Acta Palaeontologica Polonica

Vol. 28, No. 1-2 pp. 281-293 Warszawa, 1983

Second S ymposium on Mesozoic Terrestiai Ecosystems, Jadwisin 1981

JOHN R. WIBLE

TH E INTE RNAL CAROTID ARTERY IN EARLY EUTHERIANS

WI BLE, J . R. : The in tern al carotid artery in ea r ly euther ians. Ac ta Pal aeont .Po lo nica , 28, 1-2, 281-293, 1983.

Althoug h evi dence fro m co m parative anatomy an d em bry ology shows th at on lyone Internal carotid artery is present am ong extant eutherians, numerous earlyeutherians h ave two vascula r-li ke grooves on the pet rosal suggesting the presenceof two separate internal ca roti ds. It is argued he re th a t th e most accep ta blemodel for th e interpretation of this m orphology pl aces the single in ternal carotidin the la te ral groove and a venous channel (infe rior p etrosal sinus) in the media lon e. This lat eral course fo r t he in ternal carot id arte ry is n ot necess aril y primi­ti ve for Eutheria , only widespread amo ng early gr ou ps. The earliest knowneut hc r ia n basicrania have only a med ial groove and ther efore, a media l co urseto the interna l ca r otid. However, based on ontogenetic r esearch, this media lco urse in the ea rliest known eutheria ns was m os t likely no t iden ti ca l with th emedial course in non-euth erian m ammals.

K e y w 0 r d s : internal ca r otid artery, ba sicrania, ea rl y eu t her ians, pet ro sal ,infer ior petrosal si nus.

J ohn R. Wible, Departm en t of A n at omy , Duk e Un iversity Medical Center, Durham,N.C. 27710, U SA . Rec eived: September 1981.

INTRODUCTION

In a report on the middle Eocene fauna from the Bridger Basin ofWyoming, Matthew (1909) proposed that three separate longitudinal ar­teries - separate lateral and medial in ter nal carotids, plus the stapedialartery - were present in the tympanic r egion of the carnivore-insectivoreancestor (fig. 1). The presence of three grooves running across the tym­panic region in the Bridger miacids led Matthew to this conclusion. Onegroove ran medially around the promontorium of the petrosal, like thecourse of the internal carotid artery in extant carnivores. A second groovetravelled across the promontorium, like the internal carotid of extantinsectivores. Finally, a third groove ran laterally from the second grooveto the fenestra vestibuli, like the course of the stapedial artery in mo­dern insectivores. Of these three ancestral arteries, Matthew proposed,extant insect ivores presumably retain only the two lateral vessels, whileextant carnivores presumably retain the medial one. Therefore, underthis scheme the internal carotid artery of extant carnivores with its me-

282 JOHN R. WIBLE

mica

icaFig. 1. A schema tic re presenta tion of Ma tthew's model for the internal caroti dsyste m in the ca rnivore- insectivore ancesto r . A left petrosal bone is shown in ventralas pec t with a medial gr oov e and internal ca rotid artery (m i ca) , a lateral groov e andinternal ca rotid artery (pica) and a sta pe dia l groove and artery (sa). Presumablyboth the med ial and lateral internal ca roti ds supply the brain, while the stapedialar tery divides into a superior ramus (sr) feeding the dura and orbit and an inferior

ra mus (i r ) feed ing the upper and lower jaws. Abbrev iations as on page: 291.

dial course is not the homologue of the laterally placed internal carotidartery of extant insectivores.

In recent ye ars a number of researchers (McKenna 1966; Van Valen1966; Szalay 1972, 1975; Arch iba ld 1977; Bugge 1978, 1979) have adoptedMatthew 's scheme as the model of the primitive eutherian internal carotidsystem. The terms medial internal carotid artery and promontory arteryhave been coined to distin guish the two carotids of Matthew's scheme.Support for this model lies in the widespread occurrence of "miacid- like"tympanic morphologies among diverse late Cretaceous-early Tertiary eu­therian gr oups (Table 1).

Table 1

Late Cr etaceous-early Tertiary eutherian groups exhibiting a morphologyconsistent with Matthew's "two-car otid" scheme 1)

" Bug Creek Petrosals "Pa l aeo ryctesLeptictidaeHyaen od ontidaeCarnivoraOxyaenidaeArtiodactyla

. Arctocyonid aeCondylarthraRod en tia

-- MacIntyre 1972-- Van Valen 1966, McK enna 1966-- Butler 1956 , McKenna 1966-- Piveteau 1935-- Matthew 1909-- Matthew 1909-- Whitmore 1953, Dechaseaux 1974-- Ru ssell 1964-- Russell 1964, Gazin 1965-- Lavocat 1967, Wahlert 1974, Parent 1980,

1) This morphology is most of ten present in the form of vascularlike grooveson the pet ro sal bone. In so me cases, for ins tance, Palaeoryctes, the presence of anartery is inferred from fo ramin a alone.

EARLY EUTHERIAN INTERNAL CAROTID ARTERY 283

Three recent articles raise serious questions about the validity of thedistinction between the medial internal carotid and promontory arteriesmade by Matthew's scheme. Cartmill and MacPhee (1980) suggest thatthese two vessels may be homologues differing only in their positionsrelative to the promontorium. Providing support for this, Presley (1979)shows that embryologically the mammalian internal carotid is alwaysa derivative of the dorsal aorta and that its medial or promontorial po­sition can be intetpreted as a mere result of differential growth rates inthe surrounding chondrocraniaI ' elements. MacPhee (1981) notes that theinternal carotid artery in living eutherians occupies a range of positionsfrom near the midline to the lateral side of the promontorium (d. Wer­ner 1960; Wible 19~0). Further, in its course, this vessel is always accom­panied by the internal carotid nerve, a significant point considering thevery conservative nature of nerve pathways. This combined with otherevidence from comparative anatomy suggests to MacPhee that there is,in homological terms, only one internal carotid artery with variant path­ways.

According to the comparative anatomical and embryological evidence,the medial internal carotid and promontory arteries are merely two cha­racter states of the eutherian internal carotid artery. Yet, if one acceptsthe existence of a single eutherian artery, the problem of the two "in­ternal carotid" grooves in the fossil basicrania is left unanswered. If onlya single internal carotid artery could have been present in these earlyeutherians, in addition to the stapedial artery, then which groove did theinternal carotid occupy and what occupied the other groove?

MORPHOLOGICAL ALTERNATIVES

With the rejection of Matthew's "two-carotid" model, two plausibleinterpretations of the "miacid-like" basicranial morphology remain: (1) amedial; or (2) a lateral (or promontorial) course for the single internal ca­rotid artery. Both of these alternatives have been suggested to accountfor the morphology in particular fossils. However, a careful evaluationshows that ,one of these alternatives offers a more acceptable model.

(1) A medial course: In his description of Meniscotherium, an earlyEocene condylarth, Gazin (1965) placed the internal carotid artery in themedial groove and branches of the tympanic nerve plexus in the lateral(or promontorial) one. However, evidence from comparative anatomyshows that this is an unlikely interpretation. The lateral groove in Me­niscotherium and other ,early eutherians runs forward toward the apexof the petrosal anteromedially across the promontorium, while the tym­panic nerve and its rostral continua ion, the lesser petrosal nerve, follow

284 JOHN R. WIBLE

a more lateral course across the promontorium forward to the foramenovale (MacPhee 1977, 1981; personal observations). Also, the tympanicnerve rarely leaves any bony trace in living eutherians and then, certainlynot of a broad vascular-like var iety (personal observations).

The problem with any model calling for a medial course to the in­ternal carotid artery in the "miacid- like" basicrania is in filling the la­teral groove. When a lateral groove is present in extant eutherians, itnormally contains an internal carotid artery (promontorial character state).There is onl y one structure besides an internal carotid artery that hasbe en found by itself in a lateral groove in extant euthe rians; this is theinternal carotid nerve (Conroy and Wible 1978). However, the internalcarotid ar te r y in-this animal, Lemur variegatus , was lacking; in otherspecimens of this same sp ecies, the internal carotid artery has been foundin the lateral gr oove (Tandler 1899). It is highly unlikely that the ear lyeuther ian internal carotid artery was in the medial groove and the inter­nal carotid nerve in the lateral one , since these two structures travel to­gether in living eutherians.

It appears that a medially placed internal carotid artery is an un­likely alter na tive for ear ly eutherians possessing a lateral .groove. How­ever, ther e is another possibility that must be considered; the lateralgroove may have contained a structure not found among living mammals.Such a structure is a collateral arterial branch, that is, an artery runningcollaterally to the medially placed internal carotid (d. Presley 1979; Pa­rent 1980). Although this possibility cannot be ruled out entirely, it isnot necessary to rely on the formation of a de novo collateral artery whenthe following model can fill the fossil morphology with structures knownto occur in extant eutherians. •

(2) A lateral course: Whitmore (1953) suggested that the inferior pe­trosal sinus ran in the medial groove and that the internal carotid arteryran across the promontorium in Merycoidon culbertsonii, a White RiverOligocene artiodactyl. In addition, Butler (1956), Lavocat (1967) and Wah­lert (1974) have offered the inferior petrosal sinus as an alternative tothe medial internal carotid artery in their interpretations of the basicra­nial morphology in particular fossils. This model (fig. 2) fills the lateralgroove with the only structure known to run in the lateral groove inextant eutherians: an internal carotid artery (promontorial characterstate). Also, based on its morphology in extant forms , the inferior pe­trosal sinus is a plausible occupant of the "miacid-like" medial groove.

Among extant eutherians, there are three different pathways followedby venous channels running medial to the promontorium. This is bestunderstood in terms of the . ontogeny of this region. In the chondrocra­nium of an eutherian embryo (fig . 3), the cochlear capsule (a precursor ofthe petrosal bone) and parachordal plate (the future basioccipital in thisregion) are separated by the basicapsular fe nestr a and joined by anterior

E A RLY E U THER I A N INTERNAL CAROTID A R TERY 285

ips

. icaFig. 2. Th e interpretation of the early eutherian "miacid-like" basicranial morpho­logy accepted here. The single internal carotid artery (promontorial character state)occupies the lateral groove, while an inferior petrosal sinus runs medial to the pro-

. montor ium. Abbreviations as on page: 291.

a b c

Fig 3. Schematic representations of thr ee left tympanic regions of an idealized eu­therian chondrocranium in ventral aspect (modified af ter MacPhee 1981), showingthe three pathways f or the embry onic medial venous channel: a an extracranialcourse ; b a course through the basicapsular f enestra; c an intracranial course. Ter­minology for the venous channel is as in the adult. The regular stipple indicates

membrane bone. Abbreviations as on page: 291.

and posterior basicapsular commissures. 2) A complex system of venous

channels connecting the ·in ter nal jugular vein and cavernous sinus runsthrough this region. Three possible pathways, .occurr ing singly or in com­bination, have been found in embryos studied to date: (1) an extracranialcourse (ventral to both commissures and through the carotid foramen)(fig. 3a); (2) a course through the basicapsular fenestr a (ventral to theposter ior commissure and dorsal to the anterior one) (fig . 3b) ; and (3) an,

2) See Beer (1937) fo r variations on this morphology in eutherian chondrocrania.

286 JOHN R. WIBLE

intracranial course (dorsal to both commissures) (fig. 3c). These sa methree pathways are . found among adult euthe r ians : (1) an extracranialmedial vein enterin g the cranial cavity via the carotid foramen , as inCanis famili aris (Miller et al. 1964); (2) an inferior petrosal sinus runn­ing through the patent basicap sular fenestra, as in Tupaia (MacP hee1981), sor icomorph insec tivores (McDowell 1958; MacPhee 1981) and me­gachi ropterans (per sonal obser va tions ); and (3) an intracranial inf eriorpetrosal sinus , as in Canis familiaris (Miller et al. 1964) and Hom o. It isnot clear whi ch of these pa thways r epresents the primitive state for Eu­theria , but as is shown below, this is not essen tial for interpreting thefoss il morphology.

These three pathways for the medial venous channel may accountfor the variable morphologies of the medial gr oove in the fossil ba sicr ania.In some fossils , for instance, Meniscotherium (Gazin 1965) and V iver­rav us minutus (Matthew 1909), the ' medi al gr oov e is merely an openchanne l between the basioccipital and petrosal. This medial groove mayhave contained an extracranial medial vein as in Cmtis familiaris. Inothe r fossils , for instance, Pl euraspuiotheriumi aumoni eri (Russell 1964),A rct ocyonides arenae (Russell 1964) and Dich obune leporina (Dechaseaux1974), the med ial groove actually leads to a patent basicapsular fenestra(personal observations) ; this str ucture has been mistakenly identifiedas a pos terior carotid foramen in these forms. An inferior petrosal sinusas present in sor icomor ph ins ectivores may have passed through this open­in g. 3

) F in ally , in other fossils, like Vulpavus ovatus (Matthew 1909 ; per­sonal observati ons), the medial groove is actually a closed canal betweenthe basioccipit al and petrosal ; this may have given passage to an inferiorpetrosal sinus as in Hom o. It is inte rest ing that of these three medial"groove " morphologies 4) , only one, the ope n channel between the petrosaland basioccipital, gives passage to an internal carotid artery among livingeu the r ians, wh ile all three are known to give pa ssage to a ve nousch annel.

Although a venous channel fits the medial "grove" morphology inthe fossil basicrania, anot he r possibility must be considered here. Themedial "gr oove" may have (also?) contained an artery running collate­rally to the laterally plac ed internal carotid artery (cf. Presley 1979; Pa­rent 1980). The ascending pharyngeal ar ter y follows a somewhat analogouspathway in some extant eutherians (cf. Daniel et al. 1953; Cartmill 1975)and was likely present in early eutherians (MacPhee 1981). However, it is

3) However, a patent basica psula r fen estra is found in various adult ex ta n teu the r ians, for in stance microchiropterans, with ou t transmitting any struc tu re s(personal obse rva tions ).

4) Th ere is in fa ct a fou rth morphology ex hibited by th e isola ted petro salsfrom the late Cretaceous Bug Creek Anthills of Montana. These fossil s a ppare n tl yhave two medial gr ooves (MacIntyre 1972). This morphology may have h oused twoven ou s chan ne ls as in Canis. However, the interpretation of these fos sil s awaitsfurther st udy.

EARLY EUTHERIAN INTERNAL CAROTID ARTERY 287

argued here that this vessel was an unlikely occupant of the medial"gr oove" in the fossils. First of all, the course of the ascending pharyngealar te ry, like that of a medially placed internal carotid, cannot account forthe three different medial "groove" morphologies found in ea r ly euth­erians. Th e ascending pharyngeal artery in extant forms always followsan extracranial course. Therefore, of the three different medial "gr oove"morphologies , only an open groove between the basioccipital and petrosalcould have housed an ascending pharyngeal artery. Further, when theascendin g pharyngeal artery runs med ial to the auditory bulla in extanteuthe r ians , it does not run in a groo ve between the basioccipital andpetrosal. Its course is more superficial al ong the medial bullar wall andnot in the area of the ba sioccipital-petro sal junct ion (personal observa ­tions). Althoug h the ascending pharyngeal artery was likely a pa r t of theprimitive euthe rian carotid system , its course among extant forms makesit an unlikely choice for the medial "groove".

THE P R I MIT IVE COURSE OF THE EUTHERIAN INTERNAL CAROTID A RTERY

Based on the above, it seems most likely that the internal carotidartery occupied the lateral groove in the "miacid-like" basicrania andthat a ve nous channel ran medial to the promontorium. This does notnecessarily imply that a lateral course for the internal carotid arteryis primitive for Eutheria, only that it was widespread among ear ly groups(see Table 1). In fact , the earliest known eutherian basicrania, K ennalest es,As ioryctes and Barunlest es from the late Cretaceous of Asia (Ki elan-Ja­worowska 1981 ; Kielan-Jaworowska and Trofimov 1980) , lack a lateralgroove. With the presence of a groove medial to the promontorium inK ennalestes and Asioryct es, Kielan-Jaworowska (1981:58) suggests thatan inter nal carotid artery "as characteristic of marsupials" was present.However, this cannot be determined fr om the fossil evidence. In marsupi­als, the internal carotid artery runs medial to the auditory bulla (Tandler1899 ; Ar che r 1976) ; K ennalest es, Asioryctes and most ea r ly euthe r ianslack bony bullae and likely had only membranous bullae as adults (No­vacek i 977; Archibald 1977 ; MacPhee 1981). Although the presence ofa med ial groove (and th e absence of a lateral one) in K ennalest es andAsioryctes suggests a .medial course for the internal carotid artery, itdoes not show the relationship between that vessel and a membranousaudi tory bulla . However, such a membranous covering is present inmammalian embryos as the precursor of the auditory bulla (MacPhee1977, 1981) and so, ontogeny provides a possible model for the fossilmorphology.

In mammalian embryos, the developing auditory bulla makes it sfirst appe arance in the form of a connective tissue membrane, the fibrous

288 JOHN R. WIBLE

membrane of the tym pa nic cavity or FMTC of MacP hee (1977, 1981).The embryonic internal carotid ~tery follows one of three possiblecourses with r espect to this membrane (fig. 4): (1) medial to the FMTC(and therefore, outside of the tympanic cavity); (2) within the substanceof the FMTC; and (3) lateral to the FMTC (and so , within the tympanic

a

cc

..

.m l".mml1'10<

0 \ica .

......

·....·.....FMTC

b

.........

c

....

Fig. 4. Schematic representations of transverse sections through the tympanic regionof three mammalian ernbroys, showin g the relationship between. the internal ca roti dartery and FMTC, the precursor of the auditory bulla: (1 the internal ca rotid runsmedial to the FMTC ; b the internal carotid runs through the substance of theFMTC; c t he internal carot id runs lateral to the FMTC. Note t ha t in c, t he internalca rotid can oocupy a range of positions from the medial to the lateral side of the

cochlea r capsule . Abbreviations as on page: 291.

Table 2

MonotremataMarsupialiaEdentataMacroscelideaLagomorphaCarnivoralnsectlvoraScandentiaDermopteraChiropteraPrimatesArtiodactylaCetaceaPholidotaRodentia

A~~~",0 ~~ ",0

b~W~~~~,~'l;

** * /

************Incidence of internal carotid-FMTC relationships a mong mammalian embry os st udied

to date. In representatives of some eutherian orders, i.e., Lagomorpha and Carnivora ,the internal carotid is enclosed w ithin the FMTC in late ontogenetic st ages for the

for mati on of a carotid canal.

EARLY EUTHERIAN INTERNAL CAROTID ARTERY 289

cavity). Preliminary observations on the incidence of internal carotid­-FMTC relationships among mammalian embryos (Table 2) show thefollowing: (1) in non-eutherian mammalian embryos, the internal carotidis excluded from the tympanic cavity by the FMTC (the morphology inTachyglossus, the only monotreme studied to date, is not exactly compar­able to that in marsupials, as relationships are somewhat altered by theposterior expansion of the nasopharynx and auditory tube); and (2) ineutherian embryos, the internal carotid artery follows a more lateralcourse either within the substance of the FMTC or included within thetympanic cavity by the'FMTC. .

a

b

pp

II!\ . -ica ........

····················· FMTC

pp

~_._~/ica(O)~ "

<,'. .·················...FMTC

~--ab

Fig. 5. Schematic representations of two developmental processes for the formationof an internal carotid artery running medial to the auditory bulla in the adult. Innon-eutherian mammals (a), the internal carotid lies medial to the FMTC in theembryo. In later ontogenetic stages, the internal carotid is still excluded from thetympanic cavity by the formation of a bony bulla (the ectopterygoid in Tachyg~ossus

and the alisphenoid in marsupials). In edentates (b), the internal carotid runs throughthe substance of the FMTC in the embryo. Later, the entotympanic can either forma complete or incomplete carotid canal around the artery. Abbreviations as on

page: 291.

290 JOH N R. W IBLE

It is generally acc epted that the primitive course of the mammalianinternal car otid was medial to the promontorium and the auditory bullaas this is the condition in monotremes, marsupials, and some eutherians,including ede ntates (d. Presl ey 1979). However , on togenetic researchshows that the edentate artery running medial to the bulla develops ina ve ry diff erent way than the artery in monotremes and marsupials. Innon-eutherian mammals, the internal carotid is always excluded fromthe tympanic cavity , eithe r by the F MTC or the bony bulla (fig. 5a) . Incontrast, the inte r nal car otid in ede ntate embryos (Dasyp us nov emcinc tusand Bradypus) runs throu gh the subs ta nce of the FMTC (fig. 5b) .. Later,the entotympanic bullar eleme nts form with in the FMTC (d. MacPhee1979) arou nd the in ternal carotid ar tery. The extent of entotympanicformation is va r iable ; the inter nal car ot id can ei ther be enclosed wi thina 'canal in the en totympanic or merel y exc lude d from the tympanic cavityby the ento tympa nic. This va riable degree of entotympanic formationaccounts for the observations in adult edentate sku lls of complete andincomplete car oti d canals (Kampen 1905; personal observati ons).

These preliminary ontogenetic observations confir m that the primitivecourse of the internal carotid ar tery in mammals was likely medial to thebulla (FMTC) , the conditi on found in monotremes and marsupials . How­eve r, it is unlikel y that this was a lso the prim it ive cour se of the eu ther ianar te ry, as this same pathwa y is not found. among extant eutherians. Theprimitive eutherian internal carotid artery foll owed a more la teral courseei ther through the substance of the FMTC or lateral to the FMTC w ithinthe tympanic cavit y. The presence of a medi al gro ove in K ennalestes andAsioryctes suggests a medial course for the primiti ve eutherian internalcar ot id. Yet, based on the above ontoge ne t ic observations, this medialcourse was most likely not ide nt ical wi th the medial course of non-euther­ian mammals.

AC K NOW LEDGEMENTS

Th is review is pa rt of a larger study on th e ontogeny and phyloge ny of themamma lia n in terna l ca rotid artery. Th at r esearch is supported by the GermanAcademic Ex change Service, Du ke Universit y an d National Scien ce F oundationG ran t DEB-801l 634 for Doct oral Disser tation Research in Systemati c Biology. Inparti cular I want to th ank Drs. M. Cartmill , my graduate su pervisor , a ndR. D. E. MacPhee fo r in valuable discussions and advic e in this en deavor. I wantto ac know ledge and thank .the foll ow ing in div iduals and in stituti ons for permissionto st udy sp ecimens in th eir care: P rof. D. Starck and P rof. W. Mai er (Dr. Senck en­berg isch e Anatomie, Frankfurt); Prof. H.-J. Kuhn (Anatomisches Institut , Go ttingen );Prof. W. Reinbach (Ana tomisches Insti tut , Heidelberg); Dr. E. C. Bot erenbr ood(Hubrecht Laborat ory , Utrech t); Dr. D. E. Ru ssell (Ins ti t ut de Paleontologie ,Mu seu m Nationa l d 'Historie Naturelle, Paris) ; Prof. R. Lavocat a nd M. Godinot(Laborato r ie de Paleontologie, U.S.T.L., Montpellier) ; and Drs. R. H. Tedford,M. C. McKen na and S. And erson (Am erican Museum of Natu ral Hist ory, New York).Fina lly, I want to thank P rof. W. Mai er who read an d co mme n te d on the manusc rip t

EARLY ~;UTHERIAN INTERNAL CAROTID ARTERY 291

and the staff of Dr. Senckenbergische Anatomie for various favor s during the courseof my stay (in particular, M. Roser for the line ' d raw ings and U . Trautmann forphotographic help).

Abbreviations:

aba bcafatbfcccffc '

fofroFMTCfvicaijvipsirmfmicamvpbcpicappprptrcsasqsr

a uditory bullaanterior basicapsular commissureaper tu re of fo ssula of coc hlear fen est raa la temporalisbasicapsular fenest racochlear capsulecarotid foramenfenestra cochleaeforamen ovaleforamen magnumfibrous membrane of th e tympanic cavi tyfenestra vestibuliin terna l carotid arteryinternal jugular v eininferior petrosal sinusinfe rior ramus of stapedial arterymetotic fissuremedial internal carotid a rterymedial veinposter ior basicapsular commissurepromontory artery (lateral internal carotid artery)pa rachorda l platepromontorium of pet rosalpterygoid

, Reichert's cartilagesta ped ia l arterysqua m osa lsupe r ior ramus of s ta pedia l artery

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Ie-

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