British Journal of Ophthalmology 1996; 80: 177-181 177 the extraneural blood to the Anatomy of supply Br J Ophthalmol: first published as 10.1136/bjo.80.2.177 on 1 February 1996. Downloaded from intracranial oculomotor

Mark Cahill, John Bannigan, Peter Eustace

Abstract have since been classified as extraneural vessels Aims-An anatomical study was under- as they arise from outside the nerve and ramify taken to determine the extraneural blood on the surface ofthe nerve. In 1965, Parkinson supply to the intracranial oculomotor attempted to demonstrate and name the nerve. branches of the intracavernous internal carotid Methods-Human tissue blocks contain- artery.3 One of these branches, the newly titled ing , cranial II-VI, body meningohypophyseal trunk was seen to pro- of sphenoid, and associated cavernous vide a nutrient arteriole to the oculomotor sinuses were obtained, injected with con- nerve in the majority of dissections. The infe- trast material, and dissected using a rior hypophyseal artery was also seen to arise stereoscopic microscope. from the meningohypophyseal trunk. Seven Results-Eleven oculomotor nerves were years earlier McConnell had demonstrated dissected, the intracranial part being that this vessel provided a large portion of the divided into proximal, middle, and distal pituitary blood supply.4 (intracavernous) parts. The proximal part Asbury and colleagues provided further of the intracranial anatomical detail in 1970.5 They set out to received extraneural nutrient arterioles explain the clinical findings of diabetic oph- from thalamoperforating arteries in all thalmoplegia on a pathological basis. Using a specimens and in six nerves this blood serial section technique, they demonstrated an supply was supplemented by branches intraneural network of small arterioles within from other brainstem vessels. Four nerves the oculomotor nerve. By this technique it was were seen to be penetrated by branches of also determined that the extraneural arterioles brainstem vessels and these penetrating to the oculomotor nerve arose proximally from arteries also supplied nutrient arterioles. a variety ofbrainstem arteries and distally from The middle part ofthe intracranial oculo- non-specific branches of the inferior cavernous motor nerve did not receive nutrient arte- sinus artery. More recently, three studies have rioles from adjacent arteries. The distal set out to demonstrate the anatomy of the

part of the intracranial oculomotor nerve extraneural blood supply to the proximal part http://bjo.bmj.com/ received nutrient arterioles from the infe- (also termed the interpeduncular or cisternal rior artery in all 11 nerves part) of the intracranial oculomotor nerve.6-8 and in seven nerves this was supple- Two ofthese studies by Milisavljevic et al,8 and mented by a tentorial artery arising from Marinkovic and Gibo,7 noted that the proxi- the meningohypophyseal trunk. The infe- mal intracranial oculomotor nerve can be pen- rior hypophyseal artery arose from the etrated by branches of brainstem arteries.

meningohypophyseal trunk in all 11 cav- These penetrating arteries can also supply on September 27, 2021 by guest. Protected copyright. ernous sinuses dissected. nutrient arterioles to the nerves they penetrate. Conclusion-This study shows a constant The present anatomical study was under- pattern to the blood supply of the taken to demonstrate the extraneural blood intracranial oculomotor nerve. It also supply to the intracranial oculomotor nerve. highlights the close relation between the We wanted to clarify the anatomical details Institute of blood supplies to the intracavernous ocu- using information from earlier studiesl-8 1012 Ophthalmology, University College lomotor nerve and the pituitary gland. and our own dissection findings (Fig 1). We Dublin, Mater (Br_' Ophthalmol 1996; 80: 177-181) also examined the relation between the blood Misericordiae supply to the intracavernous section of the Hospital, Dublin, Ireland oculomotor nerve and that to the pituitary M Cahill Up to now no definitive detailed study of the gland. P Eustace blood supply to the intracranial portion of the Department of third cranial nerve has been published. It is this Anatomy, The Medical portion of the third cranial nerve that has par- Materials and methods School, University ticular importance in neuro-ophthalmology. Six tissue blocks containing , pons, College Dublin, Dublin, Ireland Bartholdy, in 1897, first described that cranial cerebellum, II-VI, basilar artery M Cahill nerves received nutrient vessels from adjacent (and branches), body of sphenoid with associ- J Bannigan arteries.' However, technical difficulties pre- ated pituitary gland, and cavernous sinuses Correspondence to: vented any definite anatomical patterns being were removed from postmortem subjects and Professor Peter Eustace, demonstrated. It was not until 1957 that immediately fixed in a solution of 1O% forma- Institute of Ophthalmology, University College Dublin, Dreyfus et al, in a paper dealing with diabetic lin. To facilitate identification of vessels sup- Mater Misericordiae ophthalmoplegia, demonstrated that arteries plying the intracranial oculomotor nerve and Hospital, 60 Eccles Street, Dublin 7, Ireland. from the basilar circulation and circle of Willis other structures, the basilar and internal Accepted for publication gave off nutrient arterioles to the intracranial carotid arteries were injected with India ink 1 1 October 1995 part of the oculomotor nerve.2 These vessels before dissection. The specimens were dis- 178 CahiUl, Bannigan, Eustace

Midbrain and a long circumflex artery penetrated the remaining nerve. Br J Ophthalmol: first published as 10.1136/bjo.80.2.177 on 1 February 1996. Downloaded from Sh Circum A MIDDLE NERVE The middle part ofthe intracranial oculomotor nerve was not seen to receive nutrient arter- ioles along its length from adjacent arteries.

DISTAL NERVE In seven of 11 cavernous sinuses examined, the oculomotor nerve and its surrounding ten- Figure1 The blood supply to a right intracranial oculomotor nerve seen from the right. PCA=posterior cerebral artery, S CerA=superior cerebellar artery, L Circum A=long torium was seen to receive nutrient arterioles circumflex artery, Sh Circum A=short circumflex artery, P Comm A=posterior from an anteriorly directed tentorial artery communicating artery, III CN=oculomotor nerve, ICA=internal carotid artery, which was a branch of the meningohypo- MHT= meningohypophyseal trunk, InfCav Sin A=inferior cavernous sinus artery. Dark outline represents the limits ofthe cavernous sinus. physeal trunk (Figs 3A and 3B). In all 11 cavernous sinuses examined, an attempt was made to identify four branches of the inferior sected with the aid of a stereoscopic micro- cavernous sinus artery - an anterior branch, a scope. Photographs were taken and drawings tentorial branch, a descending branch, and were made at all stages of the dissections. a posterior branch (Figs 4A and 4B). All 11 distal oculomotor nerves received nutrient arterioles from branches of the inferior Results cavernous sinus artery. In four nerves these Our of 12 possible intracranial oculomotor nutrient arterioles arose from the anterior nerves, 11 were dissected. For simplicity the branch, in five they arose from the tentorial intracranial oculomotor nerve was anatomi- branch and in two nerves both the anterior cally divided into three parts. The proximal branch and the tentorial branch supplied part consisted of the part from the emergence nutrient vessels to the oculomotor nerve. ofthe nerve at the cerebral peduncles to a point In all 11 of the cavernous sinuses dissected just distal to the anastomosis of the posterior the inferior hypophyseal artery was seen to cerebral and posterior communicating arteries. arise from the meningohypophyseal trunk The middle part was that part from the latter (Figs 3A and 3B). The ophthalmic artery did point to just before the oculomotor nerve not supply nutrient arterioles to the oculo- enters the cavernous sinus. The distal part was motor nerve in any of the 11 cavernous sinuses that part of the nerve within the cavernous dissected. sinus. http://bjo.bmj.com/ Discussion PROXIMAL NERVE To date, no study has attempted systematically In all specimens, the proximal parts ofthe ocu- to identify and name the extraneural blood lomotor nerve were supplied by thalamoperfo- supply to the intracranial oculomotor nerve. rating arteries arising from the posterior The term extraneural is used to encompass cerebral artery (Figs 2A and 2B). In five oculo- those small arterioles arising from larger on September 27, 2021 by guest. Protected copyright. motor nerves these were the only extraneural arteries adjacent to the oculomotor nerve. nutrient vessels to the proximal nerve. In the These are distinct from the intraneural arteri- remaining six nerves these were supplemented oles which form a plexus of capillaries within by a number of brainstem arteries, outlined in the nerve substance. We felt that the clearest Table 1. The proximal part of the intracranial way to demonstrate the anatomy of the extra- oculomotor nerve was seen to be penetrated by neural blood supply to the oculomotor nerve arteries in four nerves, which also supplied would be to divide it into three. Those seg- nutrient vessels to the nerve. In two nerves the ments ofthe nerve that make up these divisions penetrating artery was the long circumflex (proximal, middle, and distal) have already artery, in one nerve it was a thalamoperforating been outlined in the results section. artery, and both a thalamoperforating artery Two early studies using postmortem sub- jects combined with anatomical dissections are Table 1 Outline ofbrainstem vessels which provided important.25 These were undertaken to deter- supplementary nutrient arterioles to proximalpart of intracranial oculomotor nerve mine the pathological basis ofdiabetic ophthal- moplegia and demonstrated some of the Artery extraneural nutrient arterioles to the proximal Specimen No PCA P Comm A S CerA L Circum A part of the intracranial oculomotor nerve. The first, by Dreyfus et al,2 demonstrated that the 6 / 7 / extraneural nutrient arterioles could arise from 8 / the posterior cerebral and superior cerebellar 9 / 10 / / arteries. Unfortunately, the reporting of these 11 / // dissections was unsystematic. The second study by Asbury and colleagues,5 system- PCA=posterior cerebral artery, P Comm A=posterior communicating artery, S Cer A=superior cerebellar artery, atically determined the intraneural blood L Circum A=long circumflex artery. supply to the proximal part of the intracranial Anatomy ofthe extraneural blood supply to the intracranial oculomotor nerve 179

oculomotor nerve using a serial section tech-

nique. However, this study also only com- Br J Ophthalmol: first published as 10.1136/bjo.80.2.177 on 1 February 1996. Downloaded from mented that in general small nutrient arterioles from the posterior cerebral and basilar arteries supplied the proximal part of the intracranial oculomotor nerve...... Two._. more recent studies have demonstrated the proximal part of the intracranial oculo- *diE_ _ motor nerve to be supplied with extraneural nutrient arterioles arising from 'perforating vessels'.67 These are termed perforating vessels because they pierce the posterior per- _ forated substance to supply various midbrain structures. The first of these undertaken by Pedroza et al6 states that in 71% of specimens dissected non-specific perforating vessels vas- cularised the proximal part of the intracranial oculomotor nerve. The latter study by Marin- kovic and Gibo,7 was more specific and was able to demonstrate nutrient arterioles arising from the mesencephalic perforators in 88-9% and/or the diencephalic perforators in 40/7% ofcases. Furthermore, this latter study demon- strated that further extraneural nutrient vessels most commonly arose from the collicular artery (long circumflex artery) or branches. Both Marinkovic and Gibo,7 and Fig 2A Milisvljevic et al,8 have noted that the proximal part of the intracranial oculomotor nerve can B * 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 vessels vSub 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 outlined 5-8 above,2 as a springboard from which we http://bjo.bmj.com/ started. In the specimens that we dissected III CN 'I ....\.only the thalamoperforating arteries were seen to provide nutrient arterioles to the prox- -2;0a 8_ | _ imal intracranial oculomotor nerve. The St) Cir:um A s s "-_L°_ study undertaken by Marinkovic and Gibo7 differentiated the aforementioned perforating

vessels into diencephalic perforators on September 27, 2021 by guest. Protected copyright. (thalamoperforating arteries) and mesen- cephalic perforators. Both of these groups PCA supplied extraneural nutrient arterioles to the proximal intracranial oculomotor nerve as previously outlined. This difference between our findings and Marinkovic and Gibo's find- could be accounted for anatomical *4!9_S Cer ;;/ ings,7^ by variation. This study concurs with the findings of Marinkovic and Gibo,7 that other brainstem _ _vessels (particularly the long circumflex artery) '1 / also provide extraneural nutrient arterioles to the proximal intracranial oculomotor nerve. a Furthermore, we have also been able to con- firm the findings of Marinkovic and Gibo7 and Milisavljevic et al,8 that one of the circumflex arteries or a thalamoperforating artery can Fig 2B penetrate the proximal part of the oculomotor Figure 2 (A) Photograph ofproximal part of intracranial oculomotor nerve viewedfrom nerve. above. Demonstrates nerve beingpenetrated by thalamoperforating artery (A) and being The extraneural blood supply to the middle supplied by thalamoperforating vessels (B). Magnification X 10. (B) Drawing ofspecimen in (A). Demonstrates proximalpart ofoculomotor nerve with thalamoperforating artery part of the oculomotor nerve was both penetrating and supplying the nerve. Bas A=basilar artery, S CerA=superior more challenging.intracraNialNeither Dreyfus et al2 nor cerebellar artery, PCA =posterior cerebral artery, PerfA= Thalamoperforating arteries, Asbury et al 5 specifically examined this part of Sh Circum A=short circumflex artery, CP=, Sub Nigra=, 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 180 Cahill, Bannigan, Eustace

The final division we deal with is the distal

or intracavernous portion of the oculomotor Br J Ophthalmol: first published as 10.1136/bjo.80.2.177 on 1 February 1996. Downloaded from nerve. Parkinson3 9 carried out a major anatomical study on over 200 cadavers in the early 1960s. In this landmark study, he attempted 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 meningohypophyseal trunk' (Parkinson's nomenclature) supplied a nutrient arteriole to the oculomotor nerve. Parkinson named two other branches of the intracavernous internal carotid artery. He gave one the eponym 'McConnell's capsular artery' and the second the descriptive title 'the inferior cavernous sinus artery'. Parkinson did not comment as to whether or not either of these two branches supplied nutrient arterioles to the intracavernous oculomotor nerve. Asbury Fig 3A et al,5 utilising Parkinson's nomenclature demonstrated that non-specific branches of B the inferior cavernous sinus artery supplied nutrient arterioles to the intracavernous oculo- motor nerve. Two further studies are note- worthy.'1 12 The first one by Annabi et al,'I attempted to name the extraneural nutrient arterioles supplying the intracavernous oculo- motor nerve but unfortunately they did not use Parkinson's nomenclature. The second study was a topographical anatomical study to find a more workable nomenclature for the branches of the intracavernous internal carotid artery, Post Clin Proc which does not comment on the blood supply ' A2 ,! to the oculomotor nerve.'2 The present study utilises the nomenclature first outlined by Parkinson.3 10 Using clues from both Parkinson's3 l and Asbury's work,5 we systematically examined the extraneural http://bjo.bmj.com/ v Y0 qb TIV CN blood supply to the intracavernous oculomotor nerve. In our study reported in this paper, it has been demonstrated for the first time that Fig 3B the inferior cavernous sinus artery consistently Figure 3 (A) Photograph/ -of ;-;right cavernous sinus viewedfrom above. Demonstrates divides into four branches. We have named the trunk t~~~~~~~Tentthe ICA. Note anterior tentorial artery (B) meningohypophyseal (A) arisingfrom to the directions in which branches according on September 27, 2021 by guest. Protected copyright. supplying oculomotor nerve and tentorium. Magnification X 10. (B) Drawing of specimen in (A). Demonstrates meningohypophyseal trunk and itsfour branches. ICA=internal they were seen to travel. We have also shown carotid artery, D Men A=dorsal meningeal artery, Tent A1 =postenior tentorial artery, that of these four branches either an anterior Tent A2= anterior tentorial artery, InfHypo A=inferior hypophyseal artery, III branch, a tentorial branch, or both of these CN=oculomotor nerve, IV CN=, VI CN=, Post Clin Proc=posterior clinoid process, Pituitary=pituitary gland. branches supply the intracavernous oculo- motor nerve. In the majority of specimens dissected, the intracavernous oculomotor would arise from the adjacent posterior commu- nerve was also supplied by the tentorial branch nicating artery to supply the oculomotor nerve. ofthe meningohypophyseal trunk. This branch In fact, the middle part ofthe intracranial oculo- had previously been demonstrated by Parkin- motor nerve was not seen to receive nutrient son3 10 to supply the oculomotor nerve. arterioles from any vessels in any ofthe 1 1 spec- Unfortunately it can be confusing if small imens. Adams demonstrated that peripheral arterioles are given long titles with similarly nerves have excellent intraneural blood supplies named branches. However, Parkinson's origi- running within the epineurium.9 This extends nal nomenclature is that in common usage. from the proximal to distal parts ofthe nerve. At Thus in this paper we have used the terms regular intervals branches pierce the peri- 'meningohypophyseal trunk' and 'the inferior neurium and form longitudinal plexi of capil- cavernous sinus artery' and added the sub- laries between nerve fascicles. division 'tentorial branch' to both these simply The present study did not examine the intra- because it is a descriptive title and therefore neural blood supply of the intracranial oculo- more memorable. With regard to the extra- motor nerve. However, we conclude that the neural blood supply to the intracavernous absence of extraneural nutrient arterioles run- oculomotor nerve, we conclude that the ning onto the middle section ofthe oculomotor arterioles arising from the inferior cavernous nerve suggests that this section of the nerve is sinus artery are its main supply, as they are supplied by intraneural arterioles passing from consistently present. The arterioles arising its proximal and distal ends. from the meningohypophyseal trunk (namely Anatomy ofthe extraneural blood supply to the intracranial oculomotor nerve 181

the inferior hypophyseal artery, as determined

by McConnell in 1958.4 The inferior hypophy- Br J Ophthalmol: first published as 10.1136/bjo.80.2.177 on 1 February 1996. Downloaded from seal artery is one of the three branches of the meningohypophyseal trunk, the same trunk which gives a tentorial branch to supply the oculomotor nerve. Thus we postulate that a vascular event occurring in this trunk could cause damage to both the pituitary gland and the oculomotor nerve.

Conclusions A consistent pattern to the anatomy of the extraneural blood supply of the intracranial oculomotor nerve has been demonstrated. Proximally, the oculomotor nerve receives extraneural nutrient arterioles from the thalamoperforating arteries which are supple- mented by other nutrient arterioles from rzg 4vs brainstem vessels. The middle part of the intracranial oculomotor nerve does not receive B extraneural nutrient arterioles from adjacent arteries. The distal (intracavernous) part ofthe intracranial oculomotor nerve receives extra- neural nutrient arterioles from either the anterior branch, the tentorial branch, or both these branches of the inferior cavernous sinus artery. This may be supplemented by a ten- Tent Br torial branch of the meningohypophyseal .1" r III CN trunk. There is a close relation between the blood supply to the pituitary gland and the intracavernous oculomotor nerve - namely, the shared meningohypophyseal trunk. Post Br __ VI CN 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 portion

Desc Br ofthe carotid artery. JNeurosurg 1965; 23: 474-83. http://bjo.bmj.com/ 4 McConnell EM. The arterial blood supply of human hypophysis 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, Cabezudo Fig 4B Artero J, Berman SK, et al. Microvascular anatomy of the Figure 4 (A) Photograph of right cavernous sinus viewedfrom the right side. . J Neurosurg 1986; 64: 484-93. Demonstrates the inferior cavernous sinus artery and its branches (A). Note tentorial 7 Marinkovic S, Gibo H. The neurovascular relationship and the blood supply of the oculomotor nerve: the micro- branch oculomotor nerve X 10. in on September 27, 2021 by guest. Protected copyright. supplying (B). Magnification (B) Drawing ofspecimen surgical anatomy of its cisternal segment. Surg Neurol (A). Demonstrates thefour branches ofthe inferior cavernous sinus artery. ICA = internal 1994; 42: 505-16. carotid artery, Tent Br=tentorial branch, Ant Br= anterior branch, Post Br=posterior 8 Milisavljevic M, Marinkovic S, Lolic Draganic V, branch, Desc Br= descending branch, a and b=branches of tentorial branches supplying Kovacevic M. Oculomotor, trochlear and abducens oculomotor nerve, III CN=oculomotor nerve, IV CN= trochlear nerve, VI CN=abducens nerves penetrated by cerebral vessels. Arch Neurol 1986; nerve. 43: 505-16. 9 Adams WE. The blood supply of nerves II. The effects of exclusion of its regional sources of supply on the sciatic nerve of the rabbit. JAnat 1943; 77: 243-50. the anterior tentorial branch) provide supple- 10 Parkinson D. Collateral circulation of cavernous carotid mentary blood supply to the oculomotor nerve. artery: anatomy. CanJ Surg 1964; 7: 251-68. we come to 11 Annabi A, Lasjaunias P, Lapresle J. Paralysies de la IIIe Finally, the relation between the paire au cours du diabete et vascularisation du moteur blood supply to the pituitary gland and that to oculaire common. JNeurol Sci 1979; 41: 359-67. 12 Tran-Dinh H. Cavernous branches of the internal carotid the intracavernous oculomotor nerve. A large artery: anatomy and nomenclature. Neurosurgery 1987; part of the pituitary blood supply arises from 20: 205-10.