the neurovascular relationships of the oculomotor nerve

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ORIGINAL COMMUNICATION The Neurovascular Relationships of the Oculomotor Nerve ALI FIRAT ESMER, TULIN SEN, * AYHAN COMERT, ERAY TUCCAR, AND SULEYMAN TUNA KARAHAN Department of Anatomy, Ankara University School of Medicine, Ankara, Turkey In this study, the arterial supply of the cisternal (initial) and the subcavernous parts of the oculomotor nerve (ON) and the relation between the nerve and adjacent vascular structures like posterior cerebral artery (PCA) and superior cerebellar artery (SCA) were investigated. A total of 140 formalin fixed hemi- spheres from 70 human cadaveric brains were examined. The nutrient branches reaching the cisternal and subcavernous parts of the ON were inves- tigated, along with branches of adjacent vascular structures penetrating the nerve and passing through it. In the material examined, the ON, after arising from the midbrain, mostly continues laterally between PCA and SCA or between PCA and the rostral SCA trunk. However, in three hemispheres of our specimens, the ON run between the rostral and caudal SCA trunks. We observed that the branches of PCA-P1 segment supplied the cisternal part of the ON in all specimens. In one specimen, the cisternal part of the ON was supplied by a branch arising from the rostral SCA trunk which was also origi- nating from PCA. Differently, in four hemispheres, branches arising from PCA or SCA perforated the cisternal part of the ON and passed through it. We also observed a tortuous caudal trunk of duplicated SCA in one of our specimens and considered it as a rare variation. The anatomy of the ON and its vascular relations is significant in terms of not only understanding the compression syn- dromes and its vascular dysfunctions, but the exact diagnosis and treatment as well. Clin. Anat. 24:583–589, 2011. V V C 2011 Wiley-Liss, Inc. Key words: oculomotor nerve; posterior cerebral artery; superior cerebellar artery INTRODUCTION The oculomotor nerve emergences from the mid- brain on the medial side of the cerebral peduncles. It extends forward and laterally between the posterior cerebral artery (PCA) and superior cerebellar artery (SCA). Marinkovic and Gibo (1994) divided this nerve into four parts. The cisternal (initial) part is located between the medial sulcus of crus cerebri and the anterior surface of the P2 segment of PCA. The subcavernous part is covered by an arachnoidal sheath and continuous through the cavernous sinus. The intracavernous part courses through the cavern- ous sinus and lastly, the orbital part is located in the orbital cavity, where the oculomotor nerve enters through the superior orbital fissure after exiting the cavernous sinus. The compression syndromes and vascular dysfunctions of the ON manifest itself by clear symptoms involving eyeball movements and pupillary size changes (Good, 1990; Horiuchi et al., 1997; Hashimoto et al., 1998; Bonnaud and Salama, 2003; Taylor et al., 2003; Albayram et al., 2006; Suzuki et al., 2008). Although the compression of this nerve by cerebral aneurysm is common, some oculomotor palsies caused by the compression of blood vessels have been reported in previous studies *Correspondence to: Tulin Sen, Department of Anatomy, Ankara University School of Medicine, Sihhiye-Ankara, Turkey 06100. E-mail: [email protected] Received 30 April 2009; Revised 22 September 2009; Accepted 29 October 2010 Published online 20 January 2011 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/ca.21111 V V C 2011 Wiley-Liss, Inc. Clinical Anatomy 24:583–589 (2011)

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Page 1: The neurovascular relationships of the oculomotor nerve

ORIGINAL COMMUNICATION

The Neurovascular Relationships of theOculomotor Nerve

ALI FIRAT ESMER, TULIN SEN,* AYHAN COMERT, ERAY TUCCAR,AND SULEYMAN TUNA KARAHAN

Department of Anatomy, Ankara University School of Medicine, Ankara, Turkey

In this study, the arterial supply of the cisternal (initial) and the subcavernousparts of the oculomotor nerve (ON) and the relation between the nerve andadjacent vascular structures like posterior cerebral artery (PCA) and superiorcerebellar artery (SCA) were investigated. A total of 140 formalin fixed hemi-spheres from 70 human cadaveric brains were examined. The nutrientbranches reaching the cisternal and subcavernous parts of the ON were inves-tigated, along with branches of adjacent vascular structures penetrating thenerve and passing through it. In the material examined, the ON, after arisingfrom the midbrain, mostly continues laterally between PCA and SCA orbetween PCA and the rostral SCA trunk. However, in three hemispheres of ourspecimens, the ON run between the rostral and caudal SCA trunks. Weobserved that the branches of PCA-P1 segment supplied the cisternal part ofthe ON in all specimens. In one specimen, the cisternal part of the ON wassupplied by a branch arising from the rostral SCA trunk which was also origi-nating from PCA. Differently, in four hemispheres, branches arising from PCAor SCA perforated the cisternal part of the ON and passed through it. We alsoobserved a tortuous caudal trunk of duplicated SCA in one of our specimensand considered it as a rare variation. The anatomy of the ON and its vascularrelations is significant in terms of not only understanding the compression syn-dromes and its vascular dysfunctions, but the exact diagnosis and treatmentas well. Clin. Anat. 24:583–589, 2011. VVC 2011 Wiley-Liss, Inc.

Key words: oculomotor nerve; posterior cerebral artery; superior cerebellarartery

INTRODUCTION

The oculomotor nerve emergences from the mid-brain on the medial side of the cerebral peduncles. Itextends forward and laterally between the posteriorcerebral artery (PCA) and superior cerebellar artery(SCA). Marinkovic and Gibo (1994) divided thisnerve into four parts. The cisternal (initial) part islocated between the medial sulcus of crus cerebriand the anterior surface of the P2 segment of PCA.The subcavernous part is covered by an arachnoidalsheath and continuous through the cavernous sinus.The intracavernous part courses through the cavern-ous sinus and lastly, the orbital part is located in theorbital cavity, where the oculomotor nerve entersthrough the superior orbital fissure after exiting thecavernous sinus. The compression syndromes andvascular dysfunctions of the ON manifest itself by

clear symptoms involving eyeball movements andpupillary size changes (Good, 1990; Horiuchi et al.,1997; Hashimoto et al., 1998; Bonnaud and Salama,2003; Taylor et al., 2003; Albayram et al., 2006;Suzuki et al., 2008). Although the compression ofthis nerve by cerebral aneurysm is common, someoculomotor palsies caused by the compression ofblood vessels have been reported in previous studies

*Correspondence to: Tulin Sen, Department of Anatomy, AnkaraUniversity School of Medicine, Sihhiye-Ankara, Turkey 06100.E-mail: [email protected]

Received 30 April 2009; Revised 22 September 2009; Accepted29 October 2010

Published online 20 January 2011 in Wiley Online Library(wileyonlinelibrary.com). DOI 10.1002/ca.21111

VVC 2011 Wiley-Liss, Inc.

Clinical Anatomy 24:583–589 (2011)

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Fig. 2. BA, basilar artery; PCA, posterior cerebral artery; SCA, superior cerebel-lar artery; III, oculomotor nerve; PCoA, posterior communicating artery; arrow-heads: branches PCA-P1 segment, which supplied the cisternal part of ON. [Color fig-ure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig. 1. BA, basilar artery; PCA, posterior cerebral artery; SCA, superior cerebel-lar artery; R, rostral SCA trunk; C, Caudal SCA trunk; III, oculomotor nerve; PCoA,posterior communicating artery; arrowheads: circumflex perforator branch of SCApenetrating the ON and passing through it. [Color figure can be viewed in the onlineissue, which is available at wileyonlinelibrary.com.]

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(Nakagawa et al., 1991; Hashimoto et al., 1998;Albayram et al., 2006; Suzuki et al., 2008). There-fore, the compression of ON between the PCA andSCA can cause the oculomotor palsy. Thus, in thisstudy, we observed the arterial supply of the cister-nal and the subcavernous parts of the ON and inves-tigated the relation between these parts of the nerveand adjacent vascular structures like PCA and SCA.

MATERIALS AND METHODS

A total of 140 hemispheres of 70 adult humancadaveric brains were investigated. Brains wereobtained from routine autopsies. Internal carotid andbasilar arteries were cannulated and injected withcolored latex. Then, the brains were embalmed informaldehyde. The dissections were performed usingmicrosurgical instruments and a surgical microscope(Opmi 99; Carl Zeiss, Gottingen, Germany). Thelength between the beginning part of the PCA andSCA and the point where they contact the oculomo-tor nerve was measured. All measurements wereperformed with a digital caliper. SPSS (StatisticalProgram for Social Sciences) for Windows version15.0 was used in statistical analyses. A P value <0.05 was considered significant. The overall meas-urements were evaluated with Wilcoxon SignedRanks Test. The arterial branches which reached thecisternal and subcavernous part of the oculomotornerve were investigated.

RESULTS

In our samples, the oculomotor nerve arose fromthe midbrain in all hemispheres and it continued lat-erally between PCA and SCA or PCA and the rostralSCA trunk. However, in three hemispheres, the ocu-lomotor nerve extended between the rostral andcaudal SCA trunks (2.14%) and in addition to this,the rostral SCA trunk originating from PCA was arare variation we observed in these three hemi-spheres (Fig. 1).

The rostral surface of the oculomotor nerve had aclose relationship with P1 and P2 segments of thePCA and the caudal surface was closely related withthe SCA or its rostral trunk in the remaining 137hemispheres (97.86%).

The distance between the SCA origin or its rostraltrunk and the point where they contacted the caudalsurface of ON was 4.36 6 1.59 mm (min: 1.79,max: 7.83) on the right side and 4.36 6 1.48 mm(min: 1.07, max: 7.80) on the left side. No statisti-cally significant difference was observed betweentwo sides by Wilcoxon Signed Ranks Test (P ¼ 0.994,P > 0.05). Also, the distance between the origin ofthe PCA and its contact point with the rostral surfaceof the oculomotor nerve was 4.47 6 1.39 (min:1.87, max: 7.94) and 4.43 6 1.47 (min: 1.43, max:8.12) on the right and left sides, respectively,whereas no significant difference between two sidescould be revealed (P ¼ 0.892, P > 0.05).

In this study, we observed that the branches ofPCA-P1 segment supplied the cisternal part of the

oculomotor nerve in all specimens (Fig. 2). In onespecimen, the cisternal part of the oculomotor nervewas supplied by a branch arising from the rostralSCA trunk, which was originating from PCA as an un-usual case (Fig. 3).

When the perforators originating from PCA-P1were investigated, it was revealed that some perfo-rator branches were supplying the subcavernouspart in only 27 hemispheres and they were narrowerthan the perforators of the cisternal part (Fig. 4).

Additionally, we observed that the beginning partof the ON was perforated by some branches arisingfrom PCA. They perforated the nerve and passedthrough it differently. In two specimens, left oculo-motor nerves were perforated by a branch of poste-rior cerebral artery unilaterally (Fig. 5A) and inanother specimen, oculomotor nerves were perfo-rated bilaterally (Fig. 5B). These branches originatedfrom PCA-P1.

Except these samples, we noted an uncommoncase in another specimen with duplicated right SCA.Although the caudal trunk originated from the basilarartery (BA), the rostral trunk originated from PCAand gave a circumflex perforator branch penetratingthe ON (Fig. 1).

In one of the specimens, a tortuous caudal trunkof duplicated SCA was also observed. Here, the cau-dal trunk had an abnormal curly pattern as a rarevariation, whereas the rostral trunk coursed normally(Fig. 6).

DISCUSSION

The ON originates from the midbrain and usuallyextends between PCA and SCA. The relation of ONwith PCA and SCA was previously investigated bysome researchers. They commented that identifyingthe ON could be useful for discriminating these arteriesduring surgery (Mani et al., 1968; Caruso et al.,1991). We observed that the oculomotor nerve runbetween the rostral and caudal SCA trunks in threespecimens (2.14%). Additionally, some researchersdenoted that SCA or its branches can run superior tothe ON (Hardy et al., 1980; Uchino et al., 2003a).Therefore, using the ON to discriminate, these arteriescan lead to mistakes in diagnosis or therapy.

Cerebral aneurysms are major vascular causes ofoculomotor palsy (Good, 1990; Kanser et al., 1997;Taylor et al., 2003). The oculomotor nerve dysfunc-tion due to arterial compression without aneurysmswas mentioned by some researchers (Hashimoto etal., 1998; Albayram et al., 2006; Suzuki et al.,2008). Uchino et al. (2003a) pointed out thatanomalies of the SCA can cause ON compression. Inmost of our specimens, PCA and SCA were closelyrelated with the ON, so it is likely that these arteriescan compress the ON in the absence of any pathol-ogy such as aneurysm or atherosclerosis.

So far, it has been mentioned many times that thecisternal (initial) part of the ON was penetrated andsupplied by various branches of the PCA. Thesebranches were thin arteries such as perforating ves-sels of the PCA, the circumflex mesencephalic artery,the short circumflex artery, thalamoperforating

585Proximal Parts of the Oculomotor Nerve

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Fig. 4. PCA, posterior cerebral artery; SCA, superior cerebellar artery; BA, basi-lar artery; III, oculomotor nerve; arrowheads: perforator branch arising from PCA-P1 segment and supplying the subcavernous part of ON. [Color figure can beviewed in the online issue, which is available at wileyonlinelibrary.com.]

Fig. 3. BA, basilar artery; PCA, posterior cerebral artery; R, rostral SCA trunk;C, Caudal SCA trunk; III, oculomotor nerve; PCoA, posterior communicating artery;arrowheads: branches of the rostral SCA trunk originating from PCA, which suppliedthe cisternal part of the nerve. [Color figure can be viewed in the online issue, whichis available at wileyonlinelibrary.com.]

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Fig. 5. BA, basilar artery; PCA, posterior cerebral artery; SCA, superior cerebel-lar artery; III, oculomotor nerve. A: Arrowheads: branches arising from PCA pene-trated the ON and passed through it on the left side. B: PCoA, posterior communi-cating artery; arrowheads: branches arising from PCA penetrated the ON andpassed through it bilaterally. [Color figure can be viewed in the online issue, whichis available at wileyonlinelibrary.com.]

587Proximal Parts of the Oculomotor Nerve

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arteries, or collicular arteries (Milisavljevic et al.,1986; Marinkovic and Gibo, 1994; Uz and Tekdemir,2006). In this study, our findings were similar to theprevious studies. On the other hand, we observedthat the branches arising from the rostral SCA trunkcontributed to the ON supply in addition to thePCA branches. This was not shown before and wasonly observed in one case of our whole specimenrange.

We also observed some branches perforating theoculomotor nerve and passing through it in fourspecimens; one of them was bilateral and the otherswere unilateral. These branches, which were notmentioned in the literature previously, arose fromPCA or SCA. It is likely that these branches cancause ON dysfunction.

In the literature, there is only one radiologicalstudy indicating the tortuous initial part of SCA. Theresearchers denoted that the clinicians must beaware of tortuous SCA and its risk of misdiagnosiswith arteriovenous malformations (Uchino et al.,2003b). We observed a tortuous caudal trunk ofduplicated SCA in one of our specimens and thoughtthat this can cause ON compression.

CONCLUSIONS

The anatomy of the oculomotor nerve and its vas-cular relationships is significant for not only under-standing compression syndromes but also for theexact diagnosis and treatment. Consequently, in this

study, we enlightened the relationship between theoculomotor nerve and its adjacent vascular struc-tures.

REFERENCES

Albayram S, Ozer H, Sarici A, Murphy K, Miller N. 2006. Unilat-eral mydriasis without ophthalmoplegia—A sign of neuro-vascular compression? Case report. Neurosurgery 58:E582–E583.

Bonnaud I, Salama J. 2003. An ischemic syndrome of the oculomo-tor nucleus: Associated clinical and anatomical variations on atheme. Rev Neurol 159:781–785.

Caruso G, Vincentelli F, Rabehanta P, Giudicelli G, Grisoli F. 1991.Anomalies of the P1 segment of the posterior cerebralartery: Early bifurcation or duplication, fenestration, commontrunk with the superior cerebellar artery. Acta Neurochir109:66–71.

Good EF. 1990. Ptosis as the sole manifestation of compression ofthe oculomotor nerve by an aneurysm of the posterior communi-cating artery. J Clin Neuroophthalmol 10:59–61.

Hardy DG, Peace DA, Rhoton AL Jr. 1980. Microsurgical anatomy ofthe superior cerebellar artery. Neurosurgery 6:10–28.

Hashimoto M, Ohtsuka K, Akiba H, Harada K. 1998. Vascularcompression of the oculomotor nerve disclosed by thin-slice magnetic resonance imaging. Am J Ophthalmol 125:881–882.

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Kasner SE, Liu GT, Galeta SL. 1997. Neuro-ophthalmologic aspectsof aneurysms. Neuroimaging Clin N Am 7:679–692.

Fig. 6. BA, basilar artery; AICA, anterior inferior cerebellar artery; R, rostral SCAtrunk; C, Caudal SCA trunk; asterisk: caudal SCA trunk with a curly pattern. [Colorfigure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

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Mani RL, Newton TH, Glickman MG. 1968. The superior cerebellarartery: An anatomic-roentgenographic correlation. Radiology91:1102–1108.

Marinkovic SV, Gibo H. 1994. The neurovascular relationships andthe blood supply of the oculomotor nerve: The microsurgicalanatomy of its cisternal segment. Surg Neurol 42:505–516.

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Nakagawa H, Nakajima S, Nakajima Y, Furuta Y, Nishi O, Nishi K.1991. Bilateral oculomotor nerve palsies due to posterior cere-bral arterial compression relieved by microvascular decompres-sion—Case report. Neurol Med Chir 31:45–48.

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589Proximal Parts of the Oculomotor Nerve