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Home , Angle of the mandible, Buccal artery, Deep temporal arteries, External carotid artery, Facial artery, Greater palatine artery

The Arterial System of the Head and of the Rhesus Monkey with Emphasis on the External Carotid System '

WALTER A. CASTELLI AND DONALD F. HUELKE Department of Anatomy, The University of Michigan, Ann Arbor, Michigan

ABSTRACT The arterial plan of the head and neck of 64 immature rhesus mon- keys (Macacn mulatta) was studied using four techniques - , corrosion preparations, cleared specimens, and angiographs. In general, the arterial plan of this area in the monkey is similar to that of man. However, certain outstanding differ- ences were noted. The origin, course, and distribution of all is described as well as the vascular relations to pertinent structures.

As has been mentioned previously 10% formalin except 17 which were un- (Dyrud, '44; Schwartz and Huelke, '63) embalmed. Four different techniques were the rhesus monkey is useful for many used for the study of the arterial distribu- types of medical and dental investigations, tion : ( 1 ) - 27 specimens; (2) yet its detailed gross morphology is virtu- corrosion preparations - 6; (3) cleared ally unknown. Although certain areas of specimens - 15; (4) angiographs - 16 the monkey have been studied in detail - heads ( 11 unembalmed and 5 embalmed). brachial plexus, facial and masticatory The arterial system of the specimens used musculature, subclavian, axillary and cor- for dissection was injected with vinyl ace- onary arteries, orbital vasculature, and tate, red latex, or with a red-colored gela- other structures (Schwartz and Huelke, tion mass. For the dissection of smaller ar- '63; Chase and DeGaris, '40; DeGaris and teries, the smallest of 150 ~1 in diameter, Glidden, '38; Chase, '38; Huber, '25; Wein- the binocular dissection microscope was stein and Hedges, '62; Samuel and War- used. The corrosion specimens were pre- wick, '55; Eyster, '44; Wagenen and Catch- pared by injecting the arteries with vinyl pole, '56; Tokarski, '31; Kennard, '41). acetate followed by maceration of the soft other areas have been virtually overlooked tissue with potassium hydroxide (3-10% ) or have received but passing attention. for 24 to 72 hours. The dye selected for The literature on the arterial supply of the injection of the cleared specimens was primate head has been adequately sum- Teichmann's paste (Teichmann, '52) marized by Dyrud ('44). Very few in- colored with cinnabar. These specimens vestigators, however, have used Macaca were decalcified in 4% nitric acid and then mulatta specimens and more importantly cleared by the Spalteholtz method. The in most of the articles only brief descrip- radiopaque material for the angiographs tions have been presented with many of was the modified Schlessinger's mass the pertinent morphological details not (Reiner and Rodriguez, '57), the main having been stated, or overlooked. Addi- components being mercury and barium tionally, only a few specimens have been sulfate. used in the majority of these works. It is The head and neck was removed from our purpose to present the arterial plan of the animal at the level of the clavicles or, the head and neck, especially that of the in some cases, a V-shaped section was external carotid arterial system. made with the apex extending down to the arch of the . Both common carotid MATERIALS AND METHODS 1 This investigation was supported (in part) by USPHS research grant DE-00895 from the National Sixty-four immature rhesus monkeys Institute of Dental Research, National Institutes of (Macaca mulatta) were used for this study. Health, Bethesda, Maryland. 2 Present address: Department of Anatomy, Univer- All of the animals were embalmed with sity of Concepcion, Concepcion, Chile. AM. J. ANAT., 116: 149-170. 149 150 WALTER A. CASTELLI AND DONALD F. HUELKE arteries, or the left common carotid rior mediastinum and as it leaves the thor- and the brachiocephalic arterial trunk acic cavity, it is crossed by the left brachio- were cannulated depending on the individ- cephalic . ual situation; paraffin (Castelli, '63) or At the base of the neck, the common dental stone was applied to the cut surface carotid arteries are less than 1 cm apart. to provide adequate vascular resistance so They diverge from one another through that the injected material would pass their course in the neck, and, at the level through the arterial channels and not of the carotid bifurcation, they are 3 cm seep out through the exposed tissue. Photo- apart. The is graphs of all stages of dissection were covered by the sternomastoid muscle and taken, as well as of many of the corrosion lies medial to the and cleared specimens. with the behind and between them. At approximately the mid-neck level, OBSERVATIONS the common carotid artery is crossed by Common carotid arteries. Minor vari- the , and the artery is ations as to the origins of the common tightly bound to the posterior surface of carotid arteries were found. Most often a the lateral lobe of the gland. The trunk, averaging 7 mm in length, arises common carotid artery divides into the ex- from the apex of the aortic arch and is the ternal and internal carotid arteries approx- origin to the left common carotid artery imately 1 cm above the angle of the man- and the brachiocephalic artery. At times dible (fig. 3). The bifurcation of the a very short common trunk is found; how- common carotid artery is 4 to 5 cm above ever, on sectioning the aorta, it is noted the level of the sternoclavicular joint. that both vessels have independent open- . At the carotid ings separated only by a thin septum. Of bifurcation the external carotid artery is 32 specimens studied, the left common anterior and only slightly lateral to the carotid artery and brachiocephalic trunk . The internal caro- arose separately from the aortic arch in tid artery is tightly applied to the lateral only one animal (figs. 1 and 2). wall of the by the posterior di- The common trunk passes anterior to gastric muscle. The external carotid artery the left side of the ; between the runs parallel to the internal carotid artery superior vena cava on the right and the for approximately 1 cm, then passes be- left , left vagus nerve, tween the stylohyoid and posterior digas- and left phrenic nerve (fig. 2). tric muscles. Above the posterior digastric The brachiocephalic artery has an ob- muscle it swings laterally and passes ob- lique upward course across the front of liquely upward through the the trachea and averages 16 mm in length. toward the posterior border of the ramus It is covered by the left brachiocephalic of the reaching it slightly be- vein, or the superior vena cava, and by neath the condylar neck. Here the exter- adipose tissue of the superior mediasti- nal carotid artery continues forward, me- num. The brachiocephalic artery termi- dial to the ramus, as the . nates in the thorax by bifurcating into the Sometimes, at this point, a very small right common carotid and right subclavian superficial temporal artery is given off arteries (fig. 2). (fig. 3). The right common carotid artery has a 1. The is the short intrathoracic course (8 mm) ascend- first branch of the external carotild artery, ing along the right side of the trachea (fig. arising a few millimeters beneath the ling- 2). Close to the apex of the thorax it is ual-facial trunk, or as a branch of this covered by the origins of the sternohyoid trunk. The superior thyroid artery is found and sternothyroid muscles. inferior to the and the The left common carotid artery passes posterior . The artery is directly upward through the thorax me- extremely short (approximately 5 mm in dial to and slightly behind the left vagus length) and fans out into several branches. nerve, adjacent to the left lung. It is One, a superior laryngeal branch, passes covered by the adipose mass of the supe- horizontally deep to the HEAD AND NECK ARTERIES IN RHESUS 151

Fig. 1 The common arterial stem (1) of the brachiocephalic trunk (2) and left common carotid artery (3) overlying the trachea (4). (Dissection preparation.)

and perforating the thyrohyoid membrane, border of the lobe; the other, on the poste- supplies the upper part of the . An- rior aspect of the lateral lobe (fig. 3). other branch continues downward to sup- 2. The lingual-facial trunk arises from ply other infrahyoid muscles. A terminal the anterior part of the external carotid branch passes to the medial side of the artery 1 or 2 mm beyond its origin. The thyroid lobe, and from it very small trunk passes forward and slightly upward branches arise to supply the isthmus of the deep to the posterior digastric muscle; thyroid gland and the upper part of the near its origin the hypoglossal nerve is trachea. One or two small thyroid ter- lateral to the trunk and further on the minal branches are given off at the level nerve passes deep to the trunk to reach the of the apex of the lateral lobe. One of . The vessel continues forward for a these passes downward on the lateral distance of approximately 1 cm and di- 152 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 2 The large arteries in the upper mediastinum. The common arterial stem (1); brachiocephalic trunk (2); right subclavian artery (3); right common carotid artery (4); left common carotid artery (5); left subclavian atery (6); phrenic nerve (7); vagus nerve (8). (Dissection preparation.) vides into two main branches, the lingual The dorsal lingual branches are multi- and facial arteries (figs. 3 and 4). ple vessels arising from the lingual stem The appears to be a direct before it divides into the larger deep and continuation of the common trunk. It sublingual arteries. The dorsal lingual passes deep to the muscle con- branches are distributed mainly to the tinuing to the tip of the tongue where it posterior of the tongue, the adjacent ling- terminates. It gives rise to three main ual mucosa, the glossoepiglotic fold, pala- branches : dorsal lingual, deep lingual, and tine , and muscles of the area. Other sublingual arteries (fig. 4). muscular branches from the lingual artery HEAD AND NECK ARTERIES IN RHESUS 153

Post. auricular a. Superficial temporal a. I \ i

Superior laryngeal a EL infrohyoid muscular branch -- Post thyroid branch

Lot thyroid branch--

Fig. 3 Schematic drawing showing the course of the main branches of the external carotid artery. pass downward to supply the hyoglossus vascular network yet another smaller net- and the thyrohyoid muscles (fig. 4). work is formed by parallel arterioles which The deep lingual artery is the principal branch off toward the submucosa (fig. 4). vessel of the tongue and much of the vas- The sublingual artery passes towards cularization of the horizontal portion of the symphysis of the mandible in a deeper the tongue is dependent upon it. Ascend- plane through the tongue; frequently it is ing branches arise from it which parallel double. Numerous branches to the sub- each other in their course towards the sur- lingual gland arise from it, the largest of of the tongue. Before reaching the which arises from the lingual artery be- tongue mucosa they branch profusely and hind the origin of the main sublingual ar- anastornose with each other to form an tery. The sublingual branch as it passes arterial network which is apparent anteriorly is in contact with the lateral throughout the entire dorsal surface of the aspect of the muscle. tongue in the cleared specimens. From this Throughout its course the artery supplies 154 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 4 The distribution of the lingual artery. Lingual-facial trunk (1); lingual artery (2); dor- sal lingual branches (3); deep lingual branch (4). Note the sublingual branch (5) passing through the incisive area of the mandible (6) and into the lower (7). (Teichmann’s paste injection, decalcified and cleared preparation.) the genioglossus and geniohyoid muscles curves around the inferior border of the and it anastomoses with mylohyoid and mandible where it contacts the upper part submental branches of the . of the . It passes onto Additionally, it supplies the lingual alveo- the face in front of the anterior fibers of lar mucosa, the attached and free gingiva. the . At the symphysis, medial to the geniohyoid In its cervical course the facial artery attachment, and directly on the midline, has five major branches. The ascending either the right or left sublingual artery palatine artery arises near the bifurcation continues through a symphyseal foramen of the lingual-facial trunk. This vessel into the lower lip. As the artery passes courses posteriorly, upwards and medially, through the mandible, it supplies branches passing between the and stylo- to the pulp, periodontal membrane, and pharyngeus muscles which it supplies. The supporting tissue of the central and vessel terminates on the lateral pharyn- lateral (fig. 4). In the lip the artery geal wall at the level of the . passes vertically upward toward the free The submandibular artery is an important border; it bifurcates into right and left vessel which arises from the facial artery branches which distribute to the lower lip, when it is in contact with the medial ptery- labial mucosa and gingiva. The sublingual goid muscle; it is the main supply of the branches in the lip anastomose with small submandibular gland. Numerous small branches of the facial artery forming an muscular arteries supply the medial ptery- arterial network around the mouth (fig. 5). goid and masseter muscles near their inser- The facial artery passes downward and tion in the area of the angle of the mandi- forward lateral to the hypoglossal nerve ble. A small submental branch runs along and the thyrohyoid muscle. Laterally it is the inferior border of the mandible; it dis- in contact with the lower part of the me- tributes mainly to the anterior digastric dial pterygoid muscle. The artery then and platysma muscles. As the facial artery HEAD AND NECK ARTERIES IN RHESUS 155

Fig. 5 General distribution of the arterial vessels of the face and part of the . Facial artery (1); superior labial (2); septal branch (3); lateral nasal branch (4); inferior palpebral branch (5); superior palpebral branch (6); supraorbital branch (7); parietal and frontal branches (8 ). (Teichmann’s paste injection, cleared preparation. ) crosses the inferior border of the mandible, posteriorly, spreading out on the medial and a mylohyoid branch arises from it to pass lateral walls of the buccal pouch, where onto the lateral surface of the mylohyoid they form an intricate vascular network. muscle. The vessel then continues for- The largest branch of the facial artery, the ward, parallel to the base of the mandible, superior labial branch, arises about 1 cm and supplies the anterior digastric mus- behind and slightly above the angle of the cles (fig. 6). mouth. It passes horizontally through the The facial artery, as it passes in front upper lip very close to its free border. It of the insertion of the masseter muscle, is then courses upward to the area beneath anterior to the . It continues al- the ala of the nose. At times this artery most vertically upward to the area of the appears to be the continuation of the where it gives off its terminal branches (fig. 5). On the side facial, for, above its origin, the facial ar- of the face it is deep to the buccal pouch tery is small. In cleared specimens it can and , adjacent to the base be seen that this branch is the principal of the mandible. The vessel then traverses supply of the very rich arterial network of the muscular mass about the corner of the the upper lip. The mouth. Above the corner of the mouth, has two principal branches, the lateral na- the facial artery is more superficial, being sal branch, which passes upward beneath covered only by the zygomaticoorbital mus- the external naris and around the ala of cle complex. On the side of the face and the nose to supply the lateral surface of the close to the insertion of the masseter mus- ala, and a septal branch which courses up- cle two main buccal pouch branches pass ward, adjacent to the midline, to the nasal 156 WALTER A. CASTELLI AND DONALD F. HUELKE

Med pterygoid m

Ascending palatine

-Carotid bifurcotion

branch

Fig. 6 Schematic drawing of the proximal part of the facial artery. septum and the skin of the lobe of the passes above the posterior digastric mus- nose. These branches anastomose around cle. The common trunk passes posteriorly, the external nares (fig. 5). medial to the posterior digastric muscle At the level of the infraorbital foramen and following its fibers. The length of the the facial artery terminates by sprouting common trunk is variable; in some cases it into a variable number of smaller reaches the level of the external acoustic branches. Consistently there are anasto- meatus before dividing into occipital and motic branches which join with terminals auricular branches (figs. 3 and 7). The of the . Laterally a , sometimes double, passes branch passes along the infraorbital rim lateral to the upper part of the posterior to supply the musculature and lateral digastric muscle being covered by the parts of the lower . A medial branch, splenius capitis and longissimus capitis frequently double, passes upward towards muscles. It then continues posteriorly and the inner canthus of the eye. It passes be- upward along the bone to terminate in neath the , sup- branches which supply the muscles at- plying it as well as the medial half of the tached to the posterior aspect of the , lower eyelid, the lateral side of the bridge and to the overlying scalp. Consistently it of the nose, and the most medial portion gives rise to a branch which perforates the of the upper eyelid. At the inner canthus, skull by passing through a foreamen ap- it anastomoses with very small arteries proximately 2 cm posterior to the external passing through the orbital septum (fig. 5). acoustic meatus. This is the posterior 3. The occipital and auricular arteries meningeal artery, the main supply of the most frequently arise by a common stem posterior lateral portion of the from the external carotid artery as it (fig. 8). HEAD AND NECK ARTERIES IN RHESUS 157

Post. deeo ternDora1 a.

ecurrent meningeal a. Orbital bronches

Sup. post. olveolar a.

Ext. carotid a,-’

Carotid bifurcotion Mylohyoid branch’ I/

to mandible) Buccal a. Fig. 7 Schematic drawing showing distribution of the maxillary artery.

The auricular artery is a short trunk (fig. 3). It passes vertically upward lying which passes upward behind and beneath on the longus colli muscle. In its upward the lower part of the auricle of the course the vessel is crossed laterally by the where it almost immediately divides into stylopharyngeus and the styloglossus mus- multiple branches. Some of these continue cles. Near the base of the skull it divides upward along the attachment of the auri- into several terminal branches, one of cle and supply its posterior surface. Others which passes through the jugular foramen pass over the attachment of the sterno- to supply the in the area of the mastoid muscle and distribute there. The sigmoid sinus. Other branches pass auricular branches supply adjacent muscu- slightly forward and upward to be distrib- lature, the lateral and the posterior area of uted to the musculature and mucosa of the scalp, and the auricle (fig. 5). The the upper portion of the pharynx. Contin- branches to the auricle form rich anasto- uing upward and forward along the base moses in the form of concentric vascular of the skull, the ascending pharyngeal ar- arches. From these arches, vessels sprout tery supplies the membranous portion of off to form yet smaller vascular networks the behind the posterior edge which are located close to the free edge of of the and behind the . the auricle (fig. 5). The artery also gives Small branches from it pass into the soft rise to a small branch which passes palate (fig. 9). through the stylomastoid foramen and ac- 5. The maxillary artery arises about companies the . 11/2 cm beneath the external acoustic 4. The ascending pharyngeal artery is a 3In the Macacus rhesus, the nasal septum is con- very thin branch arising from the superior tinued behind the posterior border of the vomer by a medial side of the external carotid artery triangular-shaped membranous septum which extends backward for about 1% cm along the base of the immediately above the lingual-facial trunk skull. Its inferior attachment is to the . 158 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 8 Disposition of meningeal arteries. Posterior meningeal (1); middle meningeal (2); ante- rior meningeal (3). (Teichmann’s paste injection, decalcified and cleared preparation.)

Fig. 9 The arterial supply of the nasal septum. The septal branch of ascending pharyngeal artery (1); nasopalatine branch (2); septal branch of internal nasal artery (3). (Vinyl acetate injection, dissection preparation.) HEAD AND NECK ARTERIES IN RHESUS 159 meatus and less than 1 cm behind the the parotid gland tissue and also supply ramus of the mandible at the level of the the adjacent structures (figs. 7, 10 and neck of the condyle. As a direct continua- 11). One of these, a large massetric ar- tion of the external carotid artery it passes tery, passes forward along the lateral side horizontally forward medial to the neck of the subcondylar portion of the ramus of of the condyle toward the pterygopalatine the mandible to enter the deep head of the fossa. Passing slightly medial and upward masseter muscle. It supplies most of this throughout this course the artery is in con- muscle and anastomoses along the front tact with the lower lateral surface of the edge of the ramus with other branches . In the pterygopal- from the maxillary artery. Near the angle, atine fossa the vessel terminates by divid- this artery joins with branches of the ing into numerous branches. The main facial artery which also supply the inferior branches of the maxillary artery are 12 in part of the masseter muscle (fig. 10). A number, several of which arise by common transverse facial artery likewise is one of origins (fig. 7). these branches which pass horizontally Very near the point of origin of the forward, approximately Y2 cm beneath the maxillary artery, the first branch arises; it . It joins branches of the is a short parotid trunk which soon divides facial artery at the lateral inferior margin into six or seven secondary branches. of the . A very small ascending These parotid gland branches spread out in branch, the zygomaticoorbital artery,

Fig. 10 The main arterial vessels of face, and occipital regions. Occipital and posterior auricular arteries (1); posterior deep temporal artery (2); facial artery (3); subman- dibular branches (4); masseteric branch (5) and capsular arteries (6). (Vinyl acetate injection, cor- rosion preparation.) 160 WALTER A. CASTELLI AND DONALD F. HUELKE courses obliquqely forward to anastomose The tympanic and middle meningeal ar- with the arteries about the orbit. It teries arise from a common trunk near the supplies the skin on the side of the cal- beginning of the maxillary artery, medial varium, and anastomoses at the side of the to the condylar neck (fig. 11). The trunk orbit with lateral branches from the facial passes around the inferior border of the as well as supraorbital branches from the lateral pterygoid muscle to run medially (fig. 5). inward toward the . Several small temporomandibular cap- Near the base of the skull the vessel di- sular branches arise from the maxillary ar- vides into its two named branches (figs. 7 tery as the vessel passes adjacent to the and 8). The tympanic artery is very small medial side of the condylar neck. These and passes posteriorly into the petrotym- ascending branches have a very short panic fissure towards the middle ear. The course, and pass into the medial aspect of meningeal artery passes through the lat- the temporomandibular capsule and ad- eral end of the foramen ovale to enter the jacent tissue. Additionally, articular . It grooves the inner branches arise from the posterior deep table of bone at the base of the near its origin, and from cranial fossa immediately above the roof the parotid branches (fig. 11). of the glenoid cavity. Here it divides into

Fig. 11 Vessels in relation to the temporomandibular area. Maxillary artery (1); parotid trunk (2); tympanic-middle meningeal trunk (3); condyle (4); posterior deep temporal artery (5); masseteric branch (6); buccal branch (7); (8); and mylohyoid branch (9). (Vinyl acetate injection; corrosion preparation.) HEAD AND NECK ARTERIES IN RHESUS 161 two main branches which run anteriorly the , the inferior alveo- and posteriorly. The anterior branch lar artery usually gives rise to a small my- passes on the inner aspect of the squam- lohyoid branch which distributes to the ous portion of the towards posterior part of the . the tip of the lesser wing of the sphenoid Within the mandible, the inferior alveolar bone where it anastomoses with the men- artery supplies the dental pulps, periodon- ingeal branch of the ophthalmic artery. tal membranes, interdental and interradic- The posterior branch is much smaller and ular septa, base of the mandible and the runs over the petrosquamous suture to an- area of the angle of the mandible (figs. 7, astomose with meningeal vessels of the 11, 12 and 13). A mental artery emerges posterior auricular and occipital arteries. through the and supplies In general, the meningeal artery is quite the soft tissue of that area. small and in half of the cases most of the medial side of the cranial vault is supplied Pterygoid arteries supply both the me- by a meningeal branch of the ophthalmic dial and lateral pterygoid muscles. The artery and by meningeal branches of the area of origin of the medial pterygoid mus- occipital and posterior auricular arteries cle receives its supply from arteries (fig. 8). The also arising from the tympanic-middle men- has anastomotic connections with its fel- ingeal trunk. These vessels distribute low of the opposite side by means of short mainly to the area of the . transverse communications which pass The middle portion and mandibular in- across the top of the skull above the supe- sertion of the is rior sagittal sinus. supplied by branches arising from the infe- A posterior deep temporal artery ascends rior alveolar artery, and by small branches vertically from its origin in front of the arising directly from the maxillary artery. capsule of the , The lateral pterygoid muscle receives small passes over the lateral pterygoid muscle arteries which come directly from the max- which it supplies, and continues upwards illary artery; additionally, the posterior to supply the deeper fibers of the tem- deep temporal artery sends small branches poralis muscle (fig. 18). Here it divides to it. into two or three secondary branches The , accompanied by the which spread out in a fan-shape manner buccal nerve, passes downward through towards the origin of the temporalis mus- the anterior portion of the temporalis mus- cle (figs. 7 and 10). cle to reach the posterior portion of the Near the origin of the posterior deep to which it distributes. temporal artery, small masseteric and The ascending and lateral branches of the capsular arteries arise which pass down- anterior also supply ward and posteriorly to their area of sup- the buccinator muscle by small branches ply. The masseteric branch passes through which end in the upper posterior portion the to supply the upper of the muscle. The main portion of the deep, portion of the masseter muscle. It is buccinator is supplied by branches of the a much smaller vessel than is the mas- facial artery. Anastomosis between all of seteric artery which arises with the parotid these vessels occurs within the muscle branches and is a minor arterial supply of (figs. 15 and 11). the masseter muscle. The capsular branch, Three or four anterior deep temporal often multiple, fans out as it passes back- arteries arise from the maxillary just ward to supply the anterior part of the before it passes into the pterygopalatine capsule of the temporomandibular joint fossa (fig. 7). Some ascend into the most (figs. 11 and 12). anterior fibers of the temporalis muscle The inferior alveolar artery arises me- while others descend into the fibers which dial to the neck of the condyle from the attach to the temporalis crest of the ramus lower surface of the maxillary artery. It of the mandible. passes obliquely downward and forward A few orbital branches arise from the close to the medial pterygoid muscle and maxillary artery at the pterygopalatine the interpterygoid . Before entering fossa, and pass through the inferior or- 162 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 12 Differential vascular supply of a mandible with permanent dentition. Arteries of the coronoid process (1) coming from the temporalis muscle. The arteries of the condylar process (2) arise from those of the capsule of the temporomandibular joint and lateral pterygoid muscle. Ves- sels of the angle region (3) arising from the inferior alveolar artery and from the vessels supplying the muscles attached to it. Branching arrangement of the alveolar dental arteries (4). (Teich- mann’s paste injection, decalcification and cleared preparation.) bital fissure to supply the tissues at the tal pulps, the periodontal membranes, and apex of the orbit (fig. 14). the interradicular and interdental septa The recurrent meningeal artery is ex- (fig. 14). The infraorbital branches arise tremely small and follows the maxillary either from the posterior superior alveolar nerve, passing posteriorly into the middle artery or from the . cranial fossa where it supplies the area of They are small branches which pass for- the (fig. 7). ward along the by spi- The posterior superior alveolar artery raling around and paralleling the nerve arises from the maxillary artery at the throughout its course (fig. 14). Emerging . It passes forward at the infraorbital foramen, these vessels for a very short distance along the floor terminate by distributing in the infraor- of the orbit, anterior and medial to the bital area and anastomosing with branches , where it enters a of the facial artery. small foramen near the anterior end of The sphenopalatine artery appears to be the fissure (fig. 14). It continues forward a direct continuation of the maxillary in the above and lateral to the artery. It passes through the sphenopala- . Throughout its course tine foramen and, after a short course, alveolar-dental branches are given off gives rise to posterior nasal and descend- which supply the teeth and supporting tis- ing palatine arteries (fig. 15). sues as far forward as the cuspid tooth. The posterior nasal arteries supply al- Each alveolar-dental artery divides into most all of the lateral nasal wall through secondary branches which supply the den- superior and inferior branches. The supe- HEAD AND NECK ARTERIES IN RHESUS 163

Fig. 13 Arrangement of the vessels in a mandible with mixed dentition. Vascular supply to the second molar tooth bud has two sources : from the vascular system of the temporalis muscle (1) and from the inferior alveolar artery (2); a single vessel from the inferior alveolar artery is supplying the pulp tissue of the developing first molar (3). The inferior alveolar artery ends at the level of the (4). (Schlessinger injection media; arteriograph preparation.)

Fig. 14 Distribution of arterial vessels in the maxilla. Posterior alveolar artery (1); infraorbital arteries (2); orbital branches (3); descending palatine artery (4); (5) and (6). (Teichmann’s paste injection; decalcified and cleared preparation.) 164 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 15 The sphenopalatine artery (1) branching into the posterior nasal artery (2) with its superior nasal branch (3) and inferior nasal branch (4) and the descending pala- tine artery (5) spreading out on the palate. (Vinyl acetate injection; corrosion preparation.) rior branch is distributed to the middle collateral branches, the lesser palatine nasal concha and meatus, and the maxil- arteries (fig. 14). The greater palatine lary sinus. The inferior nasal branch sup- artery is the main supply of the palate, plies the inferior concha and meatus, and and it is the direct continuation of the the floor of the (fig. 15). descending palatine trunk. It passes for- The posterior nasal artery also gives rise ward following the curvature of the upper to a branch which supplies the roof of the arch, medial to the teeth, towards the in- nasal cavity, and to a nasopalatine artery cisive foramen (fig. 16). Lateral to the which passes to the nasal septum and runs , branches of the greater obliquely forward and downward toward palatine artery pass upward through the incisive canal through which it passes. small foramina in the maxilla, behind the Here it anastomoses with the anterior anterior teeth. As small thin vessels they palatine artery (fig. 9). On the nasal sep- surround the apex of the upper central tum, the vessel also anastomoses with and lateral incisors. These branches sup- branches of the posterior and anterior ply the dental pulp, periodontal mem- arteries of the septum. branes, and supporting bone tissue of the The descending palatine artery passes anterior teeth (fig. 17). Throughout its downward and forward through the ptery- palatal course, the greater palatine artery gopalatine canal emerging at the greater distributes to adjacent tissue by medial palatine foramen (figs. 14 and 15). As it and lateral branches. The medial branches passes through the pterygopalatine canal, pass toward the midline to anastomose it gives rise to one or two small posterior with vessels of the opposite side. Lateral HEAD AND NECK ARTERIES IN RHESUS 165

Fig. 16 General distribution of greater palatine artery. Short vessels from the greater palatine artery (1) supply the gingiva and alveolar mucosa (2); palatal vascular arches anastomosing with those of the opposing side (3); lesser palatine artery (4); and arterial plexus in soft palate(5). (Teichmann’s paste injection; decalcified and cleared preparation.) branches are much thinner and supply the Internal carotid artery. From its point alveolar mucosa, gingiva, and alveolar of origin, the internal carotid artery passes bone (fig. 16). toward the base of the skull arching The lesser palatine arteries distribute slightly forward and medialward (fig. 18). mainly to the soft palate. Usually one or It is posterior to the external carotid two arteries are present, and they anasto- artery which it parallels for 1 cm. The mose with vessels from the opposite side artery is compressed between the posterior near the midline of the soft palate (figs. digastric and the longus colli muscles; the 14 and 16). is closely bound to its 166 WALTER A. CASTELLI AND DONALD F. HUELKE

Fig. 17 Profile view of greater palatine artery. Posterior alveolar artery (1); apex of the canine tooth (2); ascending terminal branch of greater palatine artery (3); greater palatine artery (4). (Teichmann's paste injection; decalcified and cleared preparation.) medial side. The ascending pharyngeal tern found in the human. However, some artery passes anterior and medial to it of these vessels have a different arrange- with the vagus nerve and internal jugular ment and therefore deserve special vein to its lateral side. Close to the base comment. of the skull the accessory, hypoglassal and Theile ('52) claims that in the Siminia glossopharyngeal nerves pass lateral to it. innus the sublingual artery passes as far In the of the base of the as the lower lip. However, in his publica- skull, the internal carotid artery is first tion there are no comments nor graphic perpendicular to the long axis of the pet- evidence showing how these arteries were rous portion of the temporal bone and distributed in the area of the mandibular then runs parallel to it. After leaving the carotid canal, the vessel passes through symphysis and lower lip. Our work has the where it traces a sig- confirmed these findings and has ex- moid course turning upward at the antero- plained the distribution of the vessel in lateral angle of the optic chiasm. The these two areas - in the mandible the course, distribution, and branches of artery supplies the bone about the sym- the internal carotid artery have been physis, the dental pulps of the four lower adequately described by Weinstein and incisors and their supporting tissues, the Hedges ('62) and by Theile ('52). alveolar bone and the periodontal mem- brane. This vascular arrangement is sim- DISCUSSION ilar to that found in the human mandible The general arterial plan of the head (Castelli, '63). In the lower lip the artery and neck of the Macaque follows the pat- passes upwards and bifurcates into two HEAD AND NECK ARTERIES IN RHESUS 167

Fig. 18 Arteriograph of head and neck. Principal arteries have been numbered. (Formalin em- balmed specimen injected with Schlessinger radioopaque media. ) 1. 12. Sphenopalatine artery 2. Internal carotid artery 13. Posterior nasal artery 3. Common trunk for occipital and posterior 14. Descending: palatine arterv auricular arteries 15. Facial artiri 4. External auditory meatus 16. Sublingual artery 5. Middle meningeal artery 17. Deep lingual artery 6. Ophthalmic artery 18. Lingual artery 7. Anterior meningeal artery 19. Inferior alveolar artery 8. 20. Superior thyroid artery 9. Posterior deep temporal artery 21. External carotid artery 10. Anterior deep temporal artery 22. Common carotid artery 11. Posterior superior alveolar artery principal lateral branches close to the free of the pharynx and is supplied by the border of the lower lip. ascending pharyngeal artery. The vascu- The structure of the nasal septum in larization of the septum then is supplied the Macaque has revealed an additional by three main arterial sources - the naso- nutrient source which is not seen in hu- palatine artery, the septal branch of the mans. The nasal septum projects back- sphenopalatine artery, and the septal ward as a membranous wall that divides branch of the ascending pharyngeal artery. the roof of the nasopharynx into two lat- The skin and subcutaneous tissue over eral compartments (Geist, '61 ). This the temporal fossa and part of the frontal membranous septum is close to the roof and parietal areas in the human is sup- 168 WALTER A. CASTELLI AND DONALD F. HUELKE plied by the superficial temporal artery. coronoid process and the area of the angle In the Macaque, however, this area is sup- is similar to that found in the human; plied by small branches arising from they arise from those vessels which supply neighboring arteries - posterior deep tem- the temporalis muscle and from those of poral, posterior auricular, and parotid the masseter and medial pterygoid mus- branches. This arterial disposition may cles respectively. account for the fact that in the Macaque Since the incisive area of the mandible the superficial temporal artery is repre- is primarily supplied by the sublingual sented by a very small vessel with limited artery, the distribution of the inferior al- distribution or is completely absent. veolar artery is, therefore, limited to the The distribution of the middle menin- body of the mandible, for as indicated geal artery in the of the above, the condyle, coronoid process, and Macaque is somewhat different from that incisive area are all supplied by other ves- found in the human. Its anterior branch sels. The inferior alveolar arterial distri- is much reduced in size and distribution. bution and its ascending alveolar-dental In the Macaque a large meningeal branch branches are quite similar to that found of the ophthalmic artery is distributed to in the human mandible. Fundamentally the lateral wall of the anterior and middle these vessels branch into thin collaterals cranial fossa, the area of supply of the to the interalveolar and interradicular anterior branch of the middle meningeal septa, to the periodontal membrane and artery in the human. to the pulp of the teeth. It was found Lineback ('61 ) described the middle that one or two arterial branches passed meningeal artery as the largest branch of into the pulp tissue of each dental root. the maxillary artery. We found as did This finding is in agreement with that Dyrud ('44) that the posterior deep tem- found in humans (Provenza, '59) and in poral artery is the largest branch arising cats (Castelli, '62). from the maxillary artery. As far as the supply of the periodontal When cleared preparations of the pa- membrane is concerned several authors rotid gland are studied a variable number (Orban, '53; Schubach and Goldman, '57; of arterial branches, arising from a com- Bernick, '60) have suggested that vessels mon trunk, are seen traversing the gland- of gingival origin also contribute to the ular tissue. These vessels radiate outward nutrition of the membrane. In fact, the toward the external surface of the gland. presence of these vessels was not con- The major part of these vessels supply the firmed as an additional vascular source parenchyma and stroma of the gland. other than those given by the alveolar-den- Some of these vessels extend beyond the tal branches; the only vessels which were gland to supply adjacent structures. One found in that area were venous and capil- artery supplies the masseter muscle and lary networks from the periodontium and is its main vessel. Others are distributed gingiva at the level of the dental crevice. to a limited area of the face distributing In the Macaque the participation of the as do the zygomaticoorbital and transverse greater palatine artery in the nutrition of facial arteries in the human. the intermaxillary bone and superior in- The distribution of the vessels supplying cisors is not like that found in the human. the mandible and maxilla have been The study of the cleared maxillae in the thoroughly studied in the cleared speci- Macaque shows the absence of the ante- mens. In general, the mandible in the rior superior alveolar artery. The region Macaque has the same arterial pattern as of distribution of the anterior superior in the human (Castelli, '63; Cohen, '59); alveolar artery was supplied by the exten- the condyle of the mandible receives its sion of the greater palatine artery upward nutrition by means of perforating arteries into the anterior part of the maxillary which come from vessels of the capsule bone. of the temporomandibular joint and from LITERATURE CITED those which supply the lateral pterygoid Bernick, S. 1960 Blood supply to developing teeth. Anat. Rec., 137: 141-145. muscle. Likewise, the origin and the dis- Castelli, W. A. 1962 Vascular structure of position of the vessels which supply the dental pulps in cats. J. Dent. Res., 41: 213. HEAD AND NECK AR TERIES IN RHESUS 169

1963 Vascular architecture of the hu- Provenza, D. V. 1959 The blood vascular sup- man adult mandible. J. Dent. Res., 42: ply of the dental pulps with emphasis on 786792. capillary circulation. Cir. Res., 6: 213-216. Chase, R. E. 1938 The coronary arteries in Reiner, L., and F. Rodriguez 1957 An injection 266 hearts of rhesus monkey. Am. J. Phys. mass of maximal radiopacity for postmortem Anthrop., 23: 299-320. . J. Mount Sinai Hospital, 24: Chase, R. E., and C. F. DeGaris 1940 On the 1139-1145. brachial plexus in macaca rhesus, compared Samuel, E. P., and R. Warwick 1955 The with man. Am. J. Phys. Anthrop., 27: 223-254. origin of the phrenic nerve in the rhesus mon- Cohen, L. 1959 Methods of investigating the vascular architecture of the mandible. J. Dent. key. J. Comp. Neur., 102: 557-563. Schubach, P. L., and H. Goldman A tech- Res., 38: 920-931. 1957 DeGaris, C. F., and E. M. Glidden 1938 nique of radiographic visualization of the vas- Branches of the aortic arch in 153 rhesus cular system of the periodontal tissues. J. monkeys. Anat. Rec., 70: 251-262. Dent. Res., 36: 245-248. Dyrud, J. 1944 The external carotid artery of Schwartz, D. J., and D. F. Huelke 1963 The the rhesus monkey (macaca mulatta). Anat. morphology of the head and neck of the Rec., 90: 17-22. macaca monkey: The Eyster, A. B. 1944 The cavernous sinus in a and the mandibular division of the trigeminal -macacus rhesus monkey. Anat. Rec., 90: 37-40. nerve. J. Dent. Res., 42: 1222-1233. Geist, D. F. 1961 The anatomy of the rhesus Teichmann, L. 1952 Cited by Schwering; monkey. Edit. by G. C. Hartman and W. L. Anatomische Trochen-Feucht und Knochenpra- Strauss, Jr., Hafner Publishing Co., New York. parate. Springer Verlag, Berlin, p. 79. Chapt. IX, 189-209. Theile, W. 1952 Die Arteriensystem of Siminia Huber, E. 1925 Ein M. Mandibulo-Auricularis Innus. Archiv Fur Anatomie, Physiologie, und Bei Primaten, Nebst Beitragen Zur Kenntnis Wissenschaftliche Medicin, 419-428. Der Phylogenese Ohrmuskulatur. Anat. Anz., Tokarski, S. 1931 Les Variations de L'Artkre 60: 11-21. Maxillaire Interne Chez L'Homme ExpliquBes Kennard, M. A. 1941 Abnormal findings in 264 par les Variations Chez les Primates. Comp. consecutive autopsies on monkeys. Yale J. Rendus, 25: 507-510. Biol. Med., 13: 701-702. Wagenen, G., and H. R. Catchpole 1956 Physi- Lineback, P. 1961 The anatomy of the rhesus cal growth of the rhesus monkey (macaca monkey. Edit. by G. C. Hartman and W. L. mulatta). Am. J. Phys. Anthrop., 14: 245-273. Strauss, Jr., Hafner Publishing Co., New York. Weinstein, J. D., and T. R. Hedges 1962 Studies Chapt. XII, 248-265. of intracranial and orbital vasculature of the Orban, B. 1953 Oral histology and embryology. rhesus monkey (macaca mulatta). Anat. Rec., Edit. by C. V. Mosby Co., St. Louis, p. 183. 144: 3742.