The Independent Functions of the Two Heads of the Lateral Pterygoid Muscle

Home , Lateral pterygoid muscle, Masseter muscle, Muscles of mastication, Temporal muscle

JAMES A. McNAMARA, JR. Department of Anatomy and Center for Human Growth and Development, The University of Michigan, Ann Arbor, Michigan 48104

ABSTRACT Investigations on the role of the lateral pterygoid muscle in mandibular movements have been limited due to difficulties in obtaining con- sistent neuromuscular recordings in human subjects. The rhesus monkey was used as a substitute experimental animal. Thirty-three Macaca mulatta were monitored in 113 electromyographic recording sessions. Two distinct functional patterns were identified from the region of the lateral pterygoid muscle, depend- ing upon the location of the electrodes within this muscle. Through anatomical dissection of areas of electrode placement in 12 animals, the two patterns of activity were related to the inferior and superior heads of the lateral pterygoid muscle. The inferior head acted synergistically with the suprahyoid muscle group in opening movements of the mandible. No activity was noted in closing movements, or in swallowing. In contrast, the superior head was not active during opening movements. Electromyographic activity of the superior head, antagonistic to the suprahyoid muscles, was observed during such closing movements as chewing and clenching of the teeth and during deglutition. The superior head presumably positioned or stabilized the condylar head and disc against the articular eminence during closing movements of the mandible, while the inferior head assisted in the translation of the condylar head downward, anteriorly, and contralaterally during opening movements. Thus, the two heads of the lateral pterygoid can be considered as two functionally distinct muscles.

The role of the lateral pterygoid in man- ness of the articular eminence and the dibular movement has historically been position of the pterygoid plates indicate a one of the most difficult to determine of more horizontal pull by the lateral ptery- all masticatory muscle functions. The goid in the monkey than in man. Schu- positions of the lateral pterygoid muscle macher ('61) and Grant ('73b) have within the infratemporal fossa has ham- demonstrated that orientation of the two pered human electromyographic studies heads of the lateral pterygoid in the mon- because electrode placement frequently key is similar to that in man, but that produced pain and regional hematomas they function at less oblique angles. In (Carlsoo, '52; Ekholm and Siirila, '60; man, a more oblique downward pull by the Griffin and Munro, '69). inferior head and a more oblique upward The rhesus monkey (Macaca mulatta) pull by the superior head is observed offers a substitute experimental animal. (Sicher, '60). However, in both man and However, specific differences exist in the the rhesus monkey, fibers from the supe- anatomy of the temporomandibular joint rior head are attached to the articular disc in man and the rhesus monkey. The flatter and capsule as well as to the condylar articular eminence, shallower glenoid head (fig. 2). fossa and larger postglenoid spine (fig. 1) The purpose of this study was to moni- have been noted in the rhesus monkey by tor and describe the functions of the lateral previous workers (Parsons, 1899; Zielin- pterygoid muscle in the rhesus monkey. ski, '65, and Zimmermann, '71). Angel 1This research was supported in part by United States public Health Service grants HD-02272 and ('48) has suggested that the relative flat- DE-03610.

AM. J. ANAT., 138: 197-206. 197 198 JAMES A. McNAMARA, JR.

Fig. 1 Photomicrograph of a sagittal section of the temporomandibular joint. PGS, postglenoid spine; C, mandibular condyle; D, articular disc; AE, articular eminence; F, superior portion of the glenoid fossa. Hematoxylin and eosin. x 8.

MATERIALS AND METHODS electrodes, 1-3 mm apart. In addition, Thirty-three Macaca mulatta, age six pairs of 8 mm bipolar platinum electrodes months to eight years, were monitored in were inserted aseptically into the anterior 113 electromyographic recording sessions, temporal, posterior temporal, anterior bor- consisting of one to two and one-half hours der of the superficial head of the masseter, each. Initially, the animal was anesthetized superior portion of orbicularis oris, and by an injection of 6-10 mg/kg of Keta- the suprahyoid group of muscles including mine HCl, a short-acting, dissociative the anterior digastric, mylohyoid and genio- anesthetic which has only a minor and hyoid muscles (fig. 3). The latter three transient effect upon the neuromuscula- muscles were regarded as a single muscle ture (McNamara and Kuroda, '71; Kuroda group because of the difficulty in separat- and McNamara, '72). ing them anatomically during positioning The anesthetized monkey was then of electrodes. The anterior heads of the placed in a sound-proof, electrically shield- two digastric muscles in the rhesus monkey ed chamber and chaired in a primate re- are not separated into two discrete bellies, straining device especially designed for as is typical in man. Rather, the anterior electromyographic procedures (McNamara, heads fuse at the midline and, in addition, '73). The head of the animal was oriented often blend with fibers of the mylohyoid in a fixed position by means of a Plexiglas muscle (Bosma, '56; Howell and Straus, headholder to allow for normal jaw func- '69). All recordings were taken from the tion in an unanesthetized condition. musculature on the left side. Electromyo- The approach to the lateral pterygoid graphic activity was recorded on Kodak muscle was made extra-orally through the Linagraph direct print paper using a Beck- sigmoid notch of the mandible using two man Type R Dynograph amplifier and a 25 mm Teflon insulated bipolar needle Honeywell Model 1108 Visicorder. FUNCTIONS OF THE LATERAL PTERYGOID HEADS 199

Fig. 2 Photomicrograph of a medial s8agittal section of the attachment of the laded pterygoid muscle into the amticular disc, joint capsule, and mandibular condyle. Hematox- ylin and oosin. x 8.

After verification of electrode placement, goid muscle. Sometimes pattern A was re- the animal was left isolated in the sound- corded, sometimes pattern B was recorded, proof room for a minimum of 30 additional and in a few instances a third pattern of minutes to allow for complete recovery activity was observed. It was soon obvious from the anesthetic. After this time, re- that the latter pattern represented a super- cordings of posture, oral reflexes, and imposition of pattern A and pattern B in random jaw movements were initiated the electromyographic records. The occur- while the animal was still in isolation. Re- rence of each pattern of lateral pterygoid flex salivary swallows were recorded at muscle activity depended upon the specific this time. Later, the investigator entered location of the pair of electrodes within the sound-proof room and generated water the muscle. The location of electrode swallows and subsequent clearing swal- placement in 12 animals was examined lows through the administration of 0.5 ml through anatomical dissection and the two tap-water by a syringe into the animal’s patterns of activity (patterns A and B) mouth. Chewing was elicited by feeding were related to the inferior and superior the animal small chunks of sugar and bits heads of the lateral pterygoid muscle, re- of apple. spectively. A drop of India ink was in- jected at the placement site of electrode OBSERVATIONS tips, the animal was sacrificed immedi- Initially no attempt was made to differ- ately, these areas were examined, and the entiate between the functions of the two precise location of the electrodes within heads of the lateral pterygoid muscle. the muscle noted. However, during the recording sessions, Pattern A (the inferior head). The lat- three patterns of muscle activity were ob- eral pterygoid muscle acted synergistically served in the region of the lateral ptery- with the suprahyoid muscle group in 200 JAMES A. McNAMARA, JR. opening movements of the mandible (figs. and contralaterally during opening move- 4, 5). The lateral pterygoid did not appear ments of the mandible. to initiate opening movements because the Pattern B (the superior head). This onset of activity in the suprahyoid usually pattern of activity was distinctly different preceded lateral pterygoid firings. How- from that of pattern A. The firings of pat- ever, the duration of suprahyoid activity tern B occurred during a different phase before the initiation of lateral pterygoid of mandibular movement than did those function varied, ranging from 25-350 of the suprahyoid musculature and thus no msec. The lateral pterygoid muscle was activity was recorded in the superior head never active during the closing movements of the lateral pterygoid during opening of the mandible, such as clenching and the movements of the mandible. Discharges closing phase of mastication, nor did it from the superior head were observed dur- function in salivary, water, or masticatory ing closing movements (figs. 4, 6). The swallows (fig. 5). onset of lateral pterygoid function was Anatomical dissection confirmed that usually concurrent with that of the eleva- pattern A originated from the inferior head tor musculature during the closing phase of the lateral pterygoid muscle. This head of mastication and during clenching of presumably assisted in the translation of teeth. the condylar head downward, anteriorly, The superior head of the lateral ptery-

Fig. 3 Animal positioned in head-holder. Needle electrodes are in the anterior and posterior portions of the temporal muscle, the anterior portion of the superficial head of the masseter muscle, the orbicularis oris muscle, the lateral pterygoid muscle and the suprahyoid muscle group. FUNCTIONS OF THE LATERAL PTERYGOID HEADS 20 1

5 sec

A. TEMP - I1

f? TEMP I

MASS. v.L. ,L

A. TEMP -t-,

f? TEMP L

ORBIC. ORIS. s SUP. HY

LATPT (SUP)--"

Fig. 4 Electromyographic recordings of the activity of the lateral pterygoid muscle during random jaw movement. (a) The activity of the inferior head (Pattern A) was usually associated with suprahyoid function during opening movements of the mandible and was antagonistic to the elevator muscles. (b) The superior head (Pattern B) acted synergistically with the masseter and temporal musculature during closing movements of the mandible. A. Temp., anterior portion of the temporal muscle; P. Temp., posterior portion of the temporal muscle; Mass., anterior portion of the superior head of the masseter muscle. Orbic. oris, superior portion of orbicularis oris; Sup. Hy., suprahyoid muscle group; Lat. Pt. (Sup.), superior head of the lateral pterygoid muscle; Lat. Pt. (Inf.), inferior head of the lateral pterygoid muscle. Recording speed 5 mm/sec. goid muscle was also active during swal- lature in a well circumscribed burst of lowing, but the onset and duration of this activity for 250-350 msec in swallows with activity varied. The superior head usually little or no elevator function. In four fired concurrently with suprahyoid muscu- animals the onset of lateral pterygoid activ- 202 JAMES A. McNAMARA, JR.

500pv 500 msec

A. TEMP

P.TEMf?

ORBIC. ORIS.

SUP. HY.

LAT. PT. (INF.) 4- -- 1 IU Masticat ion Deglutition Fig, 5 Electromyognaphic renordhgs of the activity of the inferior head of the lateral pterygoid muscle during mastication and deglutition. Recording speed 100 mm/sec. ity during this type of swallow preceded He states that the origins of the two heads suprahyoid function by 25-100 msec. In are separate, that the fibers of each head all animals, the activity of the superior run in entirely different directions, that head occurred concurrently with that of there is no fusion of the fibers of each the masseter and temporal muscles in entity, and reasons that they must have those swallows associated with mastication separate functions. Grant ('73b) notes (fig. 6). similar findings in a biomechanical study Pattern B was confirmed by dissection of the lateral pterygoid in both man and to originate within the superior head of the the rhesus monkey. He states that the lateral pterygoid muscle. This head, which two heads have quite different orientations is directly contiguous with the articu- and relationships to the instantaneous lar disc, the joint capsule, and with the centers of rotation of the mandible (Grant, condylar head, was not active during open- '73a). The superior head is biomechani- ing movements as was the inferior head, cally suited to close the jaws while the but rather had a separate and independent inferior head is suited to function in open- function. ing movements. Grant states the lateral pterygoid muscle is more efficient mechani- DISCUSSION cally in opening the mandible if only the Christensen ('69) has observed that the inferior head is active than if both heads two heads of the lateral pterygoid muscle function in this movement. in man are distinct anatomical entities. The results of the current study indicate FUNCTIONS OF THE LATERAL PTERYGOID HEADS 203

500pv 500 msec

A. TEMP

P. TEMP

MASS. I ORBIC. ORIS.

SUP. HY.

LAT. PT. (SUP) I Mastication Oeglutitioi Fig. 6 Electromyographic necordings of the activity of the supmior head of the lateral pterygoid muscle during mastication and deglutition. Recording speed 100 mm/sec. that the two heads of the lateral pterygoid ing such functional movements as chewing muscle in Macaca mulatta are functionally and swallowing. Sicher ('60) states that independent. The superior head of the the holding force of the lateral pterygoid lateral pterygoid in the monkey is shown in man is necessary to prevent the dis- to be the only portion of the muscle elec- placement of the mandible during mastica- trically active during closing movements tion. Perhaps increased contraction of the while the inferior head with a downward superior head may move the articular disc, orientation is active during opening move- condylar head, and joint capsule anteriorly ments. The latter head presumably assists and slightly superiorly, presumably against translations of the head of the condyle the posterior and inferior surface of the anteriorly, inferiorly, and contralaterally, articular eminence. Thus, this head may that is, in movements in which the condy- act as a positioner of the condyle and artic- lar head is moved freely relative to the ular disc along the articular surface of articular eminence. the temporal bone. It can be postulated that a slight con- Previous electromyographic studies in traction of the superior head may stabilize man have not differentiated between the the condylar head and articular disc, keep- functions of the two heads of the lateral ing them synchronized with one another pterygoid muscles. Most investigators have during movement against the articular emi- agreed that the lateral pterygoid muscle nence of the temporal bone, especially dur- functions in protrusive and lateral move- 204 JAMES A. McNAMARA, JR.

ments of the mandible (Moyers, '50; Zenker (e.g., specific salivary swallows). Thus, a and Zenker, '55; Carlss, '56; Woelfel et contraction of the superior head may sta- al., '57, '60; Maller, '66; Griffin and Munro, bilize the condylar head and disc against '69). However, confusion remains as to the articular eminence. In contrast, close the role of this muscle in opening and approximation of the condylar head and closing movements. Moyers ('50) has disc to the articular eminence may not be suggested that the primary function of the essential in opening movements or even lateral pterygoid is to draw the condylar desirable in wide open movements. Fur- head and disc forward, but he also sug- ther increased contractions of the superior gests that the lateral pterygoid is responsi- head of the lateral pterygoid, as in more ble for the initiation of mandibular depres- protrusive closure patterns, may help main- sion while the suprahyoid muscles are tain the relationship of the condylar head operative in the completion of the move- and disc as the mandibular condyle is ment. Hickey et al. ('57a) and Woelfel positioned or rotated anteriorly along the et al. ('60) in contrast found that the articular surface of the eminence. lateral pterygoid is active only in "uncon- Some care, of course, must be taken in trolled openings, i.e., with anterior trans- directly relating the findings of the current lation of the condyle, but when a hinge study of the role of the lateral pterygoid opening is performed, the suprahyoids muscle in Macaca mulatta to the role of function unassisted. Ekholm and Siirila the same muscle in man, especially consid- ('60) stated that the lateral pterygoid is ering the anatomical differences between not essential for opening, but that it is the two species previously described. For habitually used to place the condyle in a both the rhesus monkey and man, further more favorable position. investigations into the nature and orienta- Activity in the lateral pterygoid during tion of the fibers of each head as well as closing movements has not been observed the innervation and muscle spindle distri- by all investigators. Zenker and Zenker bution are necessary if a more complete ('55), Carlsoo ('56), Hickey et al. ('57b), understanding of the roles of the lateral Maller ('66), and Griffin and Munro ('69) pterygoid muscle is to be attained. observed some degree of activity during ACKNOWLEDGMENTS elevation of the mandible. Moyers ('50), Woelfel et al. ('57, '60), and Ekholm and The author wishes to thank Dr. Takayuki Siirila ('60) did not note firing during Kuroda, Dr. Daryl Bowden, and Dr. Robert these movements. E. Moyers for their help in the preparation The discrepancy in the above findings is of this manuscript. The author is also undoubtedly related to the fact that the grateful to Dr. Merle Lawrence and Dr. lateral pterygoid has been considered to Robert E. Stone of the Kresge Hearing Re- be a single functional entity and variations search Institute for providing the electro- in electrode placement within the separate myographic facilities used in this studv. heads of the muscle have not been consid- IlIustrations were prepared by Ms. SalIy ered. As has been found to be the case Everhardus, Mr. Gerald G. Davenport, and with other muscles of mastication (e.g., Mr. Edward E. Sayer. masseter, temporal), ascribing a single LITERATURE CITED primary function to the lateral pterygoid Angel, J. L. 1948 Factors in temporomandib- muscle likely misrepresents the total scope ular joint form. Am. J. Anat., 83: 223-246. of activity of this muscle. In the current Bosma, J. F. 1956 My-ology of the pharynx of study the lateral pterygoid muscle in cat, dog and monkey with interpretation of Macaca rnulatta demonstrated several dis- the mechanism of swallowing. Ann. Oto. Rhino. Laryng., 65: 981-992. tinct and independent functions: the infe- Carldo, S. 1952 Nervous coordination and rior head participated with the suprahyoid mechanical function of the mandibular ele- muscle group in opening movements of vators. Acta Odont. Scand., 10: 132 pp., the mandible, while the superior head was Suppl. 11. 1956 An electromyographic study of electrically active both in closing move- the activity, and an anatomic analysis of the ments (e.g., mastication) and in move- mechanics of the laterd pterygoid muscle. ments with little or no elevator activity Acta Anat., 26: 339-351 FUNCTIONS OF THE LATERAL PTERYGOID HEADS 205

Chrisbensen, F. G. 1969 Some anatomical con- cordings of rliesus monkeys. J. kt. Res., cepts associated with the temporomandibular IADR Suppl. #485, p. 184. joint. Ann. Austral. Coll. Dent. Surg., 2: 39- Mldller, E. 1966 The chewing apparatus. An 60. eleotromyographic study of the action of the Ekholm, A., adH. S. Siirila 1960 An electro- muscles of mastication and its correlation to myographic study of the function of th,e lateml facial mcuphology. Aota Physiol. Scand., Vol. pterygoid muscle. Suom. Hammaslaak. Toim, 69, Suppl. 280. 56: 90-106. Moyers, R. E. 1950 An electmmyographic Grant, P. G. 1973a Biomechanical significance analysis of oertain muscles involved in tem- of the instantaneous center of rotation: the pammandibular movement. Am. J. Orthodont., human temporomandibular joint. J. Biomech., 36: 481-515. 6: 109-113. Parsons, F. G. 1899 The joints of mammals 1973b Lateral pterygoid, two muscles? compwed with those of man. J. Anat. Physiol., Am. J. Anat., 138: 1-10. 34: 41-68. Griffin, C. J., and R. R. Mumo 1969 Electm Schumacher, G. H. 1961 Fudtionelle Mor- myogrephy of the jaw-closinlg muscles in the phologie dar Kaumuskulatur. Gustav Fischer open-close-clench cycle in man. Archs. oral Verlag, Jena. Biol., 14: 141-149. Sicher, H. 1960 Oral Anatomy. Third edition, Hickey, J. C., J. B. Woelfel and L. Rinear 1957a C. V. Mosby Co., St. Louis, Miswuri. The duenoe of overlapping electrical fields on the interpretation of electzomyograms. J. Woelfel, J. B., J. C. Hickey and L. L. Rinear Prosth. Dent., 7: 273-281. 1957 Ekctromyographic evidence supporting the mandibulax himge axis theory. J. Prosth. Hickey, J. C., R. W. Stacy and L. Rinear 19571, Eleotromyographic studies of mandibuliar Dent., 7: 361-367. muscles in basic jaw movements. J. Prosth. W(oelfe1, J. B., J. C. Hickey, R. W. Stacy and L. L. Dent., 7: 565-570. Rimear 1960 Ebctromyographic analysis of Howell, A. B., and W. L. Straus, Jr. 1969 The jaw movements. J. Prosth. Dent., 10: 688-697. Anatomy of the Rhesus Monkey, C. G. Hart- Zenker, W., and A. Zenker 1955 Die Tatigkeit man and W. L. Straus, Jr., eds. Hafner Pub- der Kiefermuekeln und ihre dektromyographi- lishing Co., New York, Chap. VII, pp. 89-175. sche Analyw. 2. Anat. Entwicklgesch., 119: Kuroda, T., and J. A. McNamara, Jr. 1972 174-200. The effect of ketamine and phencyclidine on Zielinski, D. E. 1965 A study of the nnmmal muscle activity in non-human primates. anebomy of the masticatory appar;utus of Anesth. Analg., 51: 710-716. Macaca mulatta. M.S. Thesis, Loyola Univer- McNamara, J. A,, Jr. 1973 Resrtraint of mom sity Graduate School, Chicago, Illinois. keys fa craniofacial research. J. Dent. Res., Zimmexmann, H. I. 1971 The normal gnowth 52: 183. and xmodeling of the tempmomanidibular McNamara, J. A., Jr., and T. Kuruda 1971 joint of Macaca mulatta. M.S. Thesis, Univer- Anesthetic artifacts in electmmyographic re- sity of Washington, Seattle, Washington.