AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 53:37-42 (1980) Cerebral Venous Hernodynamics and the Basicraniurn of Cebus GLENN C. CONROY Division of Biology and Medicine, Box G, Brown Uniuersity, Prouidence, Rhode Island, 02912 KEY WORDS Cebus, Hemodynamics, Venous system, Cranium, Comparative anatomy, Primates ABSTRACT 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 this. 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 37 38 GLENN C. CONROY 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. MATERIALS AND METHODS 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 below). 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. (1) 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: Q = 7ra3bJ(pl-p2) / n (a2 + bA)41 (2) All variables are as previously defined except for r4which is now replaced by the term: 2(aJbJ/ aL+ b2) (3) 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. RESULTS 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 CEREBRAL VENOUS HEMODYNAMICS TABLE 1 . Average cross sectional area (mrn') Left Jugular f. Mastoid f. Postglenoid f. Mastoid + postglenoid Total Right Two sided One sided 2.52 1.66 1.45 3.02 1.45 1.16 p=0.083 0.230 0.019 p=0.042 0.115 0.010 3.11 5.63 2.61 5.63 0.018 0.994 0.009 0.497 TABLE 2. Average cross sectional urea factor (CSAF, rnrn4) Left Jugular f. Mastoid f. Postglenoid f. Mastoid + postglenoid Total Right T w o sided One sided 0.703 1.014 p=0.071 0.396 0.353 0.693 0.286 0.174 0.020 0.682 0.528 1.385 1.542 0.182 0.445 p=0.036 0.347 0.010 0.091 0.223 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. DISCUSSION 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 39 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 platyrrhine. 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 foramina. It is evident from data summarized in Tables 1-2 and Figures 1-3 that the jugular veins are L E F T JUGULAR 40 RIGHT JUGULAR 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 & RlGWT F Q S T O L L Y O I O Fig. 2. Histograms of frequency distribution of left and right postglenoid foramen area and left and right combined mastoid and postglenoid foramen area. T0T.L. RIGHT Fig. 3. Histogram of frequency distribution of total area for emissary foramina (jugular, mastoid, postglenoid) on left and right side. CEREBRAL VENOUS HEMODYNAMICS 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. 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