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Effects of age and gender on the location and orientation of the foramen magnum in rhesus macaques (Macaca mulatta).

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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
80
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.
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