine the effects of age and gender on the position and orientation of the foramen magnum. The foramen magnum migrates from a rostra1 to a caudal position and its angle changes during postnatal development. The angles and relative positions of the foramen magnum are similar for both genders of infants and for both genders of adults. However, analyses of linear response and plateau (LRP) functions reveal significant differences between males and females in the timing of reorientation of the angle and migration of the foramen magnum. The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. A similar pattern is observed for the brainstem region of the basicranium. Mean adult lengths of the brainstem region are reached a t 5.2 years in females and 7.1 years in males. The relationships between cranial capacity, the growth pattern of the brainstem, and the pattern of change for the angle and the relative position of the foramen magnum are examined. Quantification of the effects of age and gender on the location of the foramen magnum in a large sample of endocasts from one species of higher primate has potential implications for research on human development, and for interpretation of juvenile specimens in the hominid fossil record. Dart’s (1925) classic description of bipedalism in Taung (Australopithecus africanus) was based largely on his determination that the fossil’s foramen magnum was in a humanlike position relative to other primates, and the fact that posture and locomotion are related to this feature. Recent studies of australopithecine limb, digit, and pelvic features confirm t h a t australopithecines were bipedal for a t least some of the time, but the degree of bipedalism achieved in the earliest hominids remains controversial (Jungers, 1988; Lovejoy, 1988; Stern, 1983; Susman et al., 1985). Although the position of the foramen magnum in Taung does, indeed, fall between values for pongids and humans (Ashton and Zuckerman, 1956), the exact degree of affinity with the human position is in need of clarification a s emphasized by earlier workers (Keith, 1931).
@ 1991 WILEY-LISS, INC.
Ashton and Zuckerman (1956) show that the australopithecine foramen magnum is positioned more like gorillas than humans. More recently, Dean and Wood (1981) demonstrate differences in position of this feature between “robusts” and “graciles” and also describe the position of the foramen magnum in “robusts” as more anterior, relative to a bitympanic line, than in modern humans. Other workers discuss the position and orientation of the foramen magnum a s a factor involved in posture and locomotor behavior, but stress that a clear relationship between these phenomena is not yet established (Ashton and Zuckerman, 1956; Moore et al., 1973; Aiello and Dean, 1990). Further studies identify a pattern of posterior migraReceived July 5,1990; accepted March 27,1991
76
A.V. MASTERS ET AL.
tion of the foramen magnum with age in primates (including humans) (Ashton and Zuckerman, 1956; Bjork, 1955; Michejda, 1975). Recent evidence suggests that Taung was a child of approximately 3.5 years of age, that is, 1.5 to 2.5 years younger than previously believed (Bromage and Dean, 1985). Before using the Taung fossil or other juvenile hominids to extrapolate adult positions of the foramen magnum and its behavioral correlates, it is increasingly important to explore the interaction of age, posture, and locomotor style i n higher primates. The foramen magnum has been the focus of numerous primatological studies. Previous investigations include analyses of foramen magnum involvement in primate skull and brain development (Bolk, 1910; Lager, 1958; Radinsky, 1967; Michejda, 1971,1975), studies of the association of the primate basicranium with locomotor mode and postural features (Dart, 1925; Broom, 1938; Le Gros Clark, 19541, and the role of the foramen magnum in taxonomic assessment of fossilmaterials (Dean and Wood, 1981,1982; Luboga and Wood, 1990). The relationship between the position of the foramen magnum and degree of prognathism has also been investigated (Napier and Napier, 1967; Melson, 1974). Various additional aspects of the temporal and spatial parameters of the migration of the foramen magnum have previously been reported (Lager, 1958; Melson, 1971; Michejda, 1971, 1975; Michejda and Lamey, 1971; Sirianni and Van Ness, 1978). However, many of these studies are based on small numbers of specimens and frequently span a large number of species. The objective of the present study is to quantify the ageand gender-related temporal and spatial parameters of the migration and reorientation of the foramen magnum in a large sample of individuals representing one species of higher primate (M. mulatta). Increased understanding of the parameters of age- and gender-related changes in the position and orientation of the primate foramen magnum in a large sample will provide a n initial data base for assessing the significance of the position of the foramen magnum in other primates and early hominids (including Taung).
d Fig. 1. A aratus used for endocast measurement. The ad'ustagk bar was maintained in an orientation paralle! to the platform. The endocast was placed basal side up so that its sagittal suture is aligned with the center line (dashed)on the platform and its anterior (A) and posterior (B)fiducial points are equidistant from the adjustable bar.
collection. The endocasts were prepared by DF using procedures described elsewhere (Falk, 1978). Endocasts accurately reproduce details of external brain morphology including sulci, cranial sutures, brain shape, and vessels. The endocasts represent monkeys from 6 months to 273 months of age and include 189 females, 188 males, and 1 of unknown gender. Five measurements were collected from each endocast in order to document specific age- and gender-related changes in the foramen magnum: 4 of these measurements were taken with a sliding caliper, and 1with a protractor and a metal rod (2.25 mm diameter). Cranial capacities were determined by DF using standard procedures (Falk, 1976). Age-at-death (most known within two weeks) and gender were taken from Sade et al. (1985). The remaining variable (POSFM; see below) was developed for this study. The five endocast measurements were taken using a special apparatus (Fig. 1)designed to ensure consistency in data collection. Each endocast was placed basal surface up with its sagittal suture positioned on a line marked on a grid fixed to the platform of the apparatus. A movable wooden bar was MATERIALS AND METHODS fastened to two posts attached to the platMeasurements were taken from endocra- form at 90 degrees. The wooden bar was nial casts (endocasts) of 378 monkeys (M. positioned parallel to the platform, and a mulatta) from the Cay0 Santiago skeletal level was used to maintain its parallel orien-
77
FORAMEN MAGNUM OF MACAQUES
5. Projected hypophyseal fossa-basion: length of the line located in the sagittal plane between the basion (C) and posterior margin of the hypophyseal fossa (E) (Fig. 2). 6. Cranial capacity (cc). Cranial capacity is included a s a n indicator of brain growth to allow investigation of the relationship of the migration of the foramen magnum and changes in its orientation with increasing brain size. 7. Age a t death (mo.) 8. Gender: 0 = male; 1 = female. 9. POSFM: position of the foramen magnum relative to the length of the endocast (ie., the proportion of the length of the anteFig. 2. Diagram of measurements taken from en- rior endocast, from the anterior fiducial docasts. Measurements include angle 1and lines 2 , 3 , 4 , point to the midpoint of the foramen magand 5. Anterior (A) and posterior (B) fiducial oints, num, out of total length) computed as basion (0, opisthion (D), and hypophyseal fossa See text for definitions of measurements.
(8,.
tation. The endocast was then adjusted so that a plane parallel to the platform and the horizontal bar ran through the rostra1 junction of the frontal lobe and the olfactory bulb (A) and the basal edge of the junction of the sagittal and transverse sinuses (B) (Fig. 1). These anterior (A) and posterior (B) fiducial points were chosen to maintain consistency in orientation of all endocasts during data collection, Wedges of plasticine were used to hold the endocast firmly in place throughout data collection. Each endocast was partially filled with steel BB shot for stability. The nine variables used in this study are:
+
(proj. anterior-basion proj. anterior-opisthion)/2 length of endocast.
In order to determine measurement repeatability, all measurements were taken a second time on 15 endocasts. Remeasurement errors were determined and found to be less than .02 for all individual variables. The mean remeasurement error of all variables was .003. Examination of plots of the means for POSFM, the angle, and the length of the brainstem for age-at-death groups in one year intervals revealed that the changes in these variables are not constant throughout life but increase to a n upper asymptote. Following Konigsberg e t al. (1989), a linear response and plateau (LRP) function was chosen to model the development of these features. According to Konigsberg et al. (19891, this function can be stated a s
1. Angle of foramen magnum: the angle between the horizontal line and a metal rod positioned along the midline and across the rim of the foramen magnum. The value used is the average of two readings taken without repositioning (Fig. 2). 2 . Length of endocast: the shortest distance between the anterior fiducial point (A) y = A + aBt + (l-a)Bt,, and the posterior fiducial point (B) (Fig. 2 ) . a = 0 when t 2 t, and a = 1 when t < t,. 3. Projected anterior-basion: the shortest distance between the lines perpendicular to Feature development, a s measured, “begins the horizontal plane, one containing A and a t size A (t = 0 ) and increases linearly with the other containing the point representing age, a t rate B,” until development “ceases (at the interior margin of the anterior lip (C) of age t,).” After the age of growth cessation (t,) the foramen magnum (Fig. 2). the state of development is fixed at a pla4.Projected anterior-opisthion: the short- teau. Parameters which make up the funcest distance between the lines perpendicular tion are a n intercept (A), the slope (B), and to the horizontal plane, one containing A and the age of cessation of development (t,). A the other containing the interior margin of calculated value, A,,, represents the prethe posterior lip (D) of the foramen magnum dicted y-value a t the plateau ( = A + Bt,). (Fig. 2). A,, is a measure of adult size which is fully
78
A.V. MASTERS ET AL
TABLE 1. Results Feature
N
of
A
Piece- Wise regression’ Amax
tc
B
Relative position of foramen magnum (A and A,,, are proportions of total length; t, is in years. B is in proportional unitdyr.) 145 0.795 0.873 4.64* 0.0168 FemaIe Male 146 0.805 0.899 7.08* 0.0133 Brainstem (A and A,,, are in millimeters; t, is in years. B is in mm/yr.) Female 143 13.36 19.82 5.17* 1.25 Male 141 14.37 23.57 7.08* 1.30 Cranial capacity (A and A,,, are in cubic centimeters; tc is in years. B is in cc/yr.) Female 163 87.21 95.70 5.55* 1.53 Male 170 92.70 107.77 6.33* 2.38 Angle (A and A,,, are in degrees; t, is in years. B is in degreedyr.) Female 150 13.12 27.74 4.67* 3.13 Male 152 15.83 31.90 7.08* 2.27 lResults by gender of theLRP non-linear regression for the angle and relative position of the foramen magnum, the length of the brainstem area, and cranial capacity.A = positionofthe featureat thestart ofpostnatalgrowth; Amax = positionofthe featureatcessationofgrowth; t, = time of cessation of growth; R = rate of growth before t,. *Male and female values are significantly different: P < .05.
determined by the three estimated parameters in the LRP function. Since the LRP function is non-linear, ordinary least-squares regression methods cannot be used. The SPSSx NLR (non-linear regression) program was used to model the behavior of the angle and position of the foramen magnum, the length of the brainstem, and cranial capacity. RESULTS
Table 1lists the estimated values for A, t,, B, and the calculated value of A,, for the position and angle of the foramen magnum, for the brainstem area, and for cranial capacity. The angles and relative positions of the foramen magnum are similar for both genders of infants (A) and for both genders of adults (Amax).There are, however, significant differences between males and females in the timing (t,)of reorientation of the angle and migration of the foramen magnum (P < ,051.The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. This difference in timing is readily apparent in Figure 3, which presents the gender-specific LRP functions. Earlier development for females is also observed for the brainstem region of the basicranium and for cranial capacity. Mean adult lengths of the brainstem region are reached a t 5.2 years in females and 7.1 years in males. Mean adult cranial capacities are attained at 5.6 years in females and 6.3 years in males. Female and male values for the rate of
change (B) from infancy to maturity did not differ significantly for any variables. Table 2 provides the percent changes in these values from infancy to adulthood (=[BtJAl100%). A caudal shift in the position of the foramen magnum is observed for both females and males from infancy to adulthood. Females show a 9.8% caudal shift from 0.795 to 0.873. Males show a n 11.7% caudal shift from 0.805 to 0.899. The angle of the foramen magnum increased 111.4% (from 13.1 degrees to 27.7 degrees) for females and 101.5% (from 15.8 degrees to 31.9 degrees for males. A 48.4% increase for females (from 13.4 mm to 19.8 mm) and a 64.1% increase for males (from 14.4 mm to 23.6 mm) is noted for the length of the brainstem area. Cranial capacity increased 9.7% in females (from 87.2 cc to 95.7 cc) and 16.3% in males (from 92.7 cc to 107.8 cc) during this period. DISCUSSION
The percent increase in cranial capacity in M . mulatta appears comparable to the percent change in the position of the foramen magnum. Accurate interpretation of the relationships among the variables, however, requires a n allometric approach which is beyond the scope of the current study. The observed changes in the basicranium result from regional remodeling rather than from uniform growth of the skull (Baer, 1954; Duterloo and Enlow, 1970; Sirianni and Van Ness, 1978) and will be reported on a t a future time. The present study is limited to
Fi . 3. LRP functions fitted to the age-at-death distributions for males and females for PO&M (position of the foramen magnum). The LRP functions are similar for angle of the foramen magnum, cranial capacity, and the brainstem area.
TABLE 2. Percent change in variables from. infancy to a&Lthood
Variable Position of foramen magnum Angle Brainstem Cranial capacity
Females (%)
Males (%)
9.8 111.4 48.4
11.7 101.5 64.1
9.7
16.3
analysis of the timing of the completion of these changes in the skull. Females attain mature status in position and orientation of the foramen magnum approximately one year before their cranial capacities reach the mature state. The reverse pattern appears in males; they attain full cranial capacity earlier than they achieve mature status in position and orientation of the foramen magnum. Since the mature status of the position and orientation of the foramen magnum, or the rates of change of these features, are not significantly different for males and females, the differences are probably due to differential timing of adolescent growth spurts. Within each gender, the ages a t cessation of change in the position and angle of the foramen magnum are extremely close. This finding suggests that changes in the angle and position of the foramen magnum are linked to one process. The general increase in the length of the brainstem and the migration of the foramen magnum are consistent with studies that report elongation of the
clivus due to growth a t the spheno-occipital synchondrosis (e.g., Lager, 1958; Michejda, 1971,1971; Sirianni, 1985). That the elongation of the brainstem area continues past the age of cessation of change of the position and orientation of the foramen magnum for females, but not for males, again may be due to differential timing of growth processes and deserves further investigation. As shown in this study, the position of the foramen magnum shifts dramatically (i.e., approximately 10%) in a caudal direction during postnatal development of both male and female rhesus monkeys. Similar migration patterns have been suggested €or apes and, to a lesser degree, for humans (Ashton and Zuckerman, 1956). Future investigations of ape and human skulls may also reveal specific age- and gender-related patterns in the development of the basicranium. Such patterns would have important implications for the study of early hominids. For example, since Taung was perhaps 3.5 years of age a t death (Bromage and Dean, 19851,the position of the foramen magnum may not have achieved its adult status. This contradicts the assessment made by Dart (1925), who interpreted the position of the foramen magnum a s indicating bipedal locomotion in Australopithecus africanus. Age changes in habitual posture and locomotor style may be related to changes in the position and orientation of the foramen magnum. Michejda and Lamey (1971) observed "predominantly bipedal locomotion" among Macaca mulatta infants
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A.V. MASTERS ET AL.
whereas “juveniles were strictly quadrupedal.” Increased understanding of the relationship among these factors is important to future study of locomotor behavior in extinct (and extant) primates. Although age-related changes in locomotor behavior or position and orientation of the foramen magnum in Taung and its relatives have not been ascertained by the current study, it is our hope that this study will act a s a stimulus for future investigations of basicranial and locomotor development in pongids, humans, and early hominids. ACKNOWLEDGMENTS
This work was supported by NIH grant
R 0 1 NS24904 and we acknowledge the University of Puerto Rico for free access to the Cay0 Santiago skeletal collection. We thank Ben Morgan and Steve Merrill for their participation in this project. LITERATURE CITED Aiello L, and Dean C (1990) An Introduction to Human Evolutionary Anatomy. New York: Academic Press, p. 211. Ashton EH, and Zuckerman S (1956)Age changes in the position of the foramen magnum in hominids. Proc. Zool. SOC.Lond. 126:315-325. Baer MJ (1954) Patterns of growth of the skull as revealed by vital staining. Hum. Biol. 26:80-126. Bjork A (19551Cranial base development. Am. J. Ortho. 4It198-225. Bolk L (1910) On the slope of the foramen magnum in primates. Verk. Akad. Wet. Amst. 12:525-534. Broom R (19381 The Pleistocene anthropoid apes of South Africa. Nature 142:377-379. Bromage TG, and Dean MC (1985)Re-evaluation o f the age at death of immature fossil hominids. Nature 31 7:525-527. Dart RA (1925 Australopithecus afrzcanust the man-ape of South Africa. Natural History 115t195-199. Dean MC, and Wood BA (1981) Metrical analysis of the basicranium of extant hominoids and Australopzthecus. Am. J. Phys. Anthropol. 54t63-71. Dean MC, and Wood BA (1982)Basicranial anatomy of Plio-Pleistocene hominids from East and South Africa. Am. J. Phys. Anthropol. 59t157-174. Duterloo HS. and Enlow DH (1970)A comDarative studv of cranial growth In Homo and Macaca~Am J Anat 127 357-368 Falk D (1976)External Neuroanatomy of the Cercopithecoidea. Ph.D. thesis. Ann Arbor: University of Michigan Microfilms. Falk D (1978) External neuroanatomy of Old World
monkeys (Cercopithecoideai. Contributions to Primatol. 1 5 - 9 5 . Jungers WL (1988)Relative joint size and hominid locomotor adaptations with implications for the evolution o f hominid bipedalism. J. Hum. Evol. I7t247-265. Keith A (1931) New Discoveries Relating t o the Antiquity of Man. London: Williams and Norgate. Konigsberg LW, Falk D, Hildelbolt C, Cheverud J, Helmkamp RC, and Vannier M (1990)External brain morphology in rhesus macaques lMacaca rnuluttal. J. Hum. Evol. 19:269-284. Lager H (1958) A histological description of the cranial base in Macaca rhesus. Trans. Eur. Orthodont. SOC. 4:147-156. Le Gros Clark WE (1954)Reason and fallacy in the study of fossil man. Advanc. Sci. Lond. 43:l-13. Lovejoy CO (19881 Evolution of human walking. Sci. h e r . 258f1I i : 118-125. Luboga SA, and Wood BA (1990) Position and orientation o f the foramen magnum in higher primates. Am. J . Phys. Anthropol. 81:67-76. Melson €3 (19711The postnatal growth ofthe cranial base in Macaca rhesus analyzed by the implant method. Tandlaegebladet 75t1329. Melson B (19741The cranial base. Acta Odontol. Scand. 32:Suppl. 62. Michejda M (1971I Ontogenic changes of the cranial base in Macaca mulatta. Proc. Third Int. Congr. Primatol., Zurich 1970.1t215-225. Michejda M (1972) Significance of basicranial synchondroses in nonhuman primates and man. Proc. Third Conf. Exp. Med. Surg. Primates, Lyon 1972. Part 1, pp. 372-378. Michejda M (1975) Ontogenic growth changes of the skull base in four genera of nonhuman primates. Acta Anat. 91:110-117. Michejda M, and Lamey D (1971)Flexion and metric age changes of the cranial base in the Macaca mulatta. Infant and juveniles. Folia Primat. 34t133-141. Moore WJ, Adams LM, and Lavelle CLB (1973) Head posture in the Hominoidea. Zool., Lond. 169t409-416. Napier JR, and Napier PH (1967)A Handbook o f Living Primates. New York: Academic Press. Radinsky L (1967) Relative brain size: A new measure. Science 155:836-838. Sade DS, Chepko-Sade BD, Schneider JM, Roberts SS, and Richtsmeier J T (19851Basic Demographic Observations on Free-Ranging Rhesus Monkeys. New Haven, CT: Human Relations Area Files, Vol. 2. Sirianni J E (19851 Nonhuman primates as models for human craniofacial growth. In: Nonhuman Primate Models for Human Growth and Development. Monographs in Primatology 6,955124. SirianniJE, and Van Ness AL( 1978)Postnatal growth of the cranial base in Mucaca nemestrina. Am. J. Phys. Anthropol. 49t329-340. Stern JT (1983)The locomotor anatomy ofAustralopithecus afarensis. Am. J. Phys. Anthropol. 60:279-317. Susman RL, Stern JT, and Jungers WL (1985)Locomotor adaptations in the Hadar Hominids. In: E Delson, (ed.):Ancestors: The Hard Evidence. New York: Alan R. Liss, Inc., pp. 184-192.
Effects of Age and Gender on the Location and Orientation of the Foramen Magnum in Rhesus Macaques (Macaca mulatta) ANNE V. MASTERS, DEAN FALK, AND TIMOTHY B. GAGE Department of Anthropology, State University of New York, Albany, New York 12222
KEY WORDS
Endocasts, Basicranium, Brainstem, Cranial capacity, Sexual dimorphism
ABSTRACT Endocasts from 378 rhesus macaque skulls from the Cay0 Santiago skeletal collection were measured to determine the effects of age and gender on the position and orientation of the foramen magnum. The foramen magnum migrates from a rostra1 to a caudal position and its angle changes during postnatal development. The angles and relative positions of the foramen magnum are similar for both genders of infants and for both genders of adults. However, analyses of linear response and plateau (LRP) functions reveal significant differences between males and females in the timing of reorientation of the angle and migration of the foramen magnum. The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. A similar pattern is observed for the brainstem region of the basicranium. Mean adult lengths of the brainstem region are reached a t 5.2 years in females and 7.1 years in males. The relationships between cranial capacity, the growth pattern of the brainstem, and the pattern of change for the angle and the relative position of the foramen magnum are examined. Quantification of the effects of age and gender on the location of the foramen magnum in a large sample of endocasts from one species of higher primate has potential implications for research on human development, and for interpretation of juvenile specimens in the hominid fossil record. Dart’s (1925) classic description of bipedalism in Taung (Australopithecus africanus) was based largely on his determination that the fossil’s foramen magnum was in a humanlike position relative to other primates, and the fact that posture and locomotion are related to this feature. Recent studies of australopithecine limb, digit, and pelvic features confirm t h a t australopithecines were bipedal for a t least some of the time, but the degree of bipedalism achieved in the earliest hominids remains controversial (Jungers, 1988; Lovejoy, 1988; Stern, 1983; Susman et al., 1985). Although the position of the foramen magnum in Taung does, indeed, fall between values for pongids and humans (Ashton and Zuckerman, 1956), the exact degree of affinity with the human position is in need of clarification a s emphasized by earlier workers (Keith, 1931).
@ 1991 WILEY-LISS, INC.
Ashton and Zuckerman (1956) show that the australopithecine foramen magnum is positioned more like gorillas than humans. More recently, Dean and Wood (1981) demonstrate differences in position of this feature between “robusts” and “graciles” and also describe the position of the foramen magnum in “robusts” as more anterior, relative to a bitympanic line, than in modern humans. Other workers discuss the position and orientation of the foramen magnum a s a factor involved in posture and locomotor behavior, but stress that a clear relationship between these phenomena is not yet established (Ashton and Zuckerman, 1956; Moore et al., 1973; Aiello and Dean, 1990). Further studies identify a pattern of posterior migraReceived July 5,1990; accepted March 27,1991
76
A.V. MASTERS ET AL.
tion of the foramen magnum with age in primates (including humans) (Ashton and Zuckerman, 1956; Bjork, 1955; Michejda, 1975). Recent evidence suggests that Taung was a child of approximately 3.5 years of age, that is, 1.5 to 2.5 years younger than previously believed (Bromage and Dean, 1985). Before using the Taung fossil or other juvenile hominids to extrapolate adult positions of the foramen magnum and its behavioral correlates, it is increasingly important to explore the interaction of age, posture, and locomotor style i n higher primates. The foramen magnum has been the focus of numerous primatological studies. Previous investigations include analyses of foramen magnum involvement in primate skull and brain development (Bolk, 1910; Lager, 1958; Radinsky, 1967; Michejda, 1971,1975), studies of the association of the primate basicranium with locomotor mode and postural features (Dart, 1925; Broom, 1938; Le Gros Clark, 19541, and the role of the foramen magnum in taxonomic assessment of fossilmaterials (Dean and Wood, 1981,1982; Luboga and Wood, 1990). The relationship between the position of the foramen magnum and degree of prognathism has also been investigated (Napier and Napier, 1967; Melson, 1974). Various additional aspects of the temporal and spatial parameters of the migration of the foramen magnum have previously been reported (Lager, 1958; Melson, 1971; Michejda, 1971, 1975; Michejda and Lamey, 1971; Sirianni and Van Ness, 1978). However, many of these studies are based on small numbers of specimens and frequently span a large number of species. The objective of the present study is to quantify the ageand gender-related temporal and spatial parameters of the migration and reorientation of the foramen magnum in a large sample of individuals representing one species of higher primate (M. mulatta). Increased understanding of the parameters of age- and gender-related changes in the position and orientation of the primate foramen magnum in a large sample will provide a n initial data base for assessing the significance of the position of the foramen magnum in other primates and early hominids (including Taung).
d Fig. 1. A aratus used for endocast measurement. The ad'ustagk bar was maintained in an orientation paralle! to the platform. The endocast was placed basal side up so that its sagittal suture is aligned with the center line (dashed)on the platform and its anterior (A) and posterior (B)fiducial points are equidistant from the adjustable bar.
collection. The endocasts were prepared by DF using procedures described elsewhere (Falk, 1978). Endocasts accurately reproduce details of external brain morphology including sulci, cranial sutures, brain shape, and vessels. The endocasts represent monkeys from 6 months to 273 months of age and include 189 females, 188 males, and 1 of unknown gender. Five measurements were collected from each endocast in order to document specific age- and gender-related changes in the foramen magnum: 4 of these measurements were taken with a sliding caliper, and 1with a protractor and a metal rod (2.25 mm diameter). Cranial capacities were determined by DF using standard procedures (Falk, 1976). Age-at-death (most known within two weeks) and gender were taken from Sade et al. (1985). The remaining variable (POSFM; see below) was developed for this study. The five endocast measurements were taken using a special apparatus (Fig. 1)designed to ensure consistency in data collection. Each endocast was placed basal surface up with its sagittal suture positioned on a line marked on a grid fixed to the platform of the apparatus. A movable wooden bar was MATERIALS AND METHODS fastened to two posts attached to the platMeasurements were taken from endocra- form at 90 degrees. The wooden bar was nial casts (endocasts) of 378 monkeys (M. positioned parallel to the platform, and a mulatta) from the Cay0 Santiago skeletal level was used to maintain its parallel orien-
77
FORAMEN MAGNUM OF MACAQUES
5. Projected hypophyseal fossa-basion: length of the line located in the sagittal plane between the basion (C) and posterior margin of the hypophyseal fossa (E) (Fig. 2). 6. Cranial capacity (cc). Cranial capacity is included a s a n indicator of brain growth to allow investigation of the relationship of the migration of the foramen magnum and changes in its orientation with increasing brain size. 7. Age a t death (mo.) 8. Gender: 0 = male; 1 = female. 9. POSFM: position of the foramen magnum relative to the length of the endocast (ie., the proportion of the length of the anteFig. 2. Diagram of measurements taken from en- rior endocast, from the anterior fiducial docasts. Measurements include angle 1and lines 2 , 3 , 4 , point to the midpoint of the foramen magand 5. Anterior (A) and posterior (B) fiducial oints, num, out of total length) computed as basion (0, opisthion (D), and hypophyseal fossa See text for definitions of measurements.
(8,.
tation. The endocast was then adjusted so that a plane parallel to the platform and the horizontal bar ran through the rostra1 junction of the frontal lobe and the olfactory bulb (A) and the basal edge of the junction of the sagittal and transverse sinuses (B) (Fig. 1). These anterior (A) and posterior (B) fiducial points were chosen to maintain consistency in orientation of all endocasts during data collection, Wedges of plasticine were used to hold the endocast firmly in place throughout data collection. Each endocast was partially filled with steel BB shot for stability. The nine variables used in this study are:
+
(proj. anterior-basion proj. anterior-opisthion)/2 length of endocast.
In order to determine measurement repeatability, all measurements were taken a second time on 15 endocasts. Remeasurement errors were determined and found to be less than .02 for all individual variables. The mean remeasurement error of all variables was .003. Examination of plots of the means for POSFM, the angle, and the length of the brainstem for age-at-death groups in one year intervals revealed that the changes in these variables are not constant throughout life but increase to a n upper asymptote. Following Konigsberg e t al. (1989), a linear response and plateau (LRP) function was chosen to model the development of these features. According to Konigsberg et al. (19891, this function can be stated a s
1. Angle of foramen magnum: the angle between the horizontal line and a metal rod positioned along the midline and across the rim of the foramen magnum. The value used is the average of two readings taken without repositioning (Fig. 2). 2 . Length of endocast: the shortest distance between the anterior fiducial point (A) y = A + aBt + (l-a)Bt,, and the posterior fiducial point (B) (Fig. 2 ) . a = 0 when t 2 t, and a = 1 when t < t,. 3. Projected anterior-basion: the shortest distance between the lines perpendicular to Feature development, a s measured, “begins the horizontal plane, one containing A and a t size A (t = 0 ) and increases linearly with the other containing the point representing age, a t rate B,” until development “ceases (at the interior margin of the anterior lip (C) of age t,).” After the age of growth cessation (t,) the foramen magnum (Fig. 2). the state of development is fixed at a pla4.Projected anterior-opisthion: the short- teau. Parameters which make up the funcest distance between the lines perpendicular tion are a n intercept (A), the slope (B), and to the horizontal plane, one containing A and the age of cessation of development (t,). A the other containing the interior margin of calculated value, A,,, represents the prethe posterior lip (D) of the foramen magnum dicted y-value a t the plateau ( = A + Bt,). (Fig. 2). A,, is a measure of adult size which is fully
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A.V. MASTERS ET AL
TABLE 1. Results Feature
N
of
A
Piece- Wise regression’ Amax
tc
B
Relative position of foramen magnum (A and A,,, are proportions of total length; t, is in years. B is in proportional unitdyr.) 145 0.795 0.873 4.64* 0.0168 FemaIe Male 146 0.805 0.899 7.08* 0.0133 Brainstem (A and A,,, are in millimeters; t, is in years. B is in mm/yr.) Female 143 13.36 19.82 5.17* 1.25 Male 141 14.37 23.57 7.08* 1.30 Cranial capacity (A and A,,, are in cubic centimeters; tc is in years. B is in cc/yr.) Female 163 87.21 95.70 5.55* 1.53 Male 170 92.70 107.77 6.33* 2.38 Angle (A and A,,, are in degrees; t, is in years. B is in degreedyr.) Female 150 13.12 27.74 4.67* 3.13 Male 152 15.83 31.90 7.08* 2.27 lResults by gender of theLRP non-linear regression for the angle and relative position of the foramen magnum, the length of the brainstem area, and cranial capacity.A = positionofthe featureat thestart ofpostnatalgrowth; Amax = positionofthe featureatcessationofgrowth; t, = time of cessation of growth; R = rate of growth before t,. *Male and female values are significantly different: P < .05.
determined by the three estimated parameters in the LRP function. Since the LRP function is non-linear, ordinary least-squares regression methods cannot be used. The SPSSx NLR (non-linear regression) program was used to model the behavior of the angle and position of the foramen magnum, the length of the brainstem, and cranial capacity. RESULTS
Table 1lists the estimated values for A, t,, B, and the calculated value of A,, for the position and angle of the foramen magnum, for the brainstem area, and for cranial capacity. The angles and relative positions of the foramen magnum are similar for both genders of infants (A) and for both genders of adults (Amax).There are, however, significant differences between males and females in the timing (t,)of reorientation of the angle and migration of the foramen magnum (P < ,051.The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. This difference in timing is readily apparent in Figure 3, which presents the gender-specific LRP functions. Earlier development for females is also observed for the brainstem region of the basicranium and for cranial capacity. Mean adult lengths of the brainstem region are reached a t 5.2 years in females and 7.1 years in males. Mean adult cranial capacities are attained at 5.6 years in females and 6.3 years in males. Female and male values for the rate of
change (B) from infancy to maturity did not differ significantly for any variables. Table 2 provides the percent changes in these values from infancy to adulthood (=[BtJAl100%). A caudal shift in the position of the foramen magnum is observed for both females and males from infancy to adulthood. Females show a 9.8% caudal shift from 0.795 to 0.873. Males show a n 11.7% caudal shift from 0.805 to 0.899. The angle of the foramen magnum increased 111.4% (from 13.1 degrees to 27.7 degrees) for females and 101.5% (from 15.8 degrees to 31.9 degrees for males. A 48.4% increase for females (from 13.4 mm to 19.8 mm) and a 64.1% increase for males (from 14.4 mm to 23.6 mm) is noted for the length of the brainstem area. Cranial capacity increased 9.7% in females (from 87.2 cc to 95.7 cc) and 16.3% in males (from 92.7 cc to 107.8 cc) during this period. DISCUSSION
The percent increase in cranial capacity in M . mulatta appears comparable to the percent change in the position of the foramen magnum. Accurate interpretation of the relationships among the variables, however, requires a n allometric approach which is beyond the scope of the current study. The observed changes in the basicranium result from regional remodeling rather than from uniform growth of the skull (Baer, 1954; Duterloo and Enlow, 1970; Sirianni and Van Ness, 1978) and will be reported on a t a future time. The present study is limited to
Fi . 3. LRP functions fitted to the age-at-death distributions for males and females for PO&M (position of the foramen magnum). The LRP functions are similar for angle of the foramen magnum, cranial capacity, and the brainstem area.
TABLE 2. Percent change in variables from. infancy to a&Lthood
Variable Position of foramen magnum Angle Brainstem Cranial capacity
Females (%)
Males (%)
9.8 111.4 48.4
11.7 101.5 64.1
9.7
16.3
analysis of the timing of the completion of these changes in the skull. Females attain mature status in position and orientation of the foramen magnum approximately one year before their cranial capacities reach the mature state. The reverse pattern appears in males; they attain full cranial capacity earlier than they achieve mature status in position and orientation of the foramen magnum. Since the mature status of the position and orientation of the foramen magnum, or the rates of change of these features, are not significantly different for males and females, the differences are probably due to differential timing of adolescent growth spurts. Within each gender, the ages a t cessation of change in the position and angle of the foramen magnum are extremely close. This finding suggests that changes in the angle and position of the foramen magnum are linked to one process. The general increase in the length of the brainstem and the migration of the foramen magnum are consistent with studies that report elongation of the
clivus due to growth a t the spheno-occipital synchondrosis (e.g., Lager, 1958; Michejda, 1971,1971; Sirianni, 1985). That the elongation of the brainstem area continues past the age of cessation of change of the position and orientation of the foramen magnum for females, but not for males, again may be due to differential timing of growth processes and deserves further investigation. As shown in this study, the position of the foramen magnum shifts dramatically (i.e., approximately 10%) in a caudal direction during postnatal development of both male and female rhesus monkeys. Similar migration patterns have been suggested €or apes and, to a lesser degree, for humans (Ashton and Zuckerman, 1956). Future investigations of ape and human skulls may also reveal specific age- and gender-related patterns in the development of the basicranium. Such patterns would have important implications for the study of early hominids. For example, since Taung was perhaps 3.5 years of age a t death (Bromage and Dean, 19851,the position of the foramen magnum may not have achieved its adult status. This contradicts the assessment made by Dart (1925), who interpreted the position of the foramen magnum a s indicating bipedal locomotion in Australopithecus africanus. Age changes in habitual posture and locomotor style may be related to changes in the position and orientation of the foramen magnum. Michejda and Lamey (1971) observed "predominantly bipedal locomotion" among Macaca mulatta infants
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whereas “juveniles were strictly quadrupedal.” Increased understanding of the relationship among these factors is important to future study of locomotor behavior in extinct (and extant) primates. Although age-related changes in locomotor behavior or position and orientation of the foramen magnum in Taung and its relatives have not been ascertained by the current study, it is our hope that this study will act a s a stimulus for future investigations of basicranial and locomotor development in pongids, humans, and early hominids. ACKNOWLEDGMENTS
This work was supported by NIH grant
R 0 1 NS24904 and we acknowledge the University of Puerto Rico for free access to the Cay0 Santiago skeletal collection. We thank Ben Morgan and Steve Merrill for their participation in this project. LITERATURE CITED Aiello L, and Dean C (1990) An Introduction to Human Evolutionary Anatomy. New York: Academic Press, p. 211. Ashton EH, and Zuckerman S (1956)Age changes in the position of the foramen magnum in hominids. Proc. Zool. SOC.Lond. 126:315-325. Baer MJ (1954) Patterns of growth of the skull as revealed by vital staining. Hum. Biol. 26:80-126. Bjork A (19551Cranial base development. Am. J. Ortho. 4It198-225. Bolk L (1910) On the slope of the foramen magnum in primates. Verk. Akad. Wet. Amst. 12:525-534. Broom R (19381 The Pleistocene anthropoid apes of South Africa. Nature 142:377-379. Bromage TG, and Dean MC (1985)Re-evaluation o f the age at death of immature fossil hominids. Nature 31 7:525-527. Dart RA (1925 Australopithecus afrzcanust the man-ape of South Africa. Natural History 115t195-199. Dean MC, and Wood BA (1981) Metrical analysis of the basicranium of extant hominoids and Australopzthecus. Am. J. Phys. Anthropol. 54t63-71. Dean MC, and Wood BA (1982)Basicranial anatomy of Plio-Pleistocene hominids from East and South Africa. Am. J. Phys. Anthropol. 59t157-174. Duterloo HS. and Enlow DH (1970)A comDarative studv of cranial growth In Homo and Macaca~Am J Anat 127 357-368 Falk D (1976)External Neuroanatomy of the Cercopithecoidea. Ph.D. thesis. Ann Arbor: University of Michigan Microfilms. Falk D (1978) External neuroanatomy of Old World
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