British Journal of Ophthalmology 1996; 80: 177-181

Anatomy of the extraneural blood supply to theintracranial oculomotor nerve

Mark Cahill, John Bannigan, Peter Eustace

AbstractAims-An anatomical study was under-taken to determine the extraneural bloodsupply to the intracranial oculomotornerve.Methods-Human tissue blocks contain-ing brainstem, cranial nerves II-VI, bodyof sphenoid, and associated cavernoussinuses were obtained, injected with con-trast material, and dissected using astereoscopic microscope.Results-Eleven oculomotor nerves weredissected, the intracranial part beingdivided into proximal, middle, and distal(intracavernous) parts. The proximal partof the intracranial oculomotor nervereceived extraneural nutrient arteriolesfrom thalamoperforating arteries in allspecimens and in six nerves this bloodsupply was supplemented by branchesfrom other brainstem vessels. Four nerveswere seen to be penetrated by branches ofbrainstem vessels and these penetratingarteries also supplied nutrient arterioles.The middle part ofthe intracranial oculo-motor nerve did not receive nutrient arte-rioles from adjacent arteries. The distalpart of the intracranial oculomotor nervereceived nutrient arterioles from the infe-rior cavernous sinus artery in all 11 nervesand in seven nerves this was supple-mented by a tentorial artery arising fromthe meningohypophyseal trunk. The infe-rior hypophyseal artery arose from themeningohypophyseal trunk in all 11 cav-ernous sinuses dissected.Conclusion-This study shows a constantpattern to the blood supply of theintracranial oculomotor nerve. It alsohighlights the close relation between theblood supplies to the intracavernous ocu-lomotor nerve and the pituitary gland.(Br_' Ophthalmol 1996; 80: 177-181)

Up to now no definitive detailed study of theblood supply to the intracranial portion of thethird cranial nerve has been published. It is thisportion of the third cranial nerve that has par-ticular importance in neuro-ophthalmology.Bartholdy, in 1897, first described that cranialnerves received nutrient vessels from adjacentarteries.' However, technical difficulties pre-vented any definite anatomical patterns beingdemonstrated. It was not until 1957 thatDreyfus et al, in a paper dealing with diabeticophthalmoplegia, demonstrated that arteriesfrom the basilar circulation and circle of Willisgave off nutrient arterioles to the intracranialpart of the oculomotor nerve.2 These vessels

have since been classified as extraneural vesselsas they arise from outside the nerve and ramifyon the surface of the nerve. In 1965, Parkinsonattempted to demonstrate and name thebranches of the intracavernous internal carotidartery.3 One of these branches, the newly titledmeningohypophyseal trunk was seen to pro-vide a nutrient arteriole to the oculomotornerve in the majority of dissections. The infe-rior hypophyseal artery was also seen to arisefrom the meningohypophyseal trunk. Sevenyears earlier McConnell had demonstratedthat this vessel provided a large portion of thepituitary blood supply.4

Asbury and colleagues provided furtheranatomical detail in 1970.5 They set out toexplain the clinical findings of diabetic oph-thalmoplegia on a pathological basis. Using aserial section technique, they demonstrated anintraneural network of small arterioles withinthe oculomotor nerve. By this technique it wasalso determined that the extraneural arteriolesto the oculomotor nerve arose proximally froma variety ofbrainstem arteries and distally fromnon-specific branches of the inferior cavernoussinus artery. More recently, three studies haveset out to demonstrate the anatomy of theextraneural blood supply to the proximal part(also termed the interpeduncular or cisternalpart) of the intracranial oculomotor nerve.6-8Two of these studies by Milisavljevic et al,8 andMarinkovic and Gibo,7 noted that the proxi-mal intracranial oculomotor nerve can be pen-etrated by branches of brainstem arteries.These penetrating arteries can also supplynutrient arterioles to the nerves they penetrate.The present anatomical study was under-

taken to demonstrate the extraneural bloodsupply to the intracranial oculomotor nerve.We wanted to clarify the anatomical detailsusing information from earlier studiesl-8 1012and our own dissection findings (Fig 1). Wealso examined the relation between the bloodsupply to the intracavernous section of theoculomotor nerve and that to the pituitarygland.

Materials and methodsSix tissue blocks containing midbrain, pons,cerebellum, cranial nerves II-VI, basilar artery(and branches), body of sphenoid with associ-ated pituitary gland, and cavernous sinuseswere removed from postmortem subjects andimmediately fixed in a solution of 1O% forma-lin. To facilitate identification of vessels sup-plying the intracranial oculomotor nerve andother structures, the basilar and internalcarotid arteries were injected with India inkbefore dissection. The specimens were dis-

Institute ofOphthalmology,University CollegeDublin, MaterMisericordiaeHospital, Dublin,IrelandM CahillP Eustace

Department ofAnatomy, The MedicalSchool, UniversityCollege Dublin,Dublin, IrelandM CahillJ Bannigan

Correspondence to:Professor Peter Eustace,Institute of Ophthalmology,University College Dublin,Mater MisericordiaeHospital, 60 Eccles Street,Dublin 7, Ireland.Accepted for publication1 1 October 1995

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Midbrain

Sh Circum A

Figure1 The blood supply to a right intracranial oculomotor nerve seenfrom the right.PCA=posterior cerebral artery, S CerA=superior cerebellar artery, L Circum A=longcircumflex artery, Sh Circum A=short circumflex artery, P Comm A =posteriorcommunicating artery, III CN=oculomotor nerve, ICA=internal carotid artery,MHT= meningohypophyseal trunk, InfCav Sin A=inferior cavernous sinus artery. Darkoutline represents the limits of the cavernous sinus.

sected with the aid of a stereoscopic micro-scope. Photographs were taken and drawingswere made at all stages of the dissections.

ResultsOur of 12 possible intracranial oculomotornerves, 11 were dissected. For simplicity theintracranial oculomotor nerve was anatomi-cally divided into three parts. The proximalpart consisted of the part from the emergenceofthe nerve at the cerebral peduncles to a pointjust distal to the anastomosis of the posteriorcerebral and posterior communicating arteries.The middle part was that part from the latterpoint to just before the oculomotor nerveenters the cavernous sinus. The distal part wasthat part of the nerve within the cavernoussinus.

PROXIMAL NERVEIn all specimens, the proximal parts of the ocu-lomotor nerve were supplied by thalamoperfo-rating arteries arising from the posteriorcerebral artery (Figs 2A and 2B). In five oculo-motor nerves these were the only extraneuralnutrient vessels to the proximal nerve. In theremaining six nerves these were supplementedby a number of brainstem arteries, outlined inTable 1. The proximal part of the intracranialoculomotor nerve was seen to be penetrated byarteries in four nerves, which also suppliednutrient vessels to the nerve. In two nerves thepenetrating artery was the long circumflexartery, in one nerve it was a thalamoperforatingartery, and both a thalamoperforating artery

Table 1 Outline of brainstem vessels which providedsupplementary nutrient arterioles to proximalpart ofintracranial oculomotor nerve

ArterySpecimenNo PCA P Comm A S CerA L Circum A

6 /7 /8 /9 /10 / /11 / / /

PCA=posterior cerebral artery, P Comm A=posteriorcommunicating artery, S Cer A=superior cerebellar artery,L Circum A=long circumflex artery.

and a long circumflex artery penetrated theremaining nerve.

MIDDLE NERVEThe middle part of the intracranial oculomotornerve was not seen to receive nutrient arter-ioles along its length from adjacent arteries.

DISTAL NERVEIn seven of 11 cavernous sinuses examined, theoculomotor nerve and its surrounding ten-torium was seen to receive nutrient arteriolesfrom an anteriorly directed tentorial arterywhich was a branch of the meningohypo-physeal trunk (Figs 3A and 3B). In all 11cavernous sinuses examined, an attempt wasmade to identify four branches of the inferiorcavernous sinus artery - an anterior branch, atentorial branch, a descending branch, anda posterior branch (Figs 4A and 4B). All 11distal oculomotor nerves received nutrientarterioles from branches of the inferiorcavernous sinus artery. In four nerves thesenutrient arterioles arose from the anteriorbranch, in five they arose from the tentorialbranch and in two nerves both the anteriorbranch and the tentorial branch suppliednutrient vessels to the oculomotor nerve.

In all 11 of the cavernous sinuses dissectedthe inferior hypophyseal artery was seen toarise from the meningohypophyseal trunk(Figs 3A and 3B). The ophthalmic artery didnot supply nutrient arterioles to the oculo-motor nerve in any of the 11 cavernous sinusesdissected.

DiscussionTo date, no study has attempted systematicallyto identify and name the extraneural bloodsupply to the intracranial oculomotor nerve.The term extraneural is used to encompassthose small arterioles arising from largerarteries adjacent to the oculomotor nerve.These are distinct from the intraneural arteri-oles which form a plexus of capillaries withinthe nerve substance. We felt that the clearestway to demonstrate the anatomy of the extra-neural blood supply to the oculomotor nervewould be to divide it into three. Those seg-ments ofthe nerve that make up these divisions(proximal, middle, and distal) have alreadybeen outlined in the results section.Two early studies using postmortem sub-

jects combined with anatomical dissections areimportant.2 5 These were undertaken to deter-mine the pathological basis of diabetic ophthal-moplegia and demonstrated some of theextraneural nutrient arterioles to the proximalpart of the intracranial oculomotor nerve. Thefirst, by Dreyfus et al,2 demonstrated that theextraneural nutrient arterioles could arise fromthe posterior cerebral and superior cerebellararteries. Unfortunately, the reporting of thesedissections was unsystematic. The secondstudy by Asbury and colleagues,5 system-atically determined the intraneural bloodsupply to the proximal part of the intracranial

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Anatomy of the extraneural blood supply to the intracranial oculomotor nerve

oculomotor nerve using a serial section tech-nique. However, this study also only com-mented that in general small nutrient arteriolesfrom the posterior cerebral and basilar arteriessupplied the proximal part of the intracranialoculomotor nerve.

.._.......Two more recent studies have demonstratedthe proximal part of the intracranial oculo-

*diE_ _ motor nerve to be supplied with extraneuralnutrient arterioles arising from 'perforatingvessels'.67 These are termed perforatingvessels because they pierce the posterior per-

_ forated substance to supply various midbrainstructures. The first of these undertaken byPedroza et al6 states that in 71% of specimensdissected non-specific perforating vessels vas-cularised the proximal part of the intracranialoculomotor nerve. The latter study by Marin-kovic and Gibo,7 was more specific and wasable to demonstrate nutrient arterioles arisingfrom the mesencephalic perforators in 88-9%and/or the diencephalic perforators in 40/7%of cases. Furthermore, this latter study demon-strated that further extraneural nutrient vesselsmost commonly arose from the collicularartery (long circumflex artery) or branches.

Both Marinkovic and Gibo,7 andFig 2A Milisvljevic et al,8 have noted that the proximal

part of the intracranial oculomotor nerve canB * w be penetrated by either a perforating artery, a

long or short circumflex artery, or both (56%.4" and 40% of cases respectively). While passing

through the nerve these penetrating vesselsvSub Nigran g =_g>,give small extraneural nutrient arterioles to the

N ~~~proximal part of the nerve.The present study utilised the anatomical

details provided by the studies outlinedabove,2 5-8 as a springboard from which westarted. In the specimens that we dissected

IIICN 'I ....\.only the thalamoperforating arteries wereseen to provide nutrient arterioles to the prox-

a-2;08_ | _ imal intracranial oculomotor nerve. TheSt) Cir:um A s s "-_L°_ study undertaken by Marinkovic and Gibo7

differentiated the aforementioned perforatingvessels into diencephalic perforators(thalamoperforating arteries) and mesen-cephalic perforators. Both of these groups

PCA supplied extraneural nutrient arterioles to theproximal intracranial oculomotor nerve aspreviously outlined. This difference betweenour findings and Marinkovic and Gibo's find-

*4!9_S Cer;;/ ^ings,7 could be accounted for by anatomicalvariation.

This study concurs with the findings ofMarinkovic and Gibo,7 that other brainstem

'1 / _ _vessels (particularly the long circumflex artery)also provide extraneural nutrient arterioles tothe proximal intracranial oculomotor nerve.

a Furthermore, we have also been able to con-firm the findings of Marinkovic and Gibo7 andMilisavljevic et al,8 that one of the circumflexarteries or a thalamoperforating artery can

Fig 2B penetrate the proximal part of the oculomotorFigure 2 (A) Photograph ofproximal part of intracranial oculomotor nerve viewedfrom nerve.above. Demonstrates nerve being penetrated by thalamoperforating artery (A) and being The extraneural blood supply to the middlesupplied by thalamoperforating vessels (B). Magnification X 10. (B) Drawing ofspecimenin (A). Demonstrates proximal part of oculomotor nerve with thalamoperforating artery part of the intracraNial oculomotor nerve wasboth penetrating and supplying the nerve. Bas A= basilar artery, S Cer A=superior more challenging. Neither Dreyfus et al2 norcerebellar artery, PCA =posterior cerebral artery, PerfA= Thalamoperforating arteries, Asbury et al 5 specifically examined this part ofSh Circum A=short circumflex artery, CP=cerebral peduncle, Sub Nigra=substantianigra, III CN=oculomotor nerve, a=thalamoperforating artery penetrating oculomotor the nerve. Common sense would have sug-nerve, b= thalamoperforating artery supplying nutrient vessel to oculomotor nerve. gested before the study that a nutrient arteriole

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Fig 3A

B

Post Clin Proc

'/ - ;-; t~~~~~~~Tent A2 ,!

v Y0 qb TIV CN

Fig 3BFigure 3 (A) Photograph ofright cavernous sinus viewedfrom above. Demonstratesmeningohypophyseal trunk (A) arisingfrom the ICA. Note anterior tentorial artery (B)supplying oculomotor nerve and tentorium. Magnification X 10. (B) Drawing ofspecimenin (A). Demonstrates meningohypophyseal trunk and its four branches. ICA=internalcarotid artery, D Men A=dorsal meningeal artery, TentA1 =postenior tentorial artery,TentA2= anterior tentorial artery, InfHypoA= inferior hypophyseal artery, IIICN=oculomotor nerve, IV CN=trochlear nerve, VI CN=abducens nerve, Post ClinProc=posterior clinoid process, Pituitary=pituitary gland.

would arise from the adjacent posterior commu-nicating artery to supply the oculomotor nerve.In fact, the middle part ofthe intracranial oculo-motor nerve was not seen to receive nutrientarterioles from any vessels in any of the 1 1 spec-imens. Adams demonstrated that peripheralnerves have excellent intraneural blood suppliesrunning within the epineurium.9 This extendsfrom the proximal to distal parts of the nerve. Atregular intervals branches pierce the peri-neurium and form longitudinal plexi of capil-laries between nerve fascicles.The present study did not examine the intra-

neural blood supply of the intracranial oculo-motor nerve. However, we conclude that theabsence of extraneural nutrient arterioles run-

ning onto the middle section ofthe oculomotornerve suggests that this section of the nerve issupplied by intraneural arterioles passing fromits proximal and distal ends.

The final division we deal with is the distalor intracavernous portion of the oculomotornerve. Parkinson3 9 carried out a majoranatomical study on over 200 cadavers in theearly 1960s. In this landmark study, heattempted to name the branches of the intra-cavernous internal carotid artery by their dis-tribution. In passing, Parkinson noted that a'tentorial branch of the meningohypophysealtrunk' (Parkinson's nomenclature) supplied anutrient arteriole to the oculomotor nerve.Parkinson named two other branches of theintracavernous internal carotid artery. He gaveone the eponym 'McConnell's capsular artery'and the second the descriptive title 'the inferiorcavernous sinus artery'. Parkinson did notcomment as to whether or not either of thesetwo branches supplied nutrient arterioles tothe intracavernous oculomotor nerve. Asburyet al,5 utilising Parkinson's nomenclaturedemonstrated that non-specific branches ofthe inferior cavernous sinus artery suppliednutrient arterioles to the intracavernous oculo-motor nerve. Two further studies are note-worthy.'1 12 The first one by Annabi et al,'Iattempted to name the extraneural nutrientarterioles supplying the intracavernous oculo-motor nerve but unfortunately they did not useParkinson's nomenclature. The second studywas a topographical anatomical study to find amore workable nomenclature for the branchesof the intracavernous internal carotid artery,which does not comment on the blood supplyto the oculomotor nerve.'2The present study utilises the nomenclature

first outlined by Parkinson.3 10 Using cluesfrom both Parkinson's3 l and Asbury's work,5we systematically examined the extraneuralblood supply to the intracavernous oculomotornerve. In our study reported in this paper, ithas been demonstrated for the first time thatthe inferior cavernous sinus artery consistentlydivides into four branches. We have named thebranches according to the directions in whichthey were seen to travel. We have also shownthat of these four branches either an anteriorbranch, a tentorial branch, or both of thesebranches supply the intracavernous oculo-motor nerve. In the majority of specimensdissected, the intracavernous oculomotornerve was also supplied by the tentorial branchof the meningohypophyseal trunk. This branchhad previously been demonstrated by Parkin-son3 10 to supply the oculomotor nerve.

Unfortunately it can be confusing if smallarterioles are given long titles with similarlynamed branches. However, Parkinson's origi-nal nomenclature is that in common usage.Thus in this paper we have used the terms'meningohypophyseal trunk' and 'the inferiorcavernous sinus artery' and added the sub-division 'tentorial branch' to both these simplybecause it is a descriptive title and thereforemore memorable. With regard to the extra-neural blood supply to the intracavernousoculomotor nerve, we conclude that thearterioles arising from the inferior cavernoussinus artery are its main supply, as they areconsistently present. The arterioles arisingfrom the meningohypophyseal trunk (namely

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rzg 4vs

B

Tent Br

.1" r III CN

Post Br __ VI CN

Desc Br

Fig 4BFigure 4 (A) Photograph of right cavernous sinus viewedfrom the right side.Demonstrates the inferior cavernous sinus artery and its branches (A). Note tentorialbranch supplying oculomotor nerve (B). Magnification X 10. (B) Drawing ofspecimen in(A). Demonstrates the four branches of the inferior cavernous sinus artery. ICA= internalcarotid artery, Tent Br=tentorial branch, Ant Br= anterior branch, Post Br=posteriorbranch, Desc Br= descending branch, a and b=branches of tentorial branches supplyingoculomotor nerve, III CN=oculomotor nerve, IV CN= trochlear nerve, VI CN=abducensnerve.

the anterior tentorial branch) provide supple-mentary blood supply to the oculomotor nerve.

Finally, we come to the relation between theblood supply to the pituitary gland and that tothe intracavernous oculomotor nerve. A largepart of the pituitary blood supply arises from

the inferior hypophyseal artery, as determinedby McConnell in 1958.4 The inferior hypophy-seal artery is one of the three branches of themeningohypophyseal trunk, the same trunkwhich gives a tentorial branch to supply theoculomotor nerve. Thus we postulate that avascular event occurring in this trunk couldcause damage to both the pituitary gland andthe oculomotor nerve.

ConclusionsA consistent pattern to the anatomy of theextraneural blood supply of the intracranialoculomotor nerve has been demonstrated.Proximally, the oculomotor nerve receivesextraneural nutrient arterioles from thethalamoperforating arteries which are supple-mented by other nutrient arterioles frombrainstem vessels. The middle part of theintracranial oculomotor nerve does not receiveextraneural nutrient arterioles from adjacentarteries. The distal (intracavernous) part of theintracranial oculomotor nerve receives extra-neural nutrient arterioles from either theanterior branch, the tentorial branch, or boththese branches of the inferior cavernous sinusartery. This may be supplemented by a ten-torial branch of the meningohypophysealtrunk. There is a close relation between theblood supply to the pituitary gland and theintracavernous oculomotor nerve - namely, theshared meningohypophyseal trunk.

1 Bartholdy K. Die Arterien der Nerven. MorpholArb 1897; 7:393-458.

2 Dreyfus PM, Hakin S, Adams RD. Diabetic ophthalmo-plegia. AMA Arch Neurol Psychiatry 1957; 77: 337-49.

3 Parkinson D. A surgical approach to the cavernous portionof the carotid artery. JNeurosurg 1965; 23: 474-83.

4 McConnell EM. The arterial blood supply of humanhypophysis cerebri. Anat Rec 1953; 115: 175-201.

5 Asbury AK, Aldredge N, Hershberg R, Fisher CM.Oculomotor palsy in diabetes mellitus: a clinico-patho-logical study. Brain 1970; 93: 555-66.

6 Pedroza A, Dujovny M, Ausman JI, Diaz FG, CabezudoArtero J, Berman SK, et al. Microvascular anatomy of theinterpeduncular fossa. J Neurosurg 1986; 64: 484-93.

7 Marinkovic S, Gibo H. The neurovascular relationship andthe blood supply of the oculomotor nerve: the micro-surgical anatomy of its cisternal segment. Surg Neurol1994; 42: 505-16.

8 Milisavljevic M, Marinkovic S, Lolic Draganic V,Kovacevic M. Oculomotor, trochlear and abducensnerves penetrated by cerebral vessels. Arch Neurol 1986;43: 505-16.

9 Adams WE. The blood supply of nerves II. The effects ofexclusion of its regional sources of supply on the sciaticnerve of the rabbit. JAnat 1943; 77: 243-50.

10 Parkinson D. Collateral circulation of cavernous carotidartery: anatomy. CanJ Surg 1964; 7: 251-68.

11 Annabi A, Lasjaunias P, Lapresle J. Paralysies de la IIIepaire au cours du diabete et vascularisation du moteuroculaire common. JNeurol Sci 1979; 41: 359-67.

12 Tran-Dinh H. Cavernous branches of the internal carotidartery: anatomy and nomenclature. Neurosurgery 1987;20: 205-10.

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