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Cerebral venous hemodynamics and the basicranium of Cebus.

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Cerebral Venous Hernodynamics and the Basicraniurn
of Cebus
Division of Biology and Medicine, Box G, Brown Uniuersity, Prouidence,
Rhode Island, 02912
KEY WORDS Cebus, Hemodynamics, Venous system,
Cranium, Comparative anatomy, Primates
The study of basicranial foramina has played an important role in
primatological investigations. They are often the only clues for deciphering cerebral vascular evolution in fossil forms. This study illustrates the significance of
considering foramina1shape when analyzing or describing basicranial anatomy in
living and fossil primates. It is suggested that certain hemodynamic properties of
cerebral venous drainage in Cebus represent patterns that were most likely
present in ancestral catarrhines.
The study of basicranial foramina has played
an important role in subjects ranging from
paleontology and systematics to neuroradiology and otolaryngology.Much of the long and
distinguished history of such studies in the
former disciplines has focused on the arterial
channels in the basicranium (e.g., Gregory, '20;
Guthrie, '63; Patterson, '65; Szalay, '75; Bugge,
'74; '78; Cartmill, '7.9, while those of the latter
are often concerned with the venous channels,
particularly the jugular foramen. For example,
radiologic features of the jugular foramen have
been used with some success to diagnose
tumors of the glomus jugulare, neuromas of
cranial nerves 9, 10, 11, and vascular malformations (see DiChiro et al., '64; Kraus et al.,
'75; Shapiro, '72).
In the primatological literature, the study of
emissary foramina has been mainly descriptive
in nature (e.g., Boyd, '30, '34) with very little
emphasis on the influence these foramina have
on venous hemodynamics. This is certainly the
case in studies of fossil primates as well.
The purpose of this report is to reevaluate
such descriptive studies of nonhuman primate
(and fossil)basicranial anatomy in terms of the
more dynamic interpretations of emissary
foramina in the human skull (e.g., Schelling,
'78). This study is intended as an illustration of
the utility of such a n approach in primate biology and not as a n exhaustive treatise on the
emissary foramina of Cebus.
The pattern of venous drainage from the
brain of man and his catarrhine relatives is
different from that found in many Lower Pri-
0092-948318015301-0037$01.400 1980 ALAN R. LISS, INC.
mates and most other mammals (Conroy, '80).
These pathways can often be accurately reconstructed from specific basicranial structures
preserved in the fossil record (e.g., Gazin, '651,
but their importance can only be understood by
investigating the dynamics of cerebral venous
flow in living primate models.
It has been customary in paleontology to
draw inferences about cerebral vascular patterns only from studies of the carotid arterial
pathways in the auditory bulla and middle ear
regions (however, for an excellent exception t o
this see Gazin, '65). It would be most helpful
and important for paleontologists to have other
lines of evidence in order to interpret cerebral
vascular evolution and a study of cerebral venous patterns and dynamics would provide
Cebus is an interesting primate to investigate since it combines primitive (large postglenoid foramen) and derived (enlarged right
jugular foramen) features in its patterns of cerebral venous flow. Many strepsirhines and
other mammals are also characterized by an
enlarged postglenoid foramen through which a
cranial dural sinus (petrosquamous sinus) continues as the external jugular vein (Padget, '57;
Dom et al., '70; Hegedus and Shackelford, '65;
Madiera and Watanabe, '73). In contrast, man
and his catarrhine relatives utilize the internal
jugular vein as the dominant cerebral venous
tract. At some time in primate evolution, this
transition from external to internal jugular
Received August 24, 1979; accepted December 4, 1979
dominance occurred and Cebus seems to represent a plausible “model” for studying this
transitional morphology.
The embryological development of the dural
sinuses and the emissary foramina they
traverse has been carefully documented by
Streeter (’15),Padget (’57),andButler (’57,’67).
Rathke (1838) was the first to emphasize the
importance of the external jugular vein in cerebral venous drainage of the embryo, and
Luschka (1862) named the foramen through
which it left the skull the “foramen jugulare
spurium.” This is the homologue of the “postglenoid foramen” of primate anatomy.
Thirty-six skulls of Cebus were chosen a t
random from the primate collections a t Brown
University. Of this total, 15were female and 12
were male (no data on sex was available for the
remainder). Three different species were included: C. apella, C. albifrons, and C .
capucinus. However, this initial project will not
consider comparisons between species or sexes.
Measurements were taken bilaterally on the
three most important emissary foramina of
each Cebus skull-jugular foramen, mastoid
foramen, and postglenoid foramen. Bilateral
measurements were taken so as to assess patterns of cerebral venous asymmetry.
For each foramen, the major and minor axis
diameters were recorded. The cross sectional
area for each foramen was calculated according
to the formula for the area of an ellipse, A = Tab
(A = area, a = major semi-axis diameter, b =
minor semi-axis diameter). The average cross
sectional area was calculated for each pair of
foramina (e.g., left and right jugular foramina)
and a Student’s t-test for the differencebetween
means of paired samples was calculated. The
values for P are based on one-sidedtests (unless
otherwise indicated) which reflect the particular nature of the hypotheses to be tested (see
Since the concern here is with the dynamics
of venous blood flow through these foramina,
some aspects of elementary hemodynamics
must be presented. Nonturbulent flow through
tubes is expressed by Poiseuille’s Law wherein
Q = d (pl-pz) / 8111.
In this equation Q = the quantity of flow
through a vessel (tube)per unit time; r = radius
of the vessel; p l = pressure at an upstream
point of the vessel; p2 = pressure a t a downstream point of the vessel; n = coefficient of
viscosity; 1 = length of the tube. This of course
means that volume flow is enhanced by any
factor which increases the numerator and is
diminished by any factor which increases the
denominator. As is evident from the formula,
volume flow is most affected by the radius of the
vessel since r is raised to the 4th power. For
example, a doubling of the radius of a vessel
will increase volume flow by a factor of 16!
The above equation is based on the ideal situation wherein the tube is circular in cross
section. The emissary foramina are rarely circular in cross section, however, being more
often elliptical in shape. This necessitates a
modification of Poiseuille’s Law to reflect volume flow through a tube of elliptical cross sectional shape:
7ra3bJ(pl-p2) / n (a2 + bA)41
All variables are as previously defined except
for r4which is now replaced by the term:
2(aJbJ/ aL+ b2)
In this case, a = major semi-axis and b = minor
semi-axis of the ellipse. This last equation (3)
will be referred to as the “cross sectional area
factor” (csaf)for volume blood flow through an
elliptical opening (Brecher, ’56). The average
csaf for volume flow was calculated bilaterally
for the three major emissary foramina.
Jugular foramen (pars vascularis)
The average cross sectional area for the left
jugular foramen is 2.52 nunLand for the right
jugular foramen 3.02mmL.The area of the
right jugular foramen is significantly larger
than the left, with a P value of 0.042 for a
one-sided test.
The csaf for determining volume blood flow
through the left jugular foramen is 0.703 mm4
and for the right jugular foramen 1.014 mm4
(Table 2 ) . Thus, while the average cross sectional area of the right jugular foramen is only
1.198 times that of the left one, the average
volume blood flow through the right foramen is
1.442 times as great.
Mastoid foramen
The average cross sectional area of the left
mastoid foramen is 1.66mmL.The right one
averages 1.45 mm2 (Table 1).A t-test for comparison of means of paired samples yields a
nonsignificant difference of P = 0.115-i.e., the
left mastoid foramen is not significantly larger
than the right one.
The average cross sectional area factor for
blood flow is 0.396 mm4 on the left and
0.353 mm4on the right. Thus, while the area of
TABLE 1 . Average cross sectional area (mrn')
Jugular f.
Mastoid f.
Postglenoid f.
Mastoid +
Right Two sided One sided
TABLE 2. Average cross sectional urea factor
(CSAF, rnrn4)
Jugular f.
Mastoid f.
Postglenoid f.
Mastoid +
Right T w o sided One sided
0.703 1.014 p=0.071
0.396 0.353
0.286 0.174
0.682 0.528
1.385 1.542
the left mastoid foramen is 1.14 times that of
the right on average, its contribution to volume
blood flow is 1.122 times as much.
Postglenoid foramen
The left postglenoid foramen averages
1.45 mm2and the right one averages 1.16 mm2
in cross sectional area. A t-test for comparison
of means of this paired sample yields a P value
for the one sided hypothesis of 0.010 indicating
the left foramen is significantly larger than the
right one.
The cross sectional area factor for the left
postglenoid is 0.286 mm4and for the right postglenoid 0.174 mm4. This is almost the mirror
image of the situation found in the jugular
foramina, in that the left cross sectional area
averages only 1.250 times that of the right, but
it also contributes 1.644 times as much to the
rate of blood flow.
At first glance, Cebus shows a similar venous
pattern to man (and presumably other catarrhines) in that the right jugular foramen is
significantly larger than the left (P = 0.042 for
a one-sided test) on average. This is probably a
derived feature for Higher Primates. In man,
this is due (at least in part) to the frequent
curving to the right of the posterior end of the
sagittal sinus and the resulting enlargement of
the right sigmoid sinus and internal jugular
vein. This cerebral venous asymmetry is well
known from anatomical and radiologic studies
(Frenckner, '40; Solter and Paljan, '73; Schelling, '78; DiChiro et al., '64; LeMay, '76). It is
interesting t o note in passing that some of the
australopithecines show peculiarities of venous
flow in this region (particularly Olduvai
Hominid 5) which are difficult to duplicate in
modern human crania (Tobias, '67).
This cerebral venous asymmetry is first
noted in the 20mm fetus (Streeter, '15) and
coincides with the development of a left-right
shunt between the anterior cardinal veins
draining the fetal head (Moore,'77). This anastomosis shunts blood from the left to the right
anterior cardinal vein and eventually develops
into the left brachiocephalic vein. The right
anterior cardinal and right common cardinal
veins become the superior vena cava. Undoubtedly then, a major factor of right sided jugular
dominance in anthropoids is due to the fact that
the right side becomes the shortest and most
direct route to the heart.
Another contributing factor might relate to
handedness, a topic explored recently by
LeMay ('76) and Hochberg and LeMay ('75).
However, if one looks closer a t the Cebus data,
it appears that the situation is not entirely
analogous to the catarrhine condition. While it
is true that the right jugular is significantly
larger than the left, it does not necessarily follow that the right side as a whole drains more
cerebral venous blood than the left side in this
The total average area for the three foramina
on the left side is 5.63 mm2and for the right side
5.63 111111'. This is obviously a nonsignificant
difference (P = 0.994 for a two-sided test). The
difference in the total cross sectional area factors for volume flow is 1.385 mm4 for the left
side and 1.542 mm4for the right side. This also
is not a significant difference.
Unlike the catarrhine condition, the dominance of the right jugular in Cebus is compensated for by the enlargement of the left mastoid
and postglenoid foramina. The average cross
sectional area for the left mastoid and postglenoid foramina is 3.11 mm2and for the right
foramina 2.61 mmz. For a one-sided test on the
difference of these paired sample means, P =
0.009, a significant difference with the left side
predominant. As can be seen from Table 2, the
cross sectional area factor is greater on the left
side for both the mastoid and postglenoid
It is evident from data summarized in Tables
1-2 and Figures 1-3 that the jugular veins are
Fig. 1. Histograms of frequencydistributionofleftand rightjugular foramen area andleft and right mastoid foramen area
= 36 and the arrow marks the mean value.
in mmz. In all figures N
Fig. 2. Histograms of frequency distribution of left and right postglenoid foramen area and left and right combined
mastoid and postglenoid foramen area.
Fig. 3. Histogram of frequency distribution of total area for emissary foramina (jugular, mastoid, postglenoid) on left and
right side.
still the singlemost significant ones for total
volume blood flow (left = 50.7% of total and
right = 65.7% of total). This statement must be
tempered by the knowledge that the vertebral
veins often play a dominant role in cerebral
drainage depending upon body posture (Eckenhoff, ’71; Epstein et al., ’70; Dilenge and
Perey, ’73).
The importance of considering cross sectional
area factors when describing basicranial
foramina is emphasized by noting that while
the average cross sectional area for the left
postglenoid and mastoid is larger than that of
the left jugular 3.11 mm2 vs. 2.52 mm’), the
average csaf of the latter is still higher
0.703 mm4 vs. 0.682 mm4).This is due to the
influence of foraminal shape on blood flow
rates. For example, volume flow through an
elliptical tube of the same cross sectional area
as a circular one will be reduced by over onehalc volume flow through an elliptical tube
with the same circumference as a circular one
will be reduced by about two-thirds; and volume flow through a n elliptical tube with the
same major semi-axis as the radius of a circular
one will be reduced by about four-fifths
(Brecher, ’56).
My observations indicate that the general
features of the emissary foramina outlined here
seem rather similar between Cebus and
Saimiri and distinguish these two genera from
most pitheciines and atelines. Thus, there is
nothing in the morphology of the cerebral venous system (as presently understood) to detract from Rosenberger’s (’77)basic conclusions
of ceboid phylogeny based on the dental and
cranial evidence.
It is tempting to speculate on whether or not
Cebus represents a “transitional” type of cerebral venous morphology through which
catarrhine ancestors may have passed. The
presence of a well developed right jugular associated with enlarged emissary foramina (particularly on the left side) leads me to suspect
that this is the case.
The importance of basicranial foramina in
primatological investigations is well known.
However, they have often been viewed from
purely a systematic, rather than functional,
perspective. This study illustrates the significance of foraminal shape in analyses of basicranial anatomy in living and fossil primates.
It is suggested that patterns of cerebral venous asymmetry seen inCebus might represent
a morphology that was present in ancestral
I am grateful to my colleague, Prof. G.E.
Erikson, for making his primate collections at
Brown University readily available. This research was funded by grants from the National
Science Foundation and Brown University.
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basicranial, venous, hemodynamics, cebus, cerebral
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