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THE BLOOD SUPPLY OF THE FACIAL NERVE BY MICHAEL J. BLUNT Department of Anatomy, Royal Free Hospital School of Medicine The precise aetiology of Bell's palsy, or idiopathic facial paralysis, has not been defined, but the opinion most generally held is that the paralysis is due to ischaemia of the facial nerve trunk. It is therefore surprising to find no general agreement on the gross form of the blood supply to the facial nerve, and no information in the literature on its intrinsic vascular anatomy. The first account of the blood supply of the nerve is that of Bartholdy (1897), who collated the observations made by earlier authors and built up from them a complete picture of the pattern of arterial supply. As might be expected, this account con- tained several inconsistencies and items of conflicting evidence. The arterial supply of the terminal branches was investigated by Tobin (1943), and Guerrier (1951) gave a further account of the gross pattern of arterial branches to the nerve which did not agree, in several respects, with the earlier observations quoted by Bartholdy. It therefore seemed necessary to re-investigate the gross features of the blood supply of the facial nerve as well as to study its intrinsic vascular arrangements.

MATERIAL AND METHODS Thirty human temporal bones were removed at post-mortem from twenty-seven subjects whose ages ranged from 14 to 85 years: the heads of two full-term foetuses were also available. The foetal heads were injected, one with neoprene, the other with indian ink in double strength plasma, and the extra-petrous portions of the nerves were dissected in both specimens. One temporal bone was removed from each and sectioned serially. In eight of the adult specimens the basilar artery was injected, and in fourteen specimens injection was made into the stem vessel giving rise to the stylomastoid artery. In both instances the injection mass used was either 5 % indian ink in double-strength plasma, or coloured neoprene. In a further group of eight specimens no injection was made. The facial canal was opened under a binocular microscope and those specimens which had been injected with neoprene were studied to find the gross form of the blood supply to the nerve. Those injected with indian ink in plasma were similarly studied; the nerve was afterwards removed from its canal and either mounted flattened on a slide, or else embedded and sectioned before mounting, in order to show the intrinsic vascular pattern. In the uninjected specimens the nerve was stained by the sodium nitroprusside- benzidine technique. Some nerves were mounted flattened out on slides, and others were embedded in gelatin and frozen sections were cut at 100z before staining. Details of preparation did not differ from those described by Pickworth (1934) except in regard to the methods of embedding and final mounting. Nerve segments were embedded in gelatin blocks which were left unfixed and unhardened: after The blood supply of the facial nerve 521 sectioning, the gelatin dissolved away in the warmed staining solutions without adversely affecting the benzidine reaction. Sections mounted in polystyrene mounting medium remained unfaded for 3 months on an average; when neutral balsam was used the stain survived for less than 2 weeks.

THE GROSS BLOOD SUPPLY (a) From the pons to the floor of the internal auditory meats Between its exit from the pons and the internal auditory meatus the facial nerve receives branches directly from the anterior inferior cerebellar artery (PI. 1, fig. 1). This vessel runs laterally from the basilar artery and forms a loop which lies between the facial and auditory nerves and projects towards, and often into, the internal auditory meatus (Stopford, 1916; Nabeya, 1923; Konaschko, 1927). The loop usually gives rise directly to the internal auditory artery but, in one of the eight adult specimens and in one of the foetal temporal bones, the anterior vestibular and vestibulo-cochlear branches took separate origin from the loop of the anterior inferior cerebellar artery. In all of the specimens examined fine vessels passed from both main branches of the internal auditory artery to supply the facial and auditory nerves.

Text-fig. 1. A diagrammatic representation of the right facial canal opened in its whole length. The arteries are shown as solid black lines which are broken where the vessels pass on the medial side of the facial nerve. (b) In thefacial canal In its course in the canal the facial nerve receives branches from both the petrosal branch of the middle meningeal artery and the stylomastoid artery (Text-fig. 1). The Jpetrosal artery Immediately after it has entered the skull through the foramen spinosum the middle meningeal artery gives off a short stem vessel which divides into the petrosal artery laterally and a branch to the trigeminal ganglion medially. The petrosal artery is sometimes double and when this is the case the second vessel may arise either from the same common trunk or from the accessory meningeal: each of these 522 Michael J. Blunt arrangements has been met with twice in a series of eighteen dissections, and in all of the four specimens an anastomosis linked the two vessels. The petrosal artery runs laterally in company with the greater superficial petrosal nerve to enter the temporal bone through the hiatus Fallopii (PI. 1, fig. 2). It gives off a short, stout branch which divides into a spray of fine vessels to the geniculate ganglion, and is then continued along the facial canal below the horizontal part of the facial nerve to anastomose with the stylomastoid artery. The anastomotic branch gives off a vessel which crosses the lateral side of the facial nerve and ramifies in the roof of the middle ear cavity. The stylomastoid artery The stylomastoid artery is usually described as taking direct origin from the posterior auricular artery but that arrangement has not been met with in eighteen dissections in this series. Below the stylomastoid foramen either the posterior auricular artery or the occipital artery gives off a common stem vessel which divides into a number of branches below the base of the skull; these branches pass to the tympanic plate, styloid process and mastoid process and to the post-auricular skin and the facial nerve (P1. 1, fig. 3). A further branch, which is the stylomastoid artery, enters the stylomastoid foramen on the medial side of the nerve. It was indirectly derived from the occipital artery twelve times and from the posterior auricular artery six times. The stylomastoid artery forms a loop in the lower part of the fa. ial canal, the returning limb of which leaves the canal with the posterior auricular nerve. From the convexity of the loop two branches usually arise: the largest ofthese accompanies the facial nerve and the other rapidly breaks up into branches which pierce the posterior meatal wall in company with filaments from the auricular branch of the vagus. The main ascending branch (PI. 1, fig. 4) lies on the medial side of the facial nerve as far as the junction between its horizontal and vertical parts and then loops around the inferior aspect of the bend, usually passing somewhat on to its lateral side, to reach the infero-medial aspect of the horizontal part of the nerve. It anastomoses directly with the petrosal artery to form a complete arterial arcade in the facial canal. From the arcade branches are given to the nerve close to the origin of the chorda tympani and at the level of the second bend; a separate branch accompanies the chorda tympani, and one or two branches run through the posterior wall of the canal to supply the mastoid air cells. From the horizontal part of the arcade a vessel leaves the facial canal and ramifies in the roof of the middle ear cavity. The lowest branch from the stylomastoid artery to the facial nerve is therefore at the level of the origin of the chorda tympani. (c) The extra-petrous course Below the stylomastoid foramen the nerve is supplied by a constant branch from the stem vessel of the stylomastoid artery (PI. 1, fig. 3), and, in the parotid gland, it receives twigs from either the posterior auricular artery or the occipital artery, and also from the superficial temporal and transverse facial arteries. The terminal branches of the nerve as they leave the parotid gland are each accompanied by a The blood supply of the facial nerve 523 fine arteria comitans which gives branches into the nerve and accompanies it until close to its termination. All the arterial branches to the facial nerve below the stylomastoid foramen are linked longitudinally by free anastomoses in the epineurium. Venous drainage In the internal auditory meatus the nerve is loosely fascicular in structure and contains little connective tissue between its fasciculi; it is widely separated from the periosteum of the meatal walls and its veins drain into branches of the internal auditory vein. At and below the geniculate ganglion the nerve is surrounded by a tough connective tissue sheath which is continuous on the one hand with the periosteum of the facial canal and on the other with the epineurium. The sheath encloses both the facial nerve and the arterial arcade, and in its substance lies a well- marked venous network which drains, anteriorly, into veins accompanying the petrosal artery and, inferiorly, into the venae comitantes of the stem vessel from which the stylomastoid artery is derived. Venous channels in the sheath also com- municate with those in the surrounding bone (P1. 1, fig. 5) and in adult material injected with indian ink venous channels in the walls of the canal were always filled through these connexions. Towards the funnel-shaped opening of the stylomastoid foramen the connective tissue sheath becomes progressively thicker and more dense, and below the stylomastoid foramen it fuses with the carotid sheath on the medial side, and behind, with the dense connective tissue deep to the mastoid process.

THE INTRINSIC VASCULAR ARRANGEMENTS Throughout the facial nerve there is a well-marked intrinsic plexus composed of capillary vessels which run mainly in a longitudinal direction and form a branching network connected at irregular intervals by transverse vessels (PI. 2, fig. 6). Just above the bifurcation of the facial nerve in the parotid gland the capillary plexus is more irregular, and in this situation venules are carried into the nerve with the abundant interfascicular connective tissue (P1. 2, figs. 7, 8). In the horizontal and vertical segments of the nerve vessels of this calibre are for the most part con- fined to the sheath, and the intrinsic plexus is mainly made up of capillary vessels. At the geniculate ganglion the density of the capillary bed is much greater than elsewhere in the course of the facial nerve (PI. 2, fig. 9) and this increased density is constantly shown in both injected and benzidine stained material. The density is greatest at the apex of the geniculate ganglion where most of the ganglion cells are aggregated. The intrinsic vessels of the geniculate ganglion are in continuity with those in the intrinsic plexuses of the nerve. They exhibit many tortuosities, and there are also irregular ampullar dilatations of their lumina which are easily dis- tinguished, in thick sections, from the tortuosities (P1. 2, figs. 10, 11). They are a striking feature of both injected and benzidine-nitroprusside stained preparations whether sectioned or mounted whole. In structure they are simple endothelial channels with no muscle tissue in their walls. For comparison, the trigeminal and vagal ganglia from four of the same group of subjects have been stained by the sodium nitroprusside-benzidine technique and no obvious ampullar dilatations have been seen. 524 Michael J. Blunt In its course in the internal auditory meatus the facial nerve has a capillary plexus similar to that seen in the post-genicular parts of the nerve, but rather finer and more open in structure.

DISCUSSION It is evident from the foregoing account that no single vessel exercises a structural autonomy over the vascular arrangements of the facial nerve, either on the arterial or the venous side, although the petrosal artery certainly provides the main arterial supply to the geniculate ganglion. There is no direct link between the petrosal artery and the branches of the internal auditory artery, but, except in this one situation, adjacent arteries of supply are linked to one another either by their parent stem vessels or by free arterial anastomoses. The anastomosis between the petrosal and stylomastoid arteries has been constantly present in this series, although not observed by Guerrier, who does not, however, describe the methods of investigation which he employed: it is therefore assumed that injections were made into some major vessel at a distance from the facial canal. Owing to the well-known difficulty of obtaining full injection of vessels over a diffuse area and especially in bone, it is not difficult to conceive that by such a method the complete length of anastomotic arcade might not become filled. The channels available for venous drainage from the intra-petrous portion of the nerve are in even freer communication than the arterial branches below the geniculate ganglion, for in this situation there is a marked venous network in the sheath. More- over, this network communicates with venous channels in the walls of the facial canal. The irregular capillary and pre-capillary dilatations in the geniculate ganglion are similar to those which have been described in the posterior root ganglia of spinal nerves (Adamkiewitz, 1886; Bergmann & Alexander, 1941). Bergmann (1942) also reports such dilatations in the Gasserian ganglion, but states that they are relatively few in number compared with those in spinal ganglia. It seems probable that they underlie some local feature of the vascular dynamics in both geniculate and posterior root ganglia, and it may be noteworthy that in both these situations the ganglia are protected by the walls of a bony canal. It is also of interest that they are present on the course of the facial nerve in the only situation where it has not been possible to demonstrate direct links between adjacent arteries of supply to the nerve. A similar state of affairs exists in spinal ganglia, for Adamkiewitz stated that their arteries of supply entered from the medial side with the nerve root, and Bergmann and Alexander confirmed this and made the further observation that the anastomosis between the ganglionic vessels and those in the spinal nerve distal to the ganglion was very poor. The intrinsic plexus below the geniculate ganglion resembles that seen in peri- pheral nerves in the limbs. An additional feature, which has not been noted else- where, is the unusual disposition of venules in the nerve trunk above its bifurcation. In conclusion, there is no anatomical evidence of precarious blood supply to any part of the facial nerve below the geniculate ganglion which would especially pre- dispose to ischemia as a result of vascular spasm. It would seem likely that the Journal of Anatomy, Vol. 88, Part 4 Plate I

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__ t _S___ _ s o BLUNT THlE BLOOD SUPPLY OF THE: FACIAL NERVE . The blood supply of the facial nerve 525 peculiar anatomical situation of the facial nerve is a more potent factor in the aetiology of idiopathic facial paralysis than are the local vascular arrangements.

SUMMARY The gross blood supply and intrinsic vascular anatomy of the facial nerve have been described and the findings are discussed. The significance of pre-capillary and capillary dilatations in the geniculate ganglion is also considered. The author is grateful to Miss D. J. Collier, through whom a grant was obtained from the Royal Free Hospital Endowment Fund, for suggesting the subject of this investigation. Thanks are extended, also, to Prof. R. E. M. Bowden for her very valuable advice and encouragement.

REFERENCES ADAMKIEWITZ, A. (1886). Der Blutkreislauf der Ganglienzelle. Berlin. BARTHOLDY, K. (1897). Die Arterien der Nerven. Morph. Arbeiten, 7, 393-458. BERGMANN, L. (1942). Studies on the blood vessels of the human Gasserian ganglion. Anat. Rec. 82, 609-630. BERGMANN, L. & ALEXANDER, L. (1941). Vascular supply of spinal ganglia. Arch. Neurol. Psychiat., Chicago, 46, 761-782. GUERRIER, Y. (1951). Les AWteres du Nerf Facial. Montpellier med. 39, no. 5, 83-95. KONASCHKO, P. I. (1927). Die Arteria Auditiva Interna des Menschen und ihre Labyrinthaste. Z. ges. Anat. 1. Z. Anat. EntwGesch. 83, 241-268. NABEYA, D. (1923). A study in the comparative anatomy of the blood vascular system of the internal ear in Mammalia and Homo (Japanese). Acta sch. med. Univ. Kioto, 6, 1-132. PICKWORTH, F. A. (1934). A new method of study of the brain capillaries and its application to the regional localization of mental disorder. J. Anat., Lond., 69, 62-71. STOPFORD, J. S. B. (1916). The arteries of the pons and medulla oblongata. J. Anat., Lond., 50, 131-164. TOBIN, C. E. (1943). Injection method to demonstrate blood supply of nerves. Anat. Rec. 87, 341-344. EXPLANATION OF PLATES Key to abbreviations used in text-figure and in Plates 1 and 2 a.i.c. anterior inferior cerebellar artery m.a.c. mastoid air cells a.n. abducent nerve m.e.c. middle ear cavity b.a. basilar artery p.a.n. posterior auricular nerve br.n. branch to facial nerve p.a. petrosal artery F.N. facial nerve s.a. stylomastoid artery G. geniculate ganglion st.v. stem vessel of the stylomastoid artery PLATE 1 Fig. 1. Full-term foetus, right side: showing the origin of the internal auditory artery from the anterior inferior cerebellar artery. Neoprene injection. x 6. Fig. 2. Left temporal bone dissected from above. There is duplication of the petrosal artery: its anastomotic branch and its branch to the geniculate ganglion are shown. Neoprene injection. x6. Fig. 3. Left temporal bone seen from below, showing the stylomastoid artery, its stem of origin, and the artery to the facial nerve below the stylomastoid foramen. Neoprene injection. x 6. Fig. 4. The lower dissection of the specimen from which Fig. 2 was photographed. The facial canal has been opened by a transmastoidal approach and the nerve displaced posteriorly. The stylomastoid artery is shown: its main ascending branch anastomoses with the petrosal artery, and branches to the facial nerve are shown. Neoprene injection. x 6. Fig. 5. A transverse section through the left temporal bone of a full-term foetus. The facial nerve sheath and its contained venous plexus is shown. Indian ink injection. x 30. 526 Michael J. Blunt

PLATE 2 Fig. 6. The interfascicular plexus in the vertical part of the facial nerve. Sodium nitroprusside- benzidine stain. x 50. Fig. 7. The interfascicular plexus above the bifurcation of the nerve. Sodium nitroprusside- benzidine stain. x 50. Fig. 8. Transverse section of the facial nerve above the bifurcation. Sodium nitroprusside- benzidine stain. x 100. Fig. 9. Geniculate ganglion. Flattened preparation. Sodium nitroprusside-benzidine stain. x 30. Fig. 10. A horizontal section through the apex of the geniculate ganglion. Sodium nitroprusside- benzidine stain. x 200. Fig. 11. A horizontal section through the angle of the geniculate ganglion. Sodium nitroprusside- benzidine stain. x 200.