Anatomy of the Extraneural Blood Supply to the Intracranial

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Anatomy of the Extraneural Blood Supply to the Intracranial 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 nerve 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 brainstem, cranial nerves 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 oculomotor nerve 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 cavernous sinus 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 midbrain, pons, College Dublin, Dublin, Ireland Bartholdy, in 1897, first described that cranial cerebellum, cranial nerves 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
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