Clinical Anatomy 27:108–117 (2014)

REVIEW

Arterial Supply of the Lower Cranial Nerves: A Comprehensive Review PHILIPP HENDRIX,1 CHRISTOPH J. GRIESSENAUER,1 PAUL FOREMAN,1 MARIOS LOUKAS,2 WINFIELD S. FISHER III,1 ELIAS RIZK,3 MOHAMMADALI M. SHOJA,3 2,3* AND R. SHANE TUBBS 1

Division of Neurosurgery, Department of Surgery, University of Alabama at Birmingham, Birmingham, Alabama 2 Department of Anatomical Sciences, St. George’s University, Grenada 3 Pediatric Neurosurgery, Children’s Hospital, Birmingham, Alabama

The lower cranial nerves receive their arterial supply from an intricate network of tributaries derived from the external carotid, internal carotid, and vertebrobasilar territories. A contemporary, comprehensive literature review of the vascular supply of the lower cranial nerves was performed. The vascular supply to the trigeminal, facial, vestibulocochlear, glossopharyngeal, vagus, spinal accessory, and hypoglossal nerves are illustrated with a special emphasis on clinical issues. Frequently the external carotid, internal carotid, and vertebrobasilar territories all contribute to the vascular supply of an individual cranial nerve along its course. Understanding of the vasculature of the lower cranial nerves is of great relevance for skull base surgery. Clin. Anat. 27:108–117, 2014. VC 2013 Wiley Periodicals, Inc. Key words: arterial supply; blood supply; cranial nerves; neurosurgery; skull base

INTRODUCTION The current literature regarding the blood supply of individual cranial nerves is sparse and lacks a contemporary, comprehensive review. Understanding of the vasculature of the cranial nerves, however, is of great relevance for skull base surgery as surgical approaches to the posterior cranial fossa and cerebellopontine angle pose a risk of postoperative cranial nerve paralysis. Mechanisms of intraoperative nerve injury include direct injury from stretch or pinch with surgical instruments, but have also been observed in the absence of direct cranial nerve manipulation and attributed to ischemia from iatrogenic injury to regional vessels and thin branches supplying the cranial nerves (Calcaterra et al., 1976; Kretschmer et al., 2009). In the 18th century, Albrecht von Haller (1756) was the first to describe the basic principles of the arterial supply to peripheral nerves. In 1897, Bartholdy also reported on the blood supply to the cranial nerves. He described nutrient vessels that arose from nearby arteries that traverse the epineurium and ramify

C V

2013 Wiley Periodicals, Inc.

within the perineurium to supply these nerves. These terminal branches are referred to as vasa nervorum (Adams, 1942). More current work on the blood supply of peripheral nerves describes a vascular plexus running parallel to the fibers that can be divided in two separate, functionally independent, but anastomozing, vascular systems: an epineural extrinsic system supplied by regional nutritive vessels and an endoneurial intrinsic system of microvessels running longitudinally with nerve fibers (Wigley, 2008). Here, we provide a contemporary, comprehensive review of the literature on the arterial supply of the lower cranial nerves with a special emphasis on clinical considerations (Fig. 1; Table 1). *Correspondence to: R. Shane Tubbs, Pediatric Neurosurgery, Children’s of Alabama, Birmingham, AL 35233. E-mail: [email protected] Received 30 July 2013; Revised 8 August 2013; Accepted 11 August 2013 Published online 21 October 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/ca.22318

Arterial Supply of the Lower Cranial Nerves

109

Fig. 1. Frontal view of brain stem showing the vertebral and basilar arteries and arterial supply of the lower cranial nerves after Leblanc (Leblanc, 2000). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

TRIGEMINAL NERVE (V) Intracranial Segments The trigeminal sensory and motor nerve roots exit the brainstem at the anterolateral aspect of the pons. At this level, the arterial supply is provided by 2–6 trigeminal arteries that form a vascular network around the trigeminal nerve roots, have a diameter of about 100–500 lm, and frequently form vascular rings around the roots (Marinkovic and Gibo, 1995; Cetkovic ´ et al., 2011). These vascular rings are located proximal and distal at the trigeminal root entry zone and the middle portion of the trigeminal nerve root before the level of its entrance into the arachnoid sleeve, respectively. The proximal vascular ring is the origin of small branches extending along the trigeminal nerve root longitudinally and distally as well as proximally, entering the pons, and supplying the trigeminal brain stem nuclei (Cetkovic ´ et al., 2011). The parent vessels of the vessels supplying the trigeminal nerve include the superior cerebellar artery (SCA), the posterolateral, superolateral, and inferolateral arteries, and the anterior inferior cerebellar artery (AICA), all branches of the basilar artery. In rare instances, the blood supply to the trigeminal arteries comes from the trigeminal segment of the trigeminocerebellar artery, a direct branch to the trigeminal root from the basilar artery. Most frequently, the superolateral pontine artery and the peduncular cerebellar branch of AICA supply the trigeminal artery network and commonly give rise to more than one trigeminal artery each while

the other parent vessels listed usually give rise to only one trigeminal artery branch. The blood supply to the motor portion, exiting the pons anterosuperomedial to the senory portion, and the rostral part of the sensory portion of the trigeminal nerve, corresponding to the ophthalmic nerve (V1), most often comes from the superolateral pontine artery. The superolateral pontine artery, inferolateral pontine artery, and the peduncular cerebellar branch of AICA supply the sensory portion corresponding to the maxillary nerve (V2). The mandibular division (V3) is commonly perfused by the peduncular cerebellar branch of AICA (Marinkovic and Gibo, 1995). According to Rhoton, recurrent perforating arteries of AICA travel with the facial and vestibulocochlear nerve toward the internal auditory meatus before taking a recurrent course to reach the pons and the entry zone of the trigeminal nerve (Rhoton, 2000a). Other studies on the arterial supply of the trigeminal nerve root have yielded comparable results (Haynes, 1896; Stopford, 1916; Grigorowsky, 1928; Leblanc, 2000). Additionally, external carotid artery (ECA) branches including the cavernous branch of the middle meningeal artery and the carotid branch of the ascending pharyngeal artery supply the trigeminal nerve while passing through the trigeminal cistern (Lasjaunias and Berenstein, 1987).

Gasserian Ganglion The Gasserian ganglion, located in Meckel’s cave, contains the sensory neurons for the three peripheral

110

Hendrix et al.

TABLE 1. Most Important Arteries Supplying the Lower Cranial Nerves Cranial nerve

Intracranial supply

Extracranial supply

Trigeminal nerve

Superior cerebellar, posterolateral, superolateral, inferolateral, anterior inferior cerebellar, trigeminocerebellar artery (basilar artery)/inferolateral, meningohypophyseal trunk (internal carotid artery)/middle meningeal, ascending pharyngeal artery (external carotid artery).

Facial nerve

Anterior inferior cerebellar, labyrinthine artery (basilar artery)/petrosal branch of middle meningeal artery, stylomastoid artery, tympanic arteries (external carotid artery). Anterior inferior cerebellar, labyrinthine, basilar, vertebral artery Labyrinth: Posterior cochlear, vestibulocochlear (common cochlear artery), anterior vestibular artery. Artery of glossophayrngeal nerve (artery of lateral fossula) (vertebral, basilar, and middle meningeal artery), neuromeningeal trunk (external carotid artery). Artery of lateral fossula (vertebral, basilar, and middle meningeal artery), neuromeningeal trunk (external carotid artery).

V1: Anteromedial branch of inferolateral trunk (internal carotid artery)/lacrimal, supraorbital, ethmoidal arteries (ophthalmic artery). V2: Anterolateral branch of inferolateral trunk, artery of foramen rotundum (internal carotid artery)/Accessory meningeal, middle meningeal, infraorbital artery (external carotid artery). V3: Posteromedial branch of inferolateral trunk, artery of foramen ovale (internal carotid artery)/Accessory meningeal, middle meningeal, lingual artery (external carotid arteries). Posterior auricular, occipital superficial temporal, facial, maxillary artery (external carotid artery).

Vestibulocochlear nerve Glossopharyngeal nerve Vagus nerve

Spinal accessory nerve Hypoglossal nerve

Posterior inferior cerebellar, muscolospinal and neuromeningeal trunk (ascending pharyngeal artery), anterior and posterior spinal arteries Anterior spinal artery, posterior inferior cerebellar, vertebral artery, posterior meningeal artery (vertebral artery), neuromeningeal trunk (external carotid artery).

trigeminal branches and the motor fibers located medial to the sensory fibers in the ganglion (Rhoton, 2000b). The cavernous internal carotid artery (ICA) gives rise to the inferolateral trunk, a remnant of the dorsal ophthalmic artery, which is of particular significance for the arterial supply of the Gasserian ganglion and has prominent anastomotic connections to the ECA system via the accessory and middle meningeal arteries, branches of the maxillary artery (Grigorowsky, 1928; Capo et al., 1991). Four distinct branches of the inferolateral trunk have been described (Lapresle and Lasjaunias, 1986). The superior branch supplies the oculomotor and trochlear nerves in the cavernous sinus and gives rise to the marginal tentorial artery. The anteromedial branch gives rise to the artery to the superior orbital fissure and has an anastomotic connection to the intraorbital ophthalmic artery via the deep recurrent ophthalmic artery and the anterolateral branch that terminates as the artery of the foramen rotundum and anastomoses with the foramen rotundum branch of the maxillary artery and the temporal rami of the middle meningeal artery. The posterior

Ascending pharyngeal, occipital, descending palatine, sphenopalatine, ascending palatine, and dorsal lingual artery (external carotid artery). Internal carotid, external carotid, common carotid, posterior meningeal artery (vertebral artery), vagal artery (inferior thyroid artery), vertebral, internal thoracic, bronchial, esophageal artery, aorta. Occipital, lingual artery (external carotid artery). Ascending pharyngeal, occipital, facial, lingual artery (external carotid artery), external carotid artery.

branch bifurcates into a posteromedial, or artery of the foramen ovale, and posterolateral branch to the Gasserian ganglion and anastomoses with the accessory meningeal artery via the foramen ovale and cavernous branch of the middle meningeal artery, respectively (Grigorowsky, 1928; Lasjaunias et al., 1977; Lapresle and Lasjaunias, 1986; Leblanc, 2000). While the entire Gasserian ganglion is supplied by the inferolateral trunk, the medial third of the ganglion also receives blood supply from the tentorial artery of the meningohypophyseal trunk of the cavernous ICA and the lateral third from branches of the middle meningeal artery (Krisht et al., 1994; Fig. 2).

Ophthalmic Nerve (V1) The nerve roots corresponding to the ophthalmic nerve (V1) are supplied by the superolateral pontine artery at the pontine entry zone (Marinkovic and Gibo, 1995). In the middle cranial fossa, the anteromedial branch of the inferolateral trunk and its tributaries, the

Arterial Supply of the Lower Cranial Nerves

111

Fig. 2. Intracranial perspective of the arterial supply of the gasserian ganglion after Leblanc (Leblanc, 2000). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

artery to the superior orbital fissure, and the deep recurrent ophthalmic artery, provide blood supply to V1 as it courses into the orbit (Lapresle and Lasjaunias, 1986; Krisht et al., 1994). Within the orbit, small vessels of the ophthalmic artery and its subdivisions, the lacrimal, supraorbital, and ethmoidal arteries supply the lacrimal nerve, frontal nerve, and nasociliary nerve, respectively (Grigorowsky, 1928; Leblanc, 2000).

Maxillary Nerve (V2) The nerve roots of the maxillary nerve (V2) are proximally supplied by the superolateral and inferolateral pontine arteries and the peduncular cerebellar branch of AICA at the level of the pons (Marinkovic and Gibo, 1995). In the middle cranial fossa, V2 receives blood supply from the artery to the foramen rotundum, the anterolateral branch of the inferolateral trunk (Lasjaunias and Berenstein, 1987; Krisht et al., 1994; Leblanc, 2000). The accessory meningeal and middle meningeal arteries provide additional blood supply. In the pterygopalatine fossa, V2 is supplied by branches of the maxillary artery including the infraorbital artery as it traverses the corresponding foramen (Lapresle and Lasjaunias, 1986; Leblanc, 2000).

Mandibular Nerve (V3) The nerve roots of the mandibular nerve (V3) are supplied by the peduncular cerebellar branch of AICA (Marinkovic and Gibo, 1995). Distal to the Gasserian ganglion an arterial network composed of the posteromedial branch of the inferolateral trunk, the artery of the foramen ovale, the accessory meningeal artery, and the middle meningeal artery provide the arterial supply of V3 including its sensory branches, the lingual, inferior alveolar, auriculotemporal, and buccal nerves (Lasjaunias and Berenstein, 1987; Leblanc, 2000). The lingual nerve and submandibular ganglion are supplied by terminal branches of the lingual artery, the sublingual and deep lingual arteries, all branches of the ECA (Grigorowsky, 1928; Fig. 3).

Clinical Considerations of the Trigeminal Nerve Vascular Supply Trigeminal neuralgia is a condition characterized by sudden, brief episodes of electric shock-like facial pain confined to the distribution of one or more branches of the trigeminal nerve. The pathophysiology has been associated with arterial compression of the

112

Hendrix et al.

Fig. 3. Extracranial perspective of the arterial supply of the gasserian ganglion and mandibular nerve after Leblanc (Leblanc, 2000). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

trigeminal nerve at the root entry zone trigeminal root territory in up to 80% of cases (Thomas and Vilensky, 2013). The SCA and AICA are the most common vessels found compressing the trigeminal nerve in these patients (Barker et al., 1996; Marinkovic and Gibo, 1995; Cetkovic ´ et al., 2011). With advancements in radiological imaging, particularly MR angiography (MRA), MR cisternography, and other sequence modifications, correlations of imaging findings and trigeminal neuralgia symptoms has been an area of widespread interest (Zeng et al., 2013).

FACIAL NERVE (VII) Intracranial The facial nerve consists of a motor root located anterior and superior to the sensory and parasympathetic part, the nervus intermedius. Both exit the medulla oblongata lateral to the inferior olive and course laterally to enter the internal auditory meatus. On its course through the fallopian canal in the temporal bone, the facial nerve is surrounded by a distinct arterial network (Blunt, 1954) that is susceptible to compression from pathology resulting in nerve edema, particularly as the canal gets progressively narrower from the meatus to the stylomastoid foramen (Haynes, 1955; Anson et al., 1973). The roots and cisternal segment of the facial nerve are supplied by branches of the vertebrobasilar system, particularly

AICA branches (Blunt, 1954; Lasjaunias and Berenstein, 1987). The labyrinthine artery, or internal auditory artery, usually originates from AICA and supplies the cisternal, meatal, and labyrinthine segments (Brunsteins and Ferreri, 1995; Leblanc, 2000). At the geniculate ganglion, the greater petrosal nerve separates from the facial nerve and receives vascular supply from the petrosal branch of the middle meningeal artery (Leblanc, 2000; El-Khouly et al., 2008). Distal to the geniculate ganglion, the tympanic and mastoid segments of the nerve are supplied by an anastomotic arterial network that receives input from the ECA territory. The stylomastoid artery ascends as a branch of the posterior auricular artery, in 60–70% of patients, or the occipital artery, and enters the facial canal via the stylomastoid foramen on the medial side of the nerve (Blunt, 1954; Monkhouse, 1990). Within the canal, the stylomastoid artery forms a loop. At the convexity of the loop it gives rise to two branches. The shorter branch gives rise to small twigs that pierce the canal in company with the auricular branch of the vagus nerve. The longer branch accompanies the facial nerve on its medial wall along the tympanic and mastoid segments to the geniculate ganglion where it enters the hiatus for the greater petrosal nerve and anastomoses with the petrosal branch of the middle meningeal artery to form a complete arterial arcade within the facial canal (Blunt, 1954; Lasjaunias and Berenstein, 1987). Collaterals of the stylomastoid artery also provide blood supply to the

Arterial Supply of the Lower Cranial Nerves chorda tympani (Monkhouse, 1990; Leblanc, 2000). Along the course of the facial nerve, the vascular network communicates with the blood vessels of bone marrow surrounding the canal, as well as those of the mucous membranes of the tympanic cavity. These arteries also leave the canal and spread along the labyrinthine part of the middle ear where they communicate with the anterior and superior tympanic branches of the maxillary artery, the posterior tympanic branch of the posterior auricular artery, and the inferior tympanic branch of the ascending pharyngeal artery (Anson et al., 1973).

Extracranial Extracranially, posterior auricular and occipital arteries and branches, including the stylomastoid artery, supply the facial nerve along its course to the parotid gland. The superior and middle portions of the extracranial facial nerve are vascularized by the superficial temporal artery and its branches including the transverse facial artery. Rami parotidei of the external carotid artery supply the middle and inferior portions. The latter portion is also supplied by collaterals of the facial and maxillary arteries (Grigorowsky, 1928; Leblanc, 2000).

VESTIBULOCOCHLEAR NERVE (VIII) The vestibulocochlear nerve enters the brainstem in close proximity to the facial nerve and shares the arterial supply of the facial nerve in the pontine cistern. Branches of the basilar artery, vertebral artery, and AICA supply the nerve root (Stopford, 1916; Grigorowsky, 1928; Lasjaunias and Berenstein, 1987; Leblanc, 2000). Bartholdy (1897) also found that the posterior spinal arteries provide vascular supply to the root. The labyrinthine arteries, or internal auditory arteries, most commonly arise from AICA, occasionally from the basilar artery, and accompany both the facial and vestibulocochlear nerves. In about 1/3 of patients, one labyrinthine artery originates outside of the internal acoustic meatus and is found on the cochlear nerve below the facial nerve ending in the fundus of the internal acoustic meatus between the cochlear and vestibular nerves. In about 2/3 of patients, two labyrinthine arteries are found. The inferior branch has its origin outside of the meatus and courses under the vestibulocochlear nerve and terminates as the vestibulocochlear artery at the fundus of the meatus whereas the superior branch may originate outside or within the meatus and follows a course similar to the labyrinthine artery in the monoarterial system ending as the cochlear and anterior vestibular artery (Brunsteins and Ferreri, 1995). The labyrinthine artery in the monoarterial system terminates at the fundus of the meatus and divides into the common cochlear artery and the anterior vestibular artery near the superior vestibular nerve. The cochlear artery divides into a posterior cochlear branch and the vestibulocochlear artery. The latter finally divides into a cochlear and a vestibular branch. The semicircular canals are supplied by the

113

anterior vestibular artery and vestibular branch of the vestibulocochlear artery. The cochlea is supplied by posterior cochlear branch and the cochlear branch of vestibulocochlear artery (Leblanc, 2000; Fig. 4).

Clinical Considerations of the Facial and Vestibulocochlear Vascular Supply Hemifacial spasm is characterized by involuntary unilateral spasm of muscles innervated by the facial nerve. Similar to trigeminal neuralgia, it is often thought to be triggered primarily by vascular compression of the facial nerve (Wilkins, 1991). Typical and atypical spasms have been described. Whereas typical hemifacial spasm affects the orbicularis oculi muscle and progresses caudally, atypical hemifacial spasm begins in the buccal muscles and progresses cranially. Anatomically, typical spasm correlates with vascular compression on the anterior and caudal aspect of the facial nerve and atypical spasm with the posterior and cranial aspects (Jannetta, 1998). Injection with botulinum toxin is a well-tolerated shortterm option for patients with mild hemifacial spam (Yoshimura et al., 1992; Mazlout et al., 2013). Definite treatment, however, is only accomplished by microvascular decompression of the facial nerve. A study by Barker et al. with 782 patients followed for over 10 years reported that post-operatively 84% of the patients experienced significantly benefit from operative treatment. Iijima et al. (2013) found usefulness of preoperative MRI and MRA to identify neurovascular contacts of the facial nerve at the root emerging and root exiting zone in patients that underwent microvascular decompression and the posterior inferior cerebellar artery (PICA) followed by AICA to be the offending vessel at the root emerging zone. El Refaee et al. (2013) found MRI and MRA to accurately detect the offending vessel at the root exiting zone when compared tow intraoperative high-definition endoscopic visualization. Disabling positional vertigo is a condition characterized by vertigo that is attributed to vascular compression of the vestibular nerve and cannot be categorized as benign paroxysmal positional vertigo, vestibular neuronitis, or Meniere’s disease. In one large series, microvascular decompression of the vestibular nerve has been found to provide significant relief of symptoms in up to approximately 80% of patients (Jannetta et al., 1984; Mïller et al., 1993). Microvascular decompression has also been reported to be of value in a selected group of patients with tinnitus (Mïller and Moller, 2007). Despite these findings the management of disabling positional vertigo and tinnitus remains a clinical challenge and the value of microvascular decompression for these disorders is controversial.

GLOSSOPHARYNGEAL NERVE (IX) Intracranial The vertebral (55%) or the basilar artery (45%) may give rise to the artery of the glossopharyngeal nerve, also referred to as the artery of the lateral

114

Hendrix et al.

Fig. 4. Arterial supply of the vestibulocochlear nerve after Leblanc (Leblanc, 2000). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

fossula of the medulla oblongata (Leblanc, 2000), and a central and a peripheral arteriole supply the nerve in the cistern close to the brainstem. The latter arteriole accompanies the glossopharyngeal nerve to the jugular foramen. In about a quarter of individuals, these arterioles do not arise from the artery of the lateral fossula, but from the middle meningeal artery (Leblanc, 2000). The intracranial glossopharyngeal nerve also receives blood supply from the ECA via the ascending pharyngeal artery, which divides into an extracranial anterior pharyngeal trunk and an intracranial posterior neuromeningeal trunk. However, the neuromeningeal trunk may also originate from the occipital or posterior auricular arteries. The neuromeningeal trunk gives rise to two major branches, the jugular, commonly located between vagus and accessory nerve, and the hypoglossal branch (Lapresle and Lasjaunias, 1986; Hacein-Bey et al., 2002). The jugular branch supplies the glossopharyngeal nerve as it travels anteromedial to the sigmoid sinus and internal jugular vein to exit through the pars nervosa of the jugular foramen (Lasjaunias and Berenstein, 1987; Ayeni et al., 1995; Leblanc, 2000).

Extracranial Collaterals of the ascending pharyngeal artery supply the nerve in the retrostyloid space. In almost 50% of specimens studied, Leblanc observed arterial rein-

forcement by the pericarotid plexus that supplies the glomus caroticum, or the carotid body (Gonzalez et al., 1994). The occipital artery and other ECA branches also supply the glomus caroticum (Heymans, 1955). In the tonsillar area, the descending palatine and sphenopalatine arteries, branches of the maxillary artery, and the ascending palatine artery, a branch of the facial artery, supply the glossopharyngeal nerve. The dorsal lingual artery, a branch of the lingual artery, feeds the terminal branch of the glossopharyngeal nerve (Leblanc, 2000).

VAGUS NERVE (X) Intracranial The vagus nerve exits the medulla oblongata between they medullary pyramid and inferior cerebellar peduncle. Due to its anatomical vicinity, arterial supply to the vagus and glossopharyngeal nerves is largely redundant. The artery for the lateral fossula of the medulla oblongata gives rise to arterioles that feed the vagus nerve roots. At the level of the jugular ganglion, where the nerve exits the skull base through the pars venosa of the jugular foramen, arterial supply is provided by the jugular branch from the neuromeningeal trunk of the ascending pharyngeal artery (Lapresle and Lasjaunias, 1986; Lasjaunias and Berenstein, 1987; Leblanc, 2000).

Arterial Supply of the Lower Cranial Nerves

115

Extracranial In the lateral pharyngeal space, below the jugular foramen, the nodose ganglion of the vagus nerve is supplied by collaterals of the ICA and the posterior meningeal artery, typically originating from the vertebral artery. Further distal, the nerve is supplied by vagal artery, a branch of the inferior thyroid artery of the thyrocervical trunk. Near the vagus nerve, the vagal artery bifurcates into an ascending cervical branch and a descending thoracic branch (Grigorowsky, 1928; Fernando and Lord, 1994). In a quarter of specimens, Grigorowsky also found that in addition to the ascending cervical branch there are direct branches anastomozing with branches of the ECA to contribute to the arterial supply. Fernando and Lord found that the vagal artery is reinforced by thin vessels from the cervical ICA and common carotid artery. At the thoracic level, the vagus nerve is supplied by branches from the vertebral arteries, internal thoracic arteries, the aorta, bronchial arteries, esophageal arteries, superior phrenic arteries, and thymical arteries in the pediatric age group (Bartholdy, 1897; Grigorowsky, 1928; Fernando and Lord, 1994). The superior laryngeal nerve is vascularized by the superior thyroid arteries and its terminal branches. The recurrent laryngeal nerves receive blood supply mainly from collaterals from the inferior thyroid arteries (Leblanc, 2000; Fig. 5).

SPINAL ACCESSORY NERVE (XI) Intracranial The spinal accessory nerve (XI) is composed of a cranial and a spinal division. The cranial roots are supplied by proximal, distal, and recurrent branches of PICA (Leblanc, 2000). The spinal roots are supplied by the musculospinal artery of the ascending pharyngeal artery (Lapresle and Lasjaunias, 1986) and collaterals from the anterior spinal artery (Lasjaunias and Berenstein, 1987). Additionally, the paired posterior spinal arteries, arising from either the vertebral artery or PICA have also been found to supply the spinal roots of the accessory nerve (Lasjaunias et al., 1985; Leblanc, 2000). Distal to where the cranial and spinal divisions merge and form the accessory nerve, an accompanying distal branch of PICA travels towards the jugular foramen where the neuromeningeal trunk of the ascending pharyngeal artery contributes to the arterial supply (Leblanc, 2000).

Extracranial As the accessory nerve travels along the sternocleidomastoid muscle, it is supplied by the sternocleidomastoid branch of the occipital artery, and collaterals of the occipital and lingual arteries (Grigorowsky, 1928; Leblanc, 2000).

Fig. 5. Arterial supply of the vagus nerve after Grigorowsky (Grigorowsky, 1928). Panel A: Vagal artery with bifurcation into an ascending cervical and a descending thoracic branch. Panel B: Branches of the vagal artery function as vasa nervorum to the vagus nerve and vasa vasorum to the adjacent external carotid artery. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

HYPOGLOSSAL NERVE (XII) Intracranial The hypoglossal nerve (XII) exits the medulla oblongata at the pre-olivary sulcus. Fine branches from either the anterior spinal artery, PICA, or direct branches from the vertebral artery supply the hypoglossal nerve roots (Lasjaunias and Berenstein, 1987; Leblanc, 2000). These vessels anastomose with collaterals of the posterior meningeal artery to form an arterial network (Leblanc, 2000). The hypoglossal branch of the neuromeningeal trunk accompanies and nourishes the hypoglossal nerve while traveling through the hypoglossal canal and anastomoses with the jugular branch (Lasjaunias and Moret, 1976; Lasjaunias and Berenstein, 1987; Jukic et al., 2001; Meguro et al., 2007). In rare instances, a persistent hypoglossal artery, a persistent carotid-vertebrobasilar anastomosis, runs through the hypoglossal canal and supplies the hypoglossal nerve (Ouriel et al., 1988).

Extracranial The ascending pharyngeal artery and the arterial pericarotid plexus supply the hypoglossal nerve

116

Hendrix et al.

extracranially. The hypoglossal nerve travels between the ICA and internal jugular vein and turns around the occipital artery to run horizontally towards the tongue (Bademci and Yasargil, 2006). Collaterals from the external carotid artery, occipital artery, facial artery, and lingual artery supply the nerve fibers. At the level of the tongue, branches of the facial artery including the submental artery, and the lingual artery vascularize the hypoglossal nerve (Grigorowsky, 1928; Fernando et al., 1999; Leblanc, 2000).

Clinical Considerations of the Glossopharyngeal, Vagal, Spinal Accessory, and Hypoglossal Vascular Supply Glossopharyngeal neuralgia represents approximately 1% of the facial pain syndromes and is characterized by pain in the sensory distribution of the auricular and pharyngeal branches of the glossopharyngeal nerve. Usually, mechanical stimulation of the tonsillar fossa, e.g., swallowing cold liquids, triggers an intense, stabbing pain affecting the pharynx, tonsillar region, posterior tongue, ear, or angle of the mandible. If tympanic pain predominates, the involvement of the vagus nerve is likely and the syndrome is referred to as vagoglossopharyngeal neuralgia (Bruyn, 1983; Blumenfeld and Nikolskaya, 2013). Initial evidence for vascular compression being involved in the pathophysiology of glossopharyngeal or vagoglossopharyngeal neuralgia stems from intraoperative findings in patients who benefited from microvascular decompression. Both the vertebral artery and PICA have been found to compress the nerve (Laha and Jannetta, 1977). For patients to have a high likelihood of symptom improvement after microvascular decompression the operation has to be reserved for patients where a vascular compression site is clearly identified (Rey-Dios and Cohen-Gadol, 2013). Knight et al. retrospectively reviewed major cranial nerve injuries due to carotid endarterectomy. Of 129 cases, there were five vagus nerve, four marginal mandibular branch of the facial nerve, and three hypoglossal nerve injuries (Knight et al., 1987). Pegoraro et al. made similar observations at their institute. Of 120 patients that underwent carotid endarterectomy, seven suffered from vagus nerve injury, five marginal mandibular branch, and 3 hypoglossal nerve injury (Pegoraro et al., 1990). Even though direct manipulation resulting in nerve injury may be the culprit in the majority of those cases, nerve ischemia secondary to injury to small, nerve-irrigating twigs during exposure of the carotid artery and its related vasculature may be a contributing factor. Fernando and Lord suggested a direct anterior approach to the carotids as it more likely precludes vessels that reinforce the vagal artery that supplies the vagus nerve. Minimal retraction of the hypoglossal nerve to minimize tethering of the nerve-irrigating feeder may also reduce the incidence of hypoglossal nerve palsies from carotid endarterectomies (Fernando et al., 1999).

Spasmodic torticollis is characterized by uncontrollable clonic and intermittently tonic contractions of the neck muscles characterize leading to abnormal head posture. Vascular compression of the spinal accessory nerves, the upper cervical nerve roots, and the brainstem by the vertebral artery or, more commonly, the PICA has been associated with this condition. The spinal arteries have also been found to be involved in symptomatic accessory nerve compression (Freckmann et al., 1981). Microvascular decompression has been found to be beneficial in selected patients (Jho and Jannetta, 1995; Sun et al., 2009).

CONCLUSIONS The lower cranial nerves receive their blood supply through a complex arterial network supplied by tributaries of the external carotid, internal carotid, and vertebrobasilar circulation. Frequently all these territories contribute to the vascular supply of an individual lower cranial nerve along its course. In neurovascular compression syndromes the offending artery may provide arterial supply to the corresponding cranial nerve but is usually not the sole contributor.

REFERENCES Adams WE. 1942. The blood supply of nerves: I. Historical review. J Anat 76:323–341. Anson BJ, Donaldson JA, Warpeha RL, Rensink MJ, Shilling BB. 1973. Surgical anatomy of the facial nerve. Arch Otolaryngol Head Neck Surg 97:201–213. Ayeni SA, Ohata K, Tanaka K, Hakuba A. 1995. The microsurgical anatomy of the jugular foramen. J Neurosurg 83:903–909. Bademci G, Yasargil MG. 2006. Microsurgical anatomy of the hypoglossal nerve. J Clin Neurosci 13:841–847. Barker FG, 2nd, Jannetta PJ, Bissonette DJ, Larkins MV, Jho HD. 1996. The long-term outcome of microvascular decompression for trigeminal neuralgia. N Engl J Med 334:1077–1083. Bartholdy K. 1897. Die Arterien der Nerven. Morphologische Arbeiten p 393–458. Blumenfeld A, Nikolskaya G. 2013. Glossopharyngeal neuralgia. Curr Pain Headache Rep 17:343. Blunt MJ. 1954. The blood supply of the facial nerve. J Anat 88:520– 526. Brunsteins DB, Ferreri AJ. 1995. Microsurgical anatomy of arteries related to the internal acoustic meatus. Acta Anat (Basel) 152: 143–150. Bruyn GW. 1983. Glossopharyngeal neuralgia. Cephalalgia 3:143– 157. Calcaterra TC, Rand RW, Bentson JR. 1976. Ischemic paralysis of the facial nerve: A possible etiologic factor in Bell’s palsy. Laryngoscope 86:92–97. Capo H, Kupersmith MJ, Berenstein A, Choi IS, Diamond GA. 1991. The clinical importance of the inferolateral trunk of the internal carotid artery. Neurosurgery 28:733–737; discussion 737–738. evic Cetkovic ´ M, Antunovic ´ V, Marinkovic ´ S, Todorovic ´ V, Vitos ´ Z, Milisavljevic ´ M. 2011. Vasculature and neurovascular relationships of the trigeminal nerve root. Acta Neurochir (Wien) 153: 1051–1057; discussion 1057. El Refaee E, Langner S, Baldauf J, Matthes M, Kirsch M, Schroeder HW. 2013. Value of 3-dimensional high-resolution magnetic resonance imaging in detecting the offending vessel in hemifacial spasm: Comparison with intraoperative high definition endoscopic visualization. Neurosurgery 73:58–67.

Arterial Supply of the Lower Cranial Nerves El-Khouly H, Fernandez-Miranda J, Rhoton AL, Jr. 2008. Blood supply of the facial nerve in the middle fossa: The petrosal artery. Neurosurgery 62:ONS297–ONS303; discussion ONS303–ONS304. Fernando DA, Lord RS. 1994. The blood supply of vagus nerve in the human: Its implication in carotid endarterectomy, thyroidectomy and carotid arch aneurectomy. Ann Anat 176:333–337. Fernando DA, Lord RS, Ozmen J. 1999. The blood supply of the hypoglossal nerve and its relevance to carotid endarterectomy. Cardiovasc Surg 7:287–291. € ller D. 1981. Treatment Freckmann N, Hagenah R, Herrmann HD, Mu of neurogenic torticollis by microvascular lysis of the accessory nerve roots: Indication, technique, and first results. Acta Neurochir (Wien) 59:167–175. Gonzalez C, Almaraz L, Obeso A, Rigual R. 1994. Carotid body chemoreceptors: From natural stimuli to sensory discharges. Physiol Rev 74:829–898. € hrenden Arterien. Grigorowsky IM. 1928. Zur Anatomie der Kopferna € r Anatomie und Entwicklungsgeschichte. Zeitschrift fu Hacein-Bey L, Daniels DL, Ulmer JL, Mark LP, Smith MM, Strottmann JM, Brown D, Meyer GA, Wackym PA. 2002. The ascending pharyngeal artery: Branches, anastomoses, and clinical significance. AJNR Am J Neuroradiol 23:1246–1256. Haynes DR. 1955. The relations of the facial nerve in the temporal bone. Ann R Coll Surg Engl 16:175–185. Haynes I. 1896. A manual of anatomy. Philadelphia: Saunders. Heymans C. 1955. Action of drugs on carotid body and sinus. Pharmacol Rev 7:119–142. Iijima K, Horiguchi K, Yoshimoto Y. 2013. Microvascular decompression of the root emerging zone for hemifacial spasm: Evaluation by fusion magnetic resonance imaging and technical considerations. Acta Neurochir (Wien) 155:855–862. Jannetta PJ. 1998. Typical or atypical hemifacial spasm. J Neurosurg 89:346–347. Jannetta PJ, Mïller MB, Mïller AR. 1984. Disabling positional vertigo. N Engl J Med 310:1700–1705. Jho HD, Jannetta PJ. 1995. Microvascular decompression for spasmodic torticollis. Acta Neurochir (Wien) 134:21–26. Jukic NB, Jelic M, Basic V, Jukic T, Vinter I. 2001. Persistent hypoglossal artery. J Anat 198:315–316. Knight FW, Yeager RM, Morris DM. 1987. Cranial nerve injuries during carotid endarterectomy. Am J Surg 154:529–532. Kretschmer T, Heinen CW, Antoniadis G, Richter HP, Konig RW. 2009. Iatrogenic nerve injuries. Neurosurg Clin N Am 20:73–90, vii. Krisht A, Barnett DW, Barrow DL, Bonner G. 1994. The blood supply of the intracavernous cranial nerves: An anatomic study. Neurosurgery 34:275–279;discussion 279. Laha RK, Jannetta PJ. 1977. Glossopharyngeal neuralgia. J Neurosurg 47:316–320. Lapresle J, Lasjaunias P. 1986. Cranial nerve ischaemic arterial syndromes. A review. Brain 109(Pt 1):207–216. Lasjaunias P, Berenstein A. 1987. Functional Anatomy of Craniofacial Arteries. New York: Springer, p 413. Lasjaunias P, Moret J. 1976. The ascending pharyngeal artery: Normal and pathological radioanatomy. Neuroradiology 11:77–82. Lasjaunias P, Moret J, Mink J. 1977. The anatomy of the inferolateral trunk (ILT) of the internal carotid artery. Neuroradiology 13:215– 220. Lasjaunias P, Vallee B, Person H, Ter Brugge K, Chiu M. 1985. The lateral spinal artery of the upper cervical spinal cord. Anatomy,

117

normal variations, and angiographic aspects. J Neurosurg 63: 235–241. Leblanc A. 2000. Encephalo-peripheral nervous system. New York: Springer. Marinkovic SV, Gibo H. 1995. The blood supply of the trigeminal nerve root, with special reference to the trigeminocerebellar artery. Neurosurgery 37:309–317.  fi S, Brour J, El Afrit Mazlout H, Kamoun Gargouri H, Triki W, K e  our M, Kraiem A. 2013. [Safety and efficacy of botuMA, Ch e linum toxin in hemifacial spasm]. J Fr Ophtalmol 36:242– 246. Meguro T, Terada K, Hirotsune N, Nishino S, Asano T. 2007. Unusual variant of persistent primitive hypoglossal artery. Br J Radiol 80: e314–e316. Mïller AR, Mïller MB. 2007. Microvascular decompression operations. Prog Brain Res 166:397–400. Mïller MB, Mïller AR, Jannetta PJ, Jho HD, Sekhar LN. 1993. Microvascular decompression of the eighth nerve in patients with disabling positional vertigo: Selection criteria and operative results in 207 patients. Acta Neurochir (Wien) 125:75–82. Monkhouse WS. 1990. The anatomy of the facial nerve. Ear Nose Throat J 69:677–683, 686–677. Ouriel K, Green RM, DeWeese JA. 1988. Anomalous carotid-basilar anastomoses in cerebrovascular surgery. J Vasc Surg 7:774– 777. Pegoraro M, Barile C, Nessi F, Bertoldo U. 1990. Peripheral nerve injuries during carotid endarterectomy. Minerva Cardioangiol 38: 211–213. Rey-Dios R, Cohen-Gadol AA. 2013. Current neurosurgical management of glossopharyngeal neuralgia and technical nuances for microvascular decompression surgery. Neurosurg Focus 34: E8. Rhoton AL, Jr. 2000a. The cerebellar arteries. Neurosurgery 47: S29–S68. Rhoton AL, Jr. 2000b. The cerebellopontine angle and posterior fossa cranial nerves by the retrosigmoid approach. Neurosurgery 47: S93–S129. Stopford JS. 1916. The arteries of the pons and medulla oblongata. J Anat Physiol 50:131–164. Sun K, Lu Y, Hu G, Luo C, Hou L, Chen J, Wu X, Mei Q. 2009. Microvascular decompression of the accessory nerve for treatment of spasmodic torticollis: Early results in 12 cases. Acta Neurochir (Wien) 151:1251–1257. Thomas KL, Vilensky JA. 2013. The anatomy of vascular compression in trigeminal neuralgia. Clin Anat. Wigley C. 2008. Section 1 - Cells, Tissues and Systems; Chapter 3 Nervous System; Blood Supply of Peripheral Nerves. In: Standring S, editor. Gray’s Anatomy: The Anatomical Basis of Clinical Practice, 40 ed: Churchill Livingstone Elsevier. p 41–67. Wilkins RH. 1991. Hemifacial spasm: A review. Surg Neurol 36:251– 277. Yoshimura DM, Aminoff MJ, Tami TA, Scott AB. 1992. Treatment of hemifacial spasm with botulinum toxin. Muscle Nerve 15:1045– 1049. Zeng Q, Zhou Q, Liu Z, Li C, Ni S, Xue F. 2013. Preoperative detection of the neurovascular relationship in trigeminal neuralgia using three-dimensional fast imaging employing steady-state acquisition (FIESTA) and magnetic resonance angiography (MRA). J Clin Neurosci 20:107–111.