J. Anat. (2001) 198, pp. 423–429, with 8 figures Printed in the United Kingdom 423

The course of the buccal : relationships with the temporalis muscle during the prenatal period

! ! ! 1 1 1 J. R. ME! RIDA-VELASCO , J. F. RODRI! GUEZ-VAZQUEZ , C. DE LA CUADRA , J. A. MERIDA-VELASCO2 AND J. JIMENEZ-COLLADO1 " Departamento de Ciencias MorfoloT gicas II, Facultad de Medicina, Universidad Complutense, Madrid, # and Departamento de Ciencias MorfoloT gicas, Facultad de Medicina, Universidad de Granada, Granada, Spain

(Accepted 17 October 2000)

 The aim of this study was to describe the course of the buccal nerve and its relationships with the temporalis muscle during the prenatal period. Serial sections of 90 human fetal specimens ranging from 9 to 17 wk development were studied by light microscopy. Each fetal specimen was studied on both right and left sides, making a total of 180 cases for study. A 3-D reconstruction of the region analysed in one of the specimens was made. In 89 cases the buccal nerve was located medial to the temporalis muscle; in 73 cases it penetrated the muscle; in 15 cases it lay in a canal formed by the muscle fibres and was covered by fascia, and finally, in 3 cases it was a branch of the . The study has revealed that in a large number of cases the buccal nerve maintains an intimate association with the temporalis muscle.

Key words: Buccal nerve; temporalis muscle.

in relation to anaesthesia of the oral region through  which it extends (Jablonski et al. 1985; Hendy & The buccal nerve, a branch of the mandibular division Robinson, 1994) whereas others studied the surgical of the , carries sensory fibres which anatomy of the nerve (Bozola et al. 1989; Hendy et al. supply the lower buccal gingiva, lower buccal sulcus 1996) or described its course while carrying out and mucosa and may also contribute to the surgical procedures (Singh, 1981; Vrionis et al. 1996). extra-oral cutaneous supply of the cheek (Hendy et al. Little attention has been given to the relationships 1996). Anatomy textbooks describe the course of the between the buccal nerve and the temporalis muscle buccal nerve as running between the 2 heads of the along its course. According to Harn & Shackelford and then descending in a (1982), in adults the buccal nerve crosses the insertion forward direction in association with the maxillary of the temporalis muscle on to the mandible in a space artery and medial to the tendon of the temporalis containing lax connective tissue that is closed off by a muscle and Bichat’s fat pad to reach the external structure termed the fascial-tendinous complex. More- surface of buccinator (Gegenbaur, 1889; Testut & over, some authors found that occasionally the buccal Latarjet, 1980; Orts-Llorca, 1986; Williams, 1998; nerve penetrates the muscle or the tendon of the Rouvie' re & Delmas, 1999). temporalis muscle (Ge! rard, 1921; Hollinshead, 1962; Several authors have studied the buccal nerve from Romanes, 1987; Dubrul, 1990; Moore, 1993). The different perspectives. Some have focused on the objective of this work was to study the relationships relationships between the and its between the buccal nerve and the temporalis muscle branches with aponeurotic structures in the region during the fetal period. This was done by analysing (Hovelacque & Virenque, 1913). Others authors have serial sections of human fetal specimens from 9 to examined the sensory distribution of the buccal nerve 17 wk of development.

Correspondence to Prof. J. R. Me! rida-Velasco, Departamento de Ciencias Morfolo! gicas II, Facultad de Medicina, Universidad Com- plutense, 28040 Ciudad Universitaria, Madrid, Spain. Tel-fax: j34\1\394 13 39; e-mail: mvlopera!eucmax.sim.ucm.es 424 J. R. MeT rida-Velasco and others

McManus & Mowry’s techniques (1968) for light    microscopic study. A total of 90 human fetuses from the collection of the The region studied in specimen JR-1 (55 mm C-R Embryology Institute of the Complutense University length) was reconstructed according to the procedure of Madrid was studied. The specimens were between described by Arra! ez-Aybar et al. (1994). The images 35 and 150 mm crown-rump (C-R) length. All were generated by topographic techniques using the specimens had been previously conserved in neutral program AutoCAD V.14 for Windows 98. A standard formalin (10%). Sections with a thickness ranging PC was used with a 300 Hz Pentium II processor with from 15 to 25 µm depending on the size of the 128 Mb RAM, with a resolution of 800i600 and true specimen were cut. C-R length, plane of section, and colour images. weeks of development (O’Rahilly & Mu$ ller, 1996), are The photographs were first scanned with a HP- shown in Table 1. The slices were stained according to ScanJet 4s using a resolution of 300 dpi and a grey

Table 1. Details of fetuses and planes of section examined

C-R length Plane of Wk of C-R length Plane of Wk of Fetuses (mm) section development Fetuses (mm) section development

Pe 35 Transverse 9 Cr-2 83 Transverse 13 OY-2 38 Frontal 9 HL-2 83 Transverse 13 OI-2 38 Sagittal 9 HL-31 83 Frontal 13 ABR 40 Frontal 9 B-107 84 Transverse 13 Faus 40 Sagittal 9 HL-32 84 Transverse 13 JR-3 43 Frontal 10 LR-1 84 Transverse 13 OC 43 Frontal 10 Sa-13 84 Transverse 13 VR-2 45 Frontal 10 Bu-23 85 Transverse 13 BE 47 Sagittal 10 RI-50 85 Transverse 13 Be-503 48 Frontal 10 N-12 85, 5 Transverse 13 Faus-7 48 Frontal 10 B-250 86 Transverse 13 PT-14 49 Frontal 10 J1 86 Sagittal 13 LR-5 50 Transverse 10 Be 501 87 Transverse 13 PT-7 51 Sagittal 10 Cr-1 87 Transverse 13 Ca-6 52 Frontal 11 B 608 90 Transverse 13 JR-1 55 Transverse 11 Cer 61 90 Transverse 13 G33 56 Transverse 11 B-54 91 Transverse 13 JP-1 56 Transverse 11 Sa-14 91 Transverse 13 Fe-21 57 Transverse 11 Ca-11 92 Sagittal 13 Mu-1 58 Transverse 11 Bu-18 93 Transverse 13 B-403 62 Frontal 11 B-207 95 Frontal 13 Cabeza 64 Frontal 11 B-72 95 Transverse 13 Be-101 65 Frontal 11 Te-1 96 Transverse 13 Bu-19 66 Transverse 12 B-195 97 Transverse 13 No-9 67 Frontal 12 Be 1011 97 Transverse 13 R-11 69 Transverse 12 B6 100 Transverse 14 Be 113 70 Frontal 12 Cu-1 100 Sagittal 14 Mu-10 70 Transverse 12 HC-1 100 Transverse 14 Bu-14 72 Transverse 12 Ca-8 101 Transverse 14 Mu-11 72 Transverse 12 Be 1010 103 Transverse 14 Mu-7 73 Transverse 12 J-4 103 Sagittal 14 HL 30 74 Transverse 12 Be 502 105 Transverse 14 Mu-5 74 Sagittal 12 St 8 105 Transverse 14 VR-2 74, 5 Frontal 12 NO 10 106 Transverse 14 B-25 75 Transverse 12 Bu 007 107 Frontal 14 Be-154 75 Transverse 12 Cer-78 110 Transverse 14 JR-8 75 Frontal 12 B62 113 Frontal 14 PT-12 75 Frontal 12 Ce-2 115 Transverse 15 Ca-7 76 Frontal 12 B-29 117 Transverse 15 Mat-1 77 Transverse 12 B3 120 Transverse 15 Esc 16 78 Transverse 12 R-6 125 Transverse 15 JR-6 80 Frontal 12 Cu-2 137 Frontal 16 Vr-3 80 Frontal 12 Esc-3 140 Transverse 16 Be-516 82 Sagittal 13 Do 144 Transverse 17 Be-3 83 Transverse 13 B-28 150 Transverse 17 Course of the buccal nerve 425

Fig. 1. Human fetus B-608 (90 mm CR; wk 13 of development). Transverse section. The temporalis muscle (T) inserts into the coronoid process of the mandible and extends along the 2 fascicles (arrows). One of these inserts on the anterior border of the ramus of the mandible and the other on the medial surface of the ramus. R, ramus of mandible; M, masseter; PL, lateral pterygoid; B, buccal nerve; L, ; A, inferior alveolar nerve. Bar, 500 µm. Fig. 2. Human fetus Be-516 (82 mm CR; wk 13 of development). Sagittal section. The buccal nerve lies between the 2 heads of the lateral pterygoid muscle. At this level, the nerve gives rise to branches that supply the muscle (arrowhead). MA, mandibular nerve; B, buccal nerve; PL, lateral pterygoid muscle; PI, medial pterygoid muscle; T, temporalis muscle; C, Meckel’s cartilage; A, inferior alveolar nerve; R, ramus of the mandible; H, . Bar, 500 µm. scale of 4 bytes with the program Visioneer PaperPort maximum precision and amplification of the details v. 3.0. The images were then rastered to bidimensional on the screen. As with wax sections, the height and vectors (x, y), using the cursor to trace the contours of real spatial location of each section was recorded (z). the images scanned onto the screen. This permitted After introducing all the vectors corresponding to 426 J. R. MeT rida-Velasco and others

Fig. 3. Human fetus OY-2 (38 mm CR; wk 9 of development). Frontal section. The buccal nerve is located medial the temporalis muscle. B, buccal nerve; CP, coronoid process; M, ; T, temporalis muscle. Bar, 500 µm. Fig. 4. Human fetus Be-501 (87 mm CR; wk 13 of development). Transverse section. The buccal nerve pierces the deeper fascicle of temporalis. B, buccal nerve; T, temporalis muscle; PL, lateral pterygoid muscle; CP, coronoid process. Bar, 200 µm. the different sections in the program, different colours  were assigned to each anatomical structure. With the program, the element analysed could be represented Transverse sections of the zygomatic region showed 3-dimensionally from any spatial perspective (x, y, z). that the temporalis muscle was inserted into the Course of the buccal nerve 427 coronoid process of the mandible and extended along temporal nerve and was related to the more deeply 2 muscle fasciae: one superficial that inserted in the embedded portion of the temporalis muscle at the anterior border of the ramus of the mandible and the level of its insertion (Fig. 3). Finally, the nerve other, deeper, that inserted in the internal surface of proceeded forwards in association with the ramus of the ramus (Fig. 1). the mandible and Bichat’s fat pad to reach the The buccal nerve was a branch of the division of the and to extend along the skin and anterior trunk of the mandibular nerve. On its forward the mucous membrane of the cheek. This was the course it lay between the 2 heads of the lateral most frequent arrangement observed in 89 of the 180 pterygoid muscle (Fig. 2). As it crossed the lateral samples studied (44 left side, 45 right side). pterygoid, some small branches were provided to In 73 of the 180 samples analysed (37 left, 36 right) supply this muscle. Along its extrapterygoid course, the buccal nerve penetrated the deeper portion of the the buccal nerve gave rise to the deeper anterior temporalis muscle (Figs 4, 5). In 15 cases (6 left, 9

Fig. 5. Medial view of 3-D computer-assisted reconstruction of the buccal nerve of the right side of fetus JR-1 (55 mm CR; wk 11 of development). T, temporalis muscle; B, buccal nerve; R, ramus of mandible; A, inferior alveolar nerve; L, lingual nerve; C, Meckel’s cartilage. Fig. 6. Human fetus B-28 (150 mm CR; wk 17 of development). Transverse section. The buccal nerve is related to the deeper fascicle of temporalis surrounded by its fascia. B, buccal nerve; T, temporalis muscle; R, ramus of mandible; PL, lateral pterygoid muscle; G, Bichat’s fat pad; F, muscle fascia. Bar, 200 µm. 428 J. R. MeT rida-Velasco and others

Table 2. Arrangement of the buccal nerve in relation to the deep temporalis muscle

Left side Right side Total

Deep 44 45 89 Penetrating the muscle 37 36 73 Extending through a canal 69 15 covered by fascia The buccal nerve is a branch 12 3 of the inferior alveolar nerve

right), the nerve was surrounded by the fascia of the temporalis muscle and the muscle formed a groove along which the nerve extended (Fig. 6). In 3 cases, (1 left, 2 right), the buccal nerve was a branch of the inferior alveolar nerve (Fig. 7). In these cases, the buccal nerve proceeded at some distance from the insertion of the temporalis muscle in the mandible. Figure 8 shows a diagram of the relation between the buccal nerve and the temporalis muscle according to our results. All the results are collected in Table 2.

 The majority of standard human anatomy reference books describe the temporalis muscle as simply inserting on the coronoid process and\or the anterior border of the ramus of the mandible (Orts-Llorca, 1986; Moore, 1993; Williams, 1998). However, in the transverse sections we analysed we found that the temporalis muscle inserted on the coronoid process of the mandible and, at the level of its insertion to extend along 2 muscle fascicles: one superficial that inserted on the anterior border of the ramus of the mandible and another deeper one that inserted on the medial surface of the ramus of the mandible. These results are in agreement with those of some authors who described the temporalis muscle as inserting on the coronoid process of the mandible and proceeding along 2 tendinous extensions, one superficial that inserts in the anterior border of the ramus of the mandible and another deeper, that inserts in the temporal crest of the mandible (Harn & Shackelford, 1982; DuBrul, 1990; Ernest et al. 1991; Lang, 1995; Rouviere & Delmas, 1999). Fig. 7. Human fetus Esc-16 (78 mm CR; wk 12 of development). Anatomy textbooks all give similar descriptions for Transverse section. The buccal nerve is a branch of the inferior the course of the buccal nerve. This nerve lies between alveolar nerve. B, buccal nerve; A, inferior alveolar nerve; L, lingual nerve; C, Meckel’s cartilage; PI, medial pterygoid muscle; M, masseter muscle; R, ramus of mandible. Bar, 500 µm. (73 cases); (C) the muscle fascia covers the nerve (15 cases); (D) the Fig. 8. Diagram showing arrangement of the buccal nerve from buccal nerve is a branch of the inferior alveolar nerve (3 cases). MA, present results: (A) the nerve is located medial to temporalis (89 mandibular nerve; B, buccal nerve; L, lingual nerve; A, inferior cases); (B) the nerve penetrates the deeper fascicle of temporalis alveolar nerve; H, mylohyoid nerve; T, temporalis muscle. Course of the buccal nerve 429 the 2 heads of the lateral pterygoid muscle, and then BOZOLA AR, GASQUES JAL, CARRIQUIRY CE, CARDOSO in its extrapterygoid course it descends in a forward DE OLIVEIRA M (1989) The buccinator musculomucosal flap: anatomic study and clinical application. Plastic and Recon- direction in association with the maxillary artery, the structive Surgery 84, 250–257. tendon of temporalis and Bichat’s fat pad, reaching CARTER RB, KEEN EN (1971) The intramandibular course of the external surface of buccinator. the inferior alveolar nerve. Journal of Anatomy 108, 433–440. The buccal nerve presented the aforementioned DUBRUL EL (1990) Sicher-DuBrul AnatomıTa Oral, 8th edn, pp. 95, 96, 248. Barcelona: Doyma. arrangement, the most frequent one, in 89 of the cases ERNEST EA, MARTINEZ ME, RYDZEWSKI DB, SALTER G analysed. However, in 73 cases the buccal nerve (1991) Photomicrographic evidence of insertion tendonosis: the penetrated the more deeply embedded portion of the etiologic factor in pain for temporal tendonitis. Journal of Prosthetic Dentistry 65, 127–131. temporalis muscle at the level of its insertion on the GEGENBAUR G (1889) TraiteT d’Anatomie Humaine, 3rd edn, pp. internal surface of the ramus of the mandible. Some 1017–1018. Paris: C. Reinwald. authors (Ge! rard, 1921; Hollinshead, 1962; Romanes, GE! RARD G (1921) Manuel d’Anatomie Humaine, 2nd edn, p. 450. 1987; DuBrul, 1990; Moore, 1993) had previously Paris: Masson. HARN SD, SHACKELFORD LS (1982) Further evaluation of the described this arrangement in adults. According to superficial and deep tendons of the human temporalis muscle. Lang (1995), in one of the specimens he dissected, Anatomical Record 202, 537–548. the maxillary artery pierced the deeper portion of HENDY CW, ROBINSON PP (1994) The sensory distribution of temporalis. the buccal nerve. British Journal of Oral and Maxillofacial Surgery 32, 384–386. In 15 cases (6 left, 9 right), the buccal nerve ran HENDY CW, SMITH KG, ROBINSON PP (1996) Surgical along a groove in the muscle of the deeper fascicle of anatomy of the buccal nerve. British Journal of Oral and temporalis covered by the muscle fascia. Harn & Maxillofacial Surgery 34, 457–460. HOLLINSHEAD WH (1962) Textbook of Anatomy, pp. 890–891. Shackelford (1982) have described an identical ar- New York: Harper and Row. rangement in adults. HOVELACQUE A, VIRENQUE M (1913) Les formations In 3 cases (1 left, 2 right), the buccal nerve emerged apone! urotiques de la re! gion pte! rygomaxillaire chez l’homme et as a branch of the inferior alveolar nerve. In this chez quelques mammife' res. Journal de l’Anatomie et de la Physiologie 49, 427–488. arrangement, described by Turner (1864), the buccal JABLONSKI NG, CHENG CM, CHENG LC, CHEUNG HM nerve left the inferior alveolar nerve and emerged (1985) Unusual origins of the buccal and mylohyoid . Oral from a small foramen in the retromolar region. This Surgery, Oral Medicine, and Oral Pathology 60, 487–488. Clinical Anatomy of the Masticatory Apparatus and aberrant trajectory was found by Singh (1981) while LANG J (1995) Peripharyngeal Spaces, pp. 81–83. Stuttgart: Georg Thieme. operating on the third molar. Studies by Jablonski et MMANUS JFA, MOWRY RM (1968) TeT cnica HistoloT gica. al. (1985) and Ossenberg (1986) showed that this Madrid: Atika. unusual origin of the buccal nerve occurred more MOORE KL (1993) AnatomıTa con OrientacioT n ClıTnica, 3rd edn, pp. 753–761. Madrid: Me! dica Panamericana. frequently in certain populations (southern Chinese O’RAHILLY R, MU$ LLER F (1996) Human Embryology and population, native Americans). Moreover, in some Teratology, 2nd edn, pp. 81–104. New York: Wiley-Liss. cases this anomalous course has been associated with ORTS-LLORCA F (1986) AnatomıTa Humana, 6th edn (vols I, II), the failure of local anaesthesia in the area around the pp. 368, 804, 809. Barcelona: Cientı!fico-Me! dica. OSSENBERG NS (1986) Temporal crest canal: case report and retromolar fossa (Carter & Keen, 1971). statistics on a rare mandibular variant. Oral Surgery, Oral Our results reveal a large number of cases in which Medicine, and Oral Pathology 62, 10–12. the buccal nerve penetrated the deeper portion of ROMANES GJ (1987) Cunningham Tratado de AnatomıTa, 12th edn, p. 794. Madrid: Interamericana-McGraw-Hill. temporalis (73 cases), or remained inside a groove ROUVIE' RE H, DELMAS A (1999) AnatomıTa Humana. produced by the muscle and covered by fascia (15 Descriptiva, TopograT fica y Funcional, 10th edn (vol I), pp. cases). Knowledge of this possible arrangement in the 137, 138, 242. Barcelona: Masson. adult would be useful for some surgical procedures SINGH S (1981) Aberrant buccal nerve encountered at third molar surgery. Oral Surgery, Oral Medicine, and Oral Pathology 52, and also to provide an anatomical basis to clarify 142. unexplained pain in this region. TESTUT L, LATARJET A (1980) Tratado de AnatomıTa Humana, 9th edn (vol. III), p. 112. Barcelona: Salvat.  TURNER W (1864) On some variations in the arrangement of the nerves of the human body. Natural History Review 4, 612–617. ARRA! EZ-AYBAR LA, ME! RIDA-VELASCO JR, VRIONIS FD, CANO WG, HEILMAN CB (1996) Microsurgical RODRI! GUEZ-VA! ZQUEZ JF, JIME! NEZ-COLLADO J (1994) anatomy of the as viewed laterally and A computerised technique for morphometry and 3D recon- superiorly. Neurosurgery 39, 777–786. struction of embryological structrues. Surgical and Radiologic WILLIAMS PL (ed.) (1998) AnatomıTa de Gray, 38th edn (vols I, II), Anatomy 16, 419–422. pp. 800–1237. Madrid: Harcourt Brace.