Feeding in Golden , Mesocricetus auratus

GERARD C. GORNIAK ' Division ofBiologica1Sciences, The University of Michigan, Ann Arbor, Michigan 48109

ABSTRACT Simultaneous cine and electromyographic records of freely feed- ing, unanesthetized golden hamsters show that their motion and muscular activ- ity during mastication differ from those of albino rats (Weijs, '75). Rats show only propalinal motion while hamsters show lateral translation as well. The mas- ticatory muscles of hamsters and rats are generally similar, but their molar den- titions differ. The interlocking molar cusps of hamsters restrict propalinal pro- trusion and retrusion when the molars are in occlusion; however, hamsters readi- ly unlock occlusion by a twisting movement in the horizontal plane. Rats may perform propalinal movements even with the teeth in occlusion. In mastication the 's jaw moves laterally as well as vertically and an- teroposteriorly. Chewing orbits typically reverse after one to three orbits. Rever- sal begins at the start of the upstroke and involves a lateral shift in the opposite direction with the mouth closed. Electromyograms show that symmetric and asymmetric activities of closing protrusive and closing retrusive muscles produce a unilateral force couple on both sides. (This couple accompanies a midline closing stroke.) When the mouth is closed, unilateral activity of closing retrusors and closing protrusors also in- duces lateral translation. A bilateral force couple pits the retrusors of one side against the protrusors on the opposite side. Simultaneous with lateral excursion to the opposite side of midline and the action of these closing muscles, the anteri- or digastric and lateral pterygoid muscles of one side fire asymmetrically. The mandible moves downward coincidently with bilateral activity of the di- gastrics and lateral pterygoids. As the jaw opens further, activity differences of the lateral pterygoids accompany a shift of the mandible toward midline. At the end of the downstroke, all masticatory muscles studied are silent. The jaw returns to midline when the adductors fire asymmetrically at the start of closing. Trituration appears to coincide with an initial simple protrusion, which is sub- sequently accompanied by lateral translation. Different food types are reduced by distint chewing patterns with the differences clearest when the teeth are near occlusion. During gnawing the lateral pterygoids and digastrics fire longer, and the closing muscles fire less strongly. Chewing patterns in golden hamsters ap- pear more generalized than those of rats; the differences may be directly associ- ated with the ability of hamsters to store food in their cheek pouches.

Much of our present understanding of the terns (Turnbull, '70). Although aspects of this function of the mammalian masticatory sys- classification are certainly still open to ques- tem has been based upon comparative ana- tion (Crompton and Hiiemae, '70; Kallen and tomical studies of teeth, skulls and mastica- Gans, '72), it is clear that show one of tory musculature (cf. Arendsen de Wolff- the extremes of modifications in their masti- Exalto, '61; Becht, '53; D'Amico, '65; Hiiemae, catory apparatus. Accordingly, further infor- '67; Smith and Savage, '59; Turnbull, '70). Ex- mation about diverse rodents should enhance trapolation from such structural data has ' This study in part of my diseertation research which wan conduct- diverse masticatory processes to be edat the Department of Anatomical Sciences. The State University of subdivided into general and specialized pat- New York at Buffalo.

J. MORPH., 154: 427-458. 427 428 GERARD C. GORNIAK our understanding of the masticatory process the masticatory muscles (as in rats) tend to generally (Gans, '66a). Mastication has al- move the jaw in the sagittal plane. Asymmet- ready been studied in the laboratory rat, Rat- ric activities, which couple protrusive forces tus norvegicus albinus (Hiiemae and Ardran, of one side with retrusive forces of the other, '68; Weijs, '75; Weijs and Dantuma, '75) and apparently induce (as in bats) lateral transla- is now being investigated in guinea pigs (de tions of the mandible. Vree, '77). The present work deals with masti- Even though the masticatory muscles of cation in another myomorph , the golden hamsters and albino rats (Weijs, '75) . Mesocricetus auratw. have a similar gross configuration, the ani- The comparative morphology of teeth has mals show different molar dentitions and mas- received the greatest emphasis thus far. Wear ticatory movements. The present analysis of patterns on the occlusal surfaces of the denti- golden hamsters extends beyond the descrip- tion are assumed to reflect the path of masti- tion of their jaw movements during chewing catory movements (Brodie, '34; Butler, '56; and examines aspects of gnawing and pouch- Fox, '65; Mills, '67; Peyer, '68; Ryder, 1878). ing. It also considers whether mastication oc- In rodents the configuration of the cheek curs simultaneously on both sides, or if each teeth (molars) varies considerably; some show cycle involves chewing on one (the active) side a low brachyodont form and others have more only. prominent conical cusps (Peyer, '68). These MATERIAL AND METHODS differences in their molar dentition suggest that rodents might show chewing strokes Adult golden hamsters (Mesocricetus aura- ranging from a simple translational motion tud, members of a colony bred originally from (in frontal view) to more ellipical orbits. The five in the functional morphology lab- molar dentitions of hamsters and rats differ oratory at Buffalo, were studied. Morphology markedly. For these reasons, hamsters were of the teeth and the bony configuration of the chosen to test the current hypotheses of mas- jaws and mandibular fossae were described ticatory patterns. from four skulls. The temporomandibular While the anatomy of the masticatory sys- joints and masticatory muscles were de- tem, feeding behavior, and diet may differ scribed after dissection of twelve preserved (Walker, ,641, mammalian masticatory mo- heads. Heads of two freshly sacrificed animals tions generally incorporate a lateral compo- were stored overnight in 80%alcohol and then nent. Domestic rabbits (Ardran et al., '58; dissected; another specimen was dissected Ardran and Kemp, '60), ungulates (Becht, '53; without preservation. Muscular morphology de Free and Gans, '76; Herring and Scapino, was confirmed during routine autopsies of the '73; Hildebrand, '37; Ryder, 1878; Smith and 30 hamsters used for electromyography. Savage, '59), little brown bats (Kallen and All gross observations were made under a Gans, '72), rhesus monkeys (Luschei and Wild dissecting microscope at magnifications Goodwin, '741, and American opossums between X 3 and x 25. Drawings were made (Crompton and Hiiemae, '70) all show lateral with a Wild camera lucida, and photographs translation during matication. Distinct feed- were taken with a Miranda SLR 35mm ing habits, such as pouching in hamsters Ke., camera. the process of storing food in its cheek pouch- Masticatory muscles were dissected in lay- es), may modify chewing strokes among ro- ers to note sites of muscular attachment. The dents with generally similar anatomy. temporalis and digastric muscles became visi- We now have studies (Crompton et al., '77; ble immediately after removal of the skin. Ex- De Vree and Gans; '76; Herring and Scapino, posure of the masseteric complex entailed an- '73; Kallen and Gans, '72; Luschei and Good- terior retraction of the overlying cheek pouch. win, '74; Weijs and Dantuma, '75) in which The pterygoid muscles were exposed by re- jaw movement and electromyograms of the moval of the tongue, pharynx, and hyoid mus- masticatory muscles have been recorded si- culature; the digastrics did not have to be re- multaneously. In bats (Kallen and Gans, '72) moved to obtain adequate exposure of the the muscles of both sides are generally active pterygoids. Tissues were moistened with dis- during different times of the masticatory cy- tilled water to facilitate the separation of cle. In contrast, rats (Weijs and Dantuma, '75) muscles along fascia1 planes. have bilaterally symmetrical activity of all Dissected temporomandibular joints were masticatory muscles. Symmetric activities of examined for the relative thickness and loca- FEEDING IN GOLDEN HAMSTERS 429

D- D

Fig. 1 Diagram of feeding enclosure used in this study. A. Mirror used to record frontal views of masticatory movements. The anterior Plexiglas shelf and bottom of a laboratory pellet hw)are shown in reflection. B. Mirror used for simultaneous lateral cine views. The side of the pellet (arrowhead) irc Been through a plexiglae plate on that side of the enclosure. C. Test tube clamp used to hold pellet. D. Miniature connector (male) suspend. ed above open top of cage.

tion of capsular ligaments, the passive limits x-ray machine (filters removed) for 20 seconds of mandibular motion during vertical, hor- at 10 milliamperes. The positions of the con- izontal and propalinal excursions, and the de- dyle and teeth were recorded in all three spec- gree of rotation permitted about the long axes imens. of the mandibular bodies (i.e., the amount of Thirty conditioned hamsters were fed sep- spread permitted between the tips of the lower arately in a shielded enclosure (18 cm x 9 cm incisors). Similar passive manipulations were x 23 cm) in which the floor was elevated 5 cm performed on three anesthetized hamsters. above an anterior Plexiglas shelf and one side Capsules were also incised horizontally walled off by a vertical Plexiglas window (fig. around the anterior and lateral aspects of the 1). Mirrors, placed respectively below and to condylar neck to examine the configuration one side of the viewing partition, were adjust- and limits of the articular disc. ed to show simultaneous anterior and lateral Heads of three freshly-killed hamsters were views of the head. Sunflower seeds and labora- fixed in 10% formalin: one with the mouth tory pellets coated with sugar water (Charles closed, another near mid-opening, and a third Rivers maintenance formula) were offered. at maximum gape. Each head was split sagit- The pellets were held above the anterior plex- tally and then x-rayed with a Universal dental iglas shelf by a test tube clamp (fig. 1). 430 GERARD C. GORNIAK

Frame-by-frame analysis of cine films used parallel to the root of the arch and through the the lower incisors as indicators of mandibular posterior temporalis until it contacted the lat- movement. Actual point by point plotting of a eral cranial wall. The tip of the needle was complete chewing cycle becomes less accurate then pushed about 0.5 cm upwards and ante- when the mouth is closed; the lower incisors riorly along the bone toward the middle of the are then hidden from view by the lower lip and eye. overriding upper incisors. Hence, a 6-mm-wide Four to eight electrodes were ordinarily im- anterior segment of the lower lip was removed planted (and color coded) during a single sur- surgically two to three days before 19 experi- gical procedure. Bipolar electrodes of 0.003- mental sessions. Neither control motion pic- inch teflon-coated silver wire (Medwire Corp., ture sequences nor direct observations re- Mt. Vernon, New York; most muscles) and vealed significant change in hamster feeding 0.0009-inch “karma green” wire (Driver-Har- behavior after removal of the lower lip or sur- ris Corp., Harrison, New Jersey; lateral ptery- gical implantation of electrodes for electro- goid and deep temporalis) were used to record myography. Eight unoperated hamsters were intramuscular electrical activity. Electrode filmed (as controls) during chewing and gnaw- wires were kinked two or three times near ing and five while pouching foods of different their point of emergence from a muscle, form- size. These records made it easy to distinguish ing them into springs and thereby facilitating gnawing and pouching behavior from chewing their intramuscular retention. Each electrode in subsequent electromyographic and move- pair was passed from the surgical incisions ment analyses. through a 15-gauge hypodermic needle that An average dose of 0.3 ml nembutal sodium had been inserted from a site between the (50 mg/ml) was administered intraperitoneal- scapulae and run under the skin, superficial to ly for all surgical procedures. The ventral and the cheek pouches. The bared free ends of the lateral surfaces of the mandible as well as an electrodes were soldered to a harness of light- area from behind the eyes to the scapular re- weight earphone wire (Audio Center, Buffalo, gion were cleared of hair with a depilatory New York) collected at an Amphenol connec- lotion (“Neet,” Whitehall Laboratories, New tor and insulated with appropriately color York, New York). All electrodes were implant- coded electrical tape. The connections were ed through incisions, and most muscles were fastened to the ’s back and coated with exposed directly. Implantation into the digas- a noxious solution used to prevent nail-biting trics, medial and lateral pterygoids, and the in humans (Stop-Zit, Purepec Corp., Eliz- masseteric complex occurred through a 1-cm abeth, New York). The connector was sus- ventral incision along the side of each mandib- pended from the open top of the holding cages. ular body. Medial retraction of the digastric Recording sessions always started more than permitted direct observation of the medial 24 hours post-operative in order to permit pterygoid. Posterior retraction of the medial complete recovery from the anesthesia. pterygoid exposed the lateral pterygoid mus- Two different electrode configurations were cle. Electromyographic sequences from the used. The first (fig. 2 top) is that described by muscles, which had been retracted during sur- Kallen and Gans (‘72). In order to guard gery, showed no detectable change from those against shorting out (by contact) of the elec- of the non-retracted muscle in the same or trode tip, it was modified slightly. The bared other animals. Electrodes were placed blind tips were of equal length: one millimeter on within the deep masseter and anterior zygo- the Karma electrodes and two millimeters on maticomandibularis muscles by passing the the silver. The wire was looped in the middle needles, respectively about 1 and 1.4 cm, up- and the limbs of the loop twisted five or six ward and rostrally through the superficial times. One to two millimeters of insulation masseter. No significant change in superficial were removed on one side of the loop, just dis- masseter activity was noted as a result. The tal to the twist. One-half of this bared length anterior and posterior temporales of both sides was twisted again, around the other insulated were exposed through a 1.5-cm midline inci- limb of the loop. For the other tip, a section of sion along the dorsum of the head. Electrodes insulated wire was left intact, distal to the were placed in the deep temporalis through an twist and equal to the bared untwisted area incision along the upper posterior margin of already exposed. The second end was then the zygomatic arch; the needle was passed bared distal to this insulation and both elec- FEEDING IN GOLDEN HAMSTERS 43 1

Fig. 2 Photograph of electrodes used in this study. Top Injection type electrode made of 0.003-inchteflon coated silver wire. Bottom Pass through electrode formed from 0.003-inch teflon coated silver wire. trode tips bent backwards at the distal end of tion was provided by a notched metal disc, the twist. The silver electrodes were inserted mounted on the externally-located sound syn- with 26-gauge needles and the Karma wire chronization shaft of the camera. This disc with 27-gauge. was located in front of a prefocussed light A second electrode configuration (fig. 2 source, and the notch permitted a pulse of bottom), formed from the 0.003-inch silver light to pass through an optical fiber to the wire solely to record activities from the ante- face of the oscilloscope screen. A similar opti- rior digastric muscles, was needed to retain cal fiber arrangement displayed 1-second time electrodes in these muscles. Two separate intervals. Both ends of these optical fiber bun- lengths of wire were tied together with a dles were flattened to enhance the amount of square knot, leaving two short free ends. Two light transmitted and the end at the oscillo- millimeters of insulation were removed from scope screen was bent at right angles to face each short end, close to the knot, and each the camera. All available channels on the Tek- bared length was twisted completely about its tronix 535A oscilloscope with type M plug- respective, longer insulated segment. One end in unit could then be used for simultaneous of the electrode was threaded into a curved, recording of electromyograms. Traces were hubless, 26-gauge hypodermic needle that was photographed on Kodak 2495 RAR film with a passed completely through the muscle, im- Grass C4 camera run at 100 mmhec with con- planting the twisted portion of the electrode. tinually open shutter. Other experiments em- Some motion picture sequences were record- ployed a Beaulieu R16 camera with strobe il- ed on Kodak Ektachrome EF daylight film at lumination and a photocell providing a signal 33 and 64 frames per second with a Beaulieu for individual film frame identification (Gans, R16 camera using two Color-"ran narrow '66b). Up to eight electrode signals were beam spotlights. Individual frame identifica- amplified through four 26A2 andfor four FM 432 GERARD C. GORNIAK ANTERIOR POSTER IOR - P BUCCAL t ps pc mc I, I

Maxillary molars

I JI prcl prc hc LINGUAL

pc Id pcdI1 mcd

Mandibular molars P\rd phd h\cd BUCCAL 4 U lmm Fig. 3 M.auratus. Molar dentition. The occlusal surfaces of the right side of the specimen are shown. Hc, hypocone; hcd, hypoconid; mc, metacone; mcd, metaconid; pc, paracone; pcd, paraconid; pcld, paraconulid; prc, protocone; prcd, protoconid; prcl, protoconule; prsd, protostylid; ps, parastyle. (Nomenclature of Osborne, cf. Kraus et al., '69). With the teeth in occlusion, the protoconid of the second mandibular molar fits just mesial to the paracone of the second maxillary molar overriding the parastyle. The metacones of the first and second upper molars lie in the groove just distal to the respective hypoconids, overriding the protostylids of the second and third mandibular molars. The paraconids of the second and third mandibular molars fit lingually between the adjacent boundaries of the first and second, and second and third maxillary molars respectively.

122 Tektronix preamplifiers, monitored on a tive positions of maxillary incisors (when ex- Brush 481 strip chart recorder and a Tektron- posed) were cross checked with those of the ix 565 oscilloscope, and stored for later use on nostrils and upper end of the median cleft of a Honeywell 5600 medium bandpass, multi- the upper lip. In animals with a segment of lip channel tape recorder. removed, the point at which the cleft, between Electromyograms from a given hamster the lower incisors intersects the gingival could be recorded daily for up to five days, but margin, was employed in frontal view for all experiments usually ran for three days. Each except the one or two frames showing max- animal was then sacrificed with ether and imum gape when this reference point was autopsied to determine the exact placements nearly horizontal. This point was approxi- of the electrodes (figs. 6-81. mated by plotting the cleft between the tips of A W/R analytical motion picture projector the lower incisors. In animals with intact lips, was used to analyse mandibular movements the middle of the lower lip was used for all and plot orbits from frontal and lateral views. frames except the one or two at maximum As the teeth were incompletely and variably gape when the cleft between the incisal tips exposed throughout the orbit, even in animals was again used. For lateral views, the point with segments of the lower lip removed, it where the anterior aspect of the chin meets proved necessary to use different reference the lower border of the jaw was the landmark. points for different portions of the orbit. Rela- Actual displacements were measured from a FEEDING IN GOLDEN HAMSTERS 433 ANTERIOR- POSTERIOR- BUCCAL

I Ic I

Mandibular molars

b\C BUCCAL 1

U 1 mm Fig. 4 Camera lucida drawings of the occlusal surfaces of the right molar dentition from a young albino rat fRatfusnoruegicus albinvs). bc, buccalcusp; cc, central cusp; lc, lingualcuspa. The broken line connects the cen- tral cusp with the respective foam into which it lies when the teeth are in occlusion. millimeter scale photographed at the start of sented in comparison to published data for each session. Vertical, horizontal, and pro- laboratory rats (Weijs, '73, '75; Weijs and palinal components of motion were plotted as Dantuma, '751, with emphasis upon differ- displacements, velocities, and accelerations. ences between them. Movement analysis first determined individ- The molar cusps of hamsters show a tribo- ual orbital patterns, then sequential patterns sphenic pattern. The cusps are named accord- of masticatory orbits and patterns of reversal ing to the system of Osborn (cf. Kraus et al., in direction and side preferences. '69; Romer, '70) in which the major cusps are Electromyograms were analysed for the designated by the suffixes -cone, or -conid, and start and stop of muscle activity and changes the minor cusps by the suffixes -conule, -style, in relative firing amplitude. Twenty sets of or -stylid. The terminology of Weijs ('75) is fol- electromyograms were analysed in detail with lowed for rat molars. good simultaneous cine. Further information The molars of hamsters resemble each other was gained from other sequences of electro- much more closely than do other molars char- myograms without cine by cross correlation acterized as tribosphenic (cf. Myotis; Kallen with one or more muscles recorded previously and Gans, '72). All molars have four conical from simultaneous records. major cusps, which show no marked antero- RESULTS posterior slant, and one minor cusp. An addi- tional minor cusp is present on the first molar. Anatomy The major cusps lie on the lingual and buccal The morphology of golden hamsters is pre- borders of the molars with the lingual cusps 434 GERARD C. CORNIAK situated anterior to their corresponding buc- cal cusps (see fig. 3 for the cuspal arrangement of the molars and their interdigitating pat- / tern). In contrast, the unworn molars of young rats (about 3 months old) show low transverse ridges extending across the occlusal surfaces. These flattened grinding surfaces face poste- riorly on the upper molars and anteriorly on the lowers. In general, the maxillary molars exhibit a central, buccal, and lingual row of cusps in the long axis of the tooth-row and the mandibular a buccal and lingual row (fig. 4). The transverse ridges of the lower cusps are depressed centrally and form a trough that provides an anteroposterior guide for the cen- tral cusps of the maxillary molars. The upper and lower tooth-rows of hamsters and rats are isognathous. When the tips of the lower incisors are pressed together, the lin- gual and buccal borders of the respective molars are approximated in hamsters. In rats, the buccal borders of the mandibular molars are lateral with respect to the maxillary. In B both rodents, the maxillary tooth-rows slant Fig. 5 Diagrammatic ventral view of the skull of a ham- ster (A)and an albino rat (B).In both, the mandible has outward from midline and the mandibular in- been removedin boto. The stippled areas show the extent of ward, but the degree of slanting is greater in the mandibular fossae. See text. hamsters. Thus, the occlusal planes of ham- sters incline further inward from horizontal than in rats. In occlusion, the lower incisors of hamsters Although the incisors are longer in rats, lie on midline, with the tips nearly abutting they are nearly the same length in both the lingual base of the upper incisors. The con- rodents in relation to mandibular length. The dyles lie in a single transverse plane, each in robust lower incisors of hamsters curve up- the posterior portion of the mandibular fossa ward more sharply than those of rats and the and midway between its medial and lateral respective tips of the upper and lower teeth lie bony boundaries. nearly parallel in hamsters. The worn poste- When the teeth of rats are occluded, the rior incisal surfaces of rats are flat, but they mandibular buccal and lingual molar cusps lie are concave in hamsters. From the front, the anterior to their corresponding maxillary cutting edges of the incisors are flat and dis- cusps. The central cusps of the maxillary tinctly chisel-shaped in hamsters, whereas molars fit inside the borders of the buccal and those of rats are tapered and rounded. lingual mandibular cusps (fig. 4). The tips of Full occlusion in hamsters shows the cusps the lower incisors are spread apart and well of the upper and lower molars tightly inter- posterior to the lingual base of the uppers. locked. The major mandibular cusps fit ante- Each condyle in rats lies in the posteromedial rior (medial) to their corresponding cusps of portion of its mandibular fossa. the maxillary molars (fig. 3). The major bucco- Mandibular manipulations of hamsters re- mesial cusps of the second and third lower veal that the easiest way to unlock molar oc- molars articulate over the minor cusps of the clusion is by twisting the jaw about a vertical second and third upper. In turn, the bucco-dis- axis so that one condyle slides forward and the tal cusps of the first and second maxillary other backward. On the side of forward condy- molars override the minor cusps of the second lar excursion, the mandibular cusps move me- and third mandibular molars. The paired sio-lingually, while those on the opposite side minor cusps of the first lower molars lie ante- move disto-buccally. Thus, the lower incisors rior to those of the upper first molars. shift laterally from the midline to the side of FEEDING IN GOLDEN HAMSTERS 435

TABLE 1

Motions induced

Muscles Antero- Vertical Lateral posterior Origin Insertion displacement translation translation

Lateral pterygoid Lateral surface of lateral Medial side of condylar Open Lingual Protrusion pterygoid plate maxilla neck, joint capsule, and posteromedial to the articular disc third upper molar Medial pterygoid Lateral surface of medial Fossa on medial side of Close Lingual Protrusion pterygoid plate, ptery- angular process, forms goid fosea, medial wall muscular sling with of lateral pterygoid superficial masseter date Diagistric Anterior belly Rostral end of posterior Ventromedial border of Open Lingual Retrusion belly via a raphe the body of the mandi- ble as far as symphysis Posterior belly Paroccipital process Caudal end of anterior Open Lingual Retrusion belly via a raphe

Masseter Superficial head Anterosuperior to first Ventral and lateral sur- Close Lingual Protrusion maxillary molar, lat- faces of angular proc- eral aspect of zygoma ess, ventromedial body inferior to medial pterygoid insertion Deep head Lateral border of zygoma, Superior surface of angu- Close Lingual Protrusion orbital portion of max- lar process, masseteric illa, anterosuperior to ridge infraorbital foramen between maxillary and premaxillary suture Zygomaticomandularis Infraorbital head Maxilla anterior to infra- Joins the deep rostra1 Close Lingual Protrusion orbital foramen fibers of anterior head to insert on mandibular ramus Anterior head Medial aspect of zygoma Anterolateral border of Close Lingual Protrusion ramus of the mandible superior to insertion of deep masaeter

Posterior head Posteromedial border of Ventrolateral surface of Close Lingual Retrusion zygomatic arch condylar process of mandible, separated from anterior head by masseteric nerve Temporalis Anterior head Mid.sagitta1 crest, occip- Rostral and anteromedial Close Buccal Retrusion ital ridge, lateral and surface of ramus of anterolateral surface of mandible cranial wall, forms pos- terior boundary of orbit Posterior head Sagittal and lamboid Superior and lateral as- Close Buccal Retrusion crest, squamosa of tem- pect of coronoid process poral bone Deep head Lateral cranial wall deep Medial surface of mro- Close Buccal Retrusion to posterior head noid process Suprazygomatic head Rostral surface of zygo- Lateral aspect of coronoid Close Buccal Retrusion matic process of tempo- process directly below ral bone insertion of posterior head 436 GERARD C. GORNIAK dible. This movement terminates when the mesial borders of the first lower molars lie about half a molar length anterior to the mesial borders of their upper counterparts, and the condyles lie in the anterior portion of the mandibular fossae. In rats, a gnawing po- sition is obtained by an anterior and inferior movement, with the lower jaw first moved an- teriorly. The first mandibular molars of rats lie entirely rostral to the first maxillary molars. The skull of adult hamsters is shorter and stouter than that of adult rats. In hamsters, the zygomatic arch curves sharply outward, extending further laterally from the mandibu- .MPt lar fossa than does that of rats (fig. 5). From the side, the zygoma of hamsters are straight and high on the skull. In hamsters, the distal end of the mandible curves upward more sharply than that of rats, and the mandibular ramus is narrower and the masseteric ridge less pronounced. In both rodents, the rostral tips of the lower jaws are joined by a plate of fibrous connective tissue, which permits flexibility at the symphysis menti (cf. Scapino, '65, for Canis ). The man- 1 crn dibular ramus of hamsters diverges well later- t I al to the lower molar tooth-row, whereas the Fig. 6 M. auratus. Diagrammatic ventral relation- ramus of rats is nearly parallel to its molars. ships of the medial (MPt) and lateral (LPt) pterygoid mus- The angular process is prominent in hamsters. cles from camera lucida tracings. The right side of the figure shows a superficial exposure and the left a deeper dis- The inferior border curves sharply inward, section. Only the central portion of the digaatrics have been forming a deep fossa on the medial surface for removed on the left, leaving the bony attachments of the the insertion of the medial pterygoid muscle. anterior (AD) and posterior (PD) bellies intact. The right The coronoid process of hamsters is long, digastric has been removedin toto, as well as the superficial maaaeter (SM)and the left medial pterygoid. The circles slender and curves more caudally than in rats. superimposed are electrode placements. In the anterior di- In both animals, the condyles lie at the same gaetrics only, actual electrode location have been spread out relative distance above the occlusal surface of slightly to show the number of placements more clearly. the upper molar tooth-rows, but those of ham- sters curve inward. As a result, the coronoid backward condylar movement. When the and angular processes of hamsters are rela- teeth are occluded, neither anteroposterior tively more lateral to the condylar head than nor transverse movements occur as the cusps those of rats. interfere. Rotation of the mandibles about their long axes binds the interdigitated cusps Fig. I M. auratus. Diagrammatic lateral view of the and restricts subsequent twisting of the man- muscles of mastication based on camera lucida tracings. A Superficial view shows the maaseter, temporalis, dible about a vertical axis. In contrast, the oc- and posterior digastric muscles. cluded molars of rats permit anteroposterior B The deep maaeeter haa been fully ex@ by re- movement. The central cusps of the maxillary moval of the superficial head. molars pass through the the longitudinal C The divisions of the zygomaticomandibularis muscle are men following the removal of the deep maeseter. trough of the mandibular molars. However, The anterior digastric is also shown. AD, anterior di- the buccal and lingual cusps restrict trans- graatric; AT, anterior temporalis; AZM, anterior zygo- verse movements and rotation about a vertical maticomandibularis; DM, deep masseter; 10, infraorbital axis. portion of the zygomaticomandibularis;MPt, medial ptery. goid, PD, posterior digastric; PT, pterior temporalis; In hamsters, the incisors are brought into a PZM, posterior zygomaticomandibularis; SZT, suprazygo- gnawing position from molar occlusion by a matic temporalis. The circles superimposed are electrode downward and anterior movement of the man- placements. FEEDING IN GOLDEN HAMSTERS 437

A

0

AT AZM

C Figure I +=-+ 438 GERARD C. GORNIAK The mandibular fossae in both rodents (fig. when the condyles lie in the same position, the 5) are bounded medially by the tympanic por- lower molars are two molar lengths forward of tion of the temporal bone and laterally as well the upper, but the position of the incisors is as superiorly by the root of the zygoma; the the same as in hamsters. With the condyles at anterior and posterior ends are free of bony the posterior limits of the fossae, the mandib- boundaries. In hamsters, the posteromedial ular molars of hamsters lie one-half molar walls of the fossae are nearly parallel to each length back on the corresponding maxillary other and the base of the skull, but the antero- molars, whereas in rats there is a full one medial walls slant inward and upward. Later- molar shift. Therefore, the potential range of ally, the main bony restriction to condylar anteroposterior mandibular excursion appears movement is formed by the zygoma, which greater in rats than hamsters. However, recip- curves sharply outward along the central por- rocal anteroposterior condylar movement (ro- tion of the fossa. Only low bony ridges extend tation about a vertical axis) is obtained more rostrally and caudally. The width of the ante- readily in hamsters than in rats. In hamsters rior portion of the fossa is three-fifths of its with the teeth in occlusion or the mandible entire length, while the posterior portion is lowered, the condyle on one side is easily two-fifths of that length. The long axes of the moved to the anterior limit of the fossa and deepest parts of the fossae slant anteromedi- the other condyle to its posterior limit. On the ally. In rats, the medial and lateral bony side of the anterior condyle, the molars shift boundaries are nearly straight and parallel to horizontally to lie near the midline of the each other with the anterolateral boundary skull, a distance of one and one-half their more massive than that of hamsters. The long molar width. In rats, reciprocal anteroposte- axes of the rat fossae are nearly parallel and rior condylar movement to the limits of the show a slight upward and inward inclination fossae is obtained only when the tips of the anteriorly. The entire fossa is nearly twice as lower incisors are separated and ventral to long as it is wide. those of the upper incisors. In both rodents, In hamsters, the capsule of the temporo- rotation about their long axes moves the lower mandibular joint loosely encompasses the en- molars less than half a molar width across the tire mandibular fossa. Only two major capsu- uppers. lar ligaments are seen in an otherwise thin The gross configuration of the masticatory capsule. A stout posterolateral ligament ex- muscles in hamsters (table 1;figs. 6-8) closely tends from the posterior end of the zygomatic resembles that in rats (Weijs, '75). process of the temporal bone and slants ros- The lateral pterygoid (fig. 6) in hamsters trally to the caudolateral border of the condy- arises from the entire lateral surface of the lar neck. The other ligament is narrow and ex- lateral pterygoid plate, and it appears that the tends anteromedially from the rostral border fibers of the lateral and medial pterygoids in- of the (posterior) zygomatic root to the cline less anteriorly in hamsters than in rats. anteromedial aspect of the condyle. Laterally, In hamsters,the long axes of the anterior di- the joint capsule appears to be fused with the gastrics diverge more and the posterior digas- investing fascia of the posterior zygomatico- trics diverge less abruptly than those in rats. mandibularis muscle and medially with the Hamsters do not show an anterior medial divi- fascia of the lateral pterygoid muscle. The ar- sion of the temporalis; instead, the entire an- ticular disc is the same size and shape as the terior portion of the temporalis has a common mandibular fossa, but it is thinner centrally tendon of insertion (fig. 8). However, the pos- than peripherally and thickest at the poste- terior portion of the temporalis of hamsters rior margin. may be subdivided into three parts: (1) a pos- Passive manipulations of the mandible of terior head similar to that in rats, (2) a deep dead and anesthetized hamsters reveal a potential for anteroposterior motion, rotation Fig. 8 M. auratus. Diagrammatic lateral view of the temporalis muscle baaed on camera lucida tracings. about a vertical axis, and rotation of each A Superficial view shows the anterior temporalis mandibular body about its long axis. With (AT). both condyles lying at the anterior limit of B The posterior temporalis (PT)and suprazygo- their fossae, the mandibular molars are nearly matic temporalis (SZT) as exposed by roetral displacement of the anterior temporalis (AT). one and one-half molar lengths forward of the C The deep temporalis (DT) is seen upon removal of anterior limit of the maxillary molars, and the the posterior and suprazygomaticheads. The circlen super- lower incisors are rostral to the uppers. In rats imposed are electrotrode placements. FEEDING IN GOLDEN HAMSTERS 439 AT

A

C

Figure 8 I 1 em I 440 GERARD C. GORNIAK posterior head which insets on the medial ing is observed with the head in a more aspect of the coronoid process, and (3) a very horizontal position. Furthermore, side to side small suprazygomatic temporal head, which is movements of the mandible occur between adjacent medially to the posterior zygomati- bites, shifting the contact point between the comandibularis muscle and inserts on the lat- lower incisors and pellet. eral surface of the coronoid process. With sunflower seeds, hamsters first re- Lateral x-rays of hamsters, with the molars move the shell by crushing it between the in- in occlusion (fig. 9A), show that the condyles cisors. The upper incisors serve as a buttress lie in the posterior portion of the mandibular against one side of the shell while the lower in- fossa with the anterior half of the condylar cisors press upward against the opposing sur- head medial to the root of the zygomatic arch. face. Seeds are more frequently rotated (to The tip of the lower incisor nearly touches the change the point of impact) than are pellets, roof of the mouth; a 4-mm portion of the tooth but head turning is less frequent with seeds. is posterior to the lingual surface of the upper Portions of the shell are pried away with the incisor. As the jaw opens by 25" (fig. 9B; the incisors and pushed from the mouth by the angle measured between the occlusal surfaces tongue. Partially consumed seeds show that of molar tooth-rows), the condyle shifts slight- only part of the kernel is incised. This incised ly anteriorly, and the symphysis moves surface is smooth and nearly flat as opposed to caudally. The tip of the lower incisor is nearly the rough and irregular surface left on pellets in the same frontal plane as that of the upper after gnawing. incisor. The vertical distances between the oc- The distinct pouching behavior of hamsters clusal surfaces of the upper and lower molar differs with the size of the food object. When a tooth-rows are 3 mm anteriorly and 1mm pos- large solid mass of food, such as a whole pellet, teriorly, with no marked anteroposterior shift is pouched, the head is held vertically and of the lower tooth-row. At maximum gape (fig. moves anteroventrally towards the pellet. As W; 45" of opening measured as before), the it nears the food, the mouth opens rapidly, po- condyle lies in the anterior portion of the man- sitioning the lower incisors nearly at a right dibular fossa. The lower incisor and symphysis angle to the uppers, and the head turns to a are almost at a right angle to the upper in- more horizontal position. The mouth is then cisors and retruded more than in figure 9B. pushed over the pellet, and the food is picked The vertical separations of the upper and up by the incisors and grasped between the lower tooth-rows are 11 mm anteriorly and 5 forepaws. Hamsters then use their forepaws to mm posteriorly, with the lower tooth-row maneuver the pellet to one side of the mouth lying posteriorly by about half the length of which will be referred to here as the pouching the first upper molar. side. Concurrently, the mandible swings later- ally away from the pellet and the pouching Feeding behavior side. As the pellet is moved further into the mouth, the top of the head leans towards the When feeding on commercial hamster pel- pouching side, and the forepaws twist the lets and sunflower seeds, hamsters fix these pellet about its long axis. Gradually, the head foods with their incisors and forepaws during moves forward and then downward, so that gnawing. The pellet is a grainy texture, but of the mouth is over the pellet. The head con- the kernel of the seed is soft and covered by a tinues to move in this direction, even after the hard shell. Consequently, gnawing behavior food is completely within the mouth, but the differs between pellet and seed. forepaws are now rubbed backwards along the Gnawing begins with the upper and lower outside of the pouch, and the tongue moves in incisors in contact with the food. Pieces of food a bucco-posterior direction along its internal

are freed from the surface of pellets by short, ~ rapid, scraping or chipping movements of the Fig. 9 M. auratus. Lateral radiographs of head. The lower incisors. The accompanying jaw move- condyles are indicated by arrows. A Mouth closed. The occlusal relationships are ments involve opening protrusion and closing clear for the molars and incisors. Remnants of two elec- retrusion. The head is held down and the pellet trodes are shown; one in the anterior digastric (bottom)and is rotated by the forepaws and incisors to the other in the temporalis muscle (top). change the point of incisal impact. Feeding be- B Mouth open at 25'. The condyle has shifted only slightly forward. havior is somewhat different when the pellet C Mouth open at 45'. The condyle is well forward in is mechanically fixed, preventing food rota- the fossa. Notice the change in the position of the lower in- tion. Head turning is more frequent and gnaw- cisors in reference to the uppers when the mouth is opened. FEEDING IN GOLDEN HAMSTERS 441

Figure 9 442 GERARD C. GORNIAK surface. Together, these movements of the view, a slight posterior and downward shift oc- head, forepaws, and tongue push the pellet curs during the initial lateral-opening move- posteriorly into the cheek pouch. ment. In contrast, hamsters pouching sunflower Hamsters chew both foods at rates between seeds (one-tenththe size of pellets) seldom use four and six orbits per second. Reversal in their forepaws. The head is initially held ver- orbital direction occurs smoothly after one to tically and moved anteriorly and downward three successive orbits and involves a reversal towards the seeds. As it approaches the food, of lateral movement when the mouth is closed. the tips of the lower incisors are just below About 10%of all orbits lack a marked lateral those of the uppers. Seeds are then gathered component. Such orbits occur randomly and up by use of the incisors and tongue, and vary in their vertical displacement. Hamsters pouched whole, in series, to one side of the do not seem to show a side preference, nor do mouth. This transfer of seeds appears to cine records alone supply direct information involve a repeated posterolateral movement of about an active side. Furthermore, the lower the tongue, maneuvering the seeds from the incisor tips remain together during chewing of incisors to the pouching side. Although the both food types; no spreading was observed. head moves from side to side as well as for- Successive orbits do not follow identical ward and backward, it moves less when pouch- paths in frontal view (fig. 13). Their differ- ing seeds than for pellets, and least during ences are most obvious during the opening mastication. stroke. However, these changes (in frontal The path, described by the anterior tip of view) did not consistently relate to changes the mandible as it moves from a midline closed obtained in lateral views of the masticatory position, through one opening stroke, and back orbits. through one closing stroke, is referred to as a Data suitable for analysis of the displace- chewing orbit. This (fig. 10) indicates lateral ment, velocity and acceleration curves are as well as vertical and anteroposterior move- presently available only for chewing. ments of the mandible. Orbital direction re- The vertical displacement graphs (figs. 14, fers to lateral direction taken by the mandible 15) are derived from frontal views of orbits for across the top of the orbit. seeds and pellets. The graphs peak more In frontal view, a typical chewing orbit for sharply at the bottom of the opening stroke pellets (fig. 11A) starts with a lateral shift to than at the top when the mouth is closed. This one side, after which a vertical movement difference is even more evident for pellets begins. Next, the jaw opens sharply and, dur- when the top of the graph tends to plateau. ing the downstroke reverses horizontally to- Amplitudes of peak vertical displacement are wards midline. At the wide-open position, the greater and more consistent with sunflower jaw is just slightly to one side or the other of seeds. midline. The closing stroke (upstroke) pro- Opening and closing vertical velocities for ceeds near the midline and generally starts each food (figs. 14, 15) show nearly identical with a slight lateral shift in either direction. peak amplitudes, although the measured Lateral views (fig. 11B) indicate a strong pro- peaks are greater for seeds. Peak opening palinal component of masticatory motion. velocity is reached before peak opening dis- However, there appears to be no significant placement, and peak closing velocity is at- anteroposterior movement as the jaw moves tained rapidly about midway through the up- laterally from midline at the top of the orbit. stroke. Closing velocity then decreases grad- During opening, the orbit curves posteriorly; ually as the jaw continues to close. The rapid the rate of its caudal displacement is small at change from peak opening to peak closing the start but then increases sharply during velocity is more clearly documented in the the lower half of the downstroke. In contrast, acceleration graphs. Peak closing accelera- the closing stroke follows a relatively straight Fig. 10 M. auratus. Frames 101-108 of film showing upward and anterior path. both frontal and lateral views of the eighth orbit in a masti- When sunflower seeds are masticated, the catory sequence. An anterior segment of the lower lip is re- chewing orbit is similar in frontal view. How- moved, exposing the base of the lower incisor. Reproduction ever, lateral excursion from midline at the top from the original color film has resulted in a 1086 of resolu- tion. Lateral translation during the downstroke and mid- of the orbit is typically accompanied by slight line closure, however, are seen in frontal view. In lateral opening (fig. 12). Otherwise, orbits for sun- view, the tip of the chin displays a reversing posterior and flower seeds are the same as for pellets. In side anterior path respectively during opening and closing. FEEDING IN GOLDEN HAMSTERS 443

Figure 10 444 GERARD C. GORNIAK CLOSE CLOSE

8 26 ANTERIOR 1 50-54

A B C 12 A 2 00 60 OPEN OPEN i Fig. 11 M.auratus. Typical orbit of hamster chewing Fig. 13 M. auratus. Sequential frontal orbita of ham- on pellet. Small arrows indicate the upstroke; in A, the ster chewing on pellet. The sequence proceeds in order from arrow is on midline. Numbers correspond to the respective A to C. The arrows indicate the upstroke and midline; num- film frames. bers correspond to film frames. These sequential orbita A Frontal view showing transverae displacement. show typical variations in orbital path. The upstroke is essentially on midline. B Simultaneous lateral view showing the pro- palinal component of motion. tion passes through zero (i.e., becomes a clos- ing deceleration) and peaks, very abruptly in the case of seeds, but then diminishes towards zero as occlusion is approached. CLOSE Graphs of horizontal jaw displacement for seeds are regularly cyclic (fig. 14), whereas graphs for pellets (fig. 15) indicate irregular regions of small and large displacements. In both cases, the horizontal displacements of in- dividual orbits exhibit the previously de- scribed pattern of lateral movements. In gen- eral, velocity and acceleration graphs for both foods peak in one direction near occlusion and then in the other during the downstroke. These peak amplitudes are somewhat greater for seeds; however,they are considerably less for both foods than are those of vertical. Propalinal and vertical displacements (fig. OPEN 16) are mapped from a lateral cine view. The Fig. 12 M. auratus. Sequentialorbita of mastication propalinal graphs show marked anteroposte- of a hamster chewing on a kernel of sunflower seed. The rior shifts accompanying the upstroke and sequence proceeda in order from A to C. The small arrows downstroke. Graphs of vertical displacement, indicate the upstroke and midline; numbers correspond to the respective film frames. Orbits B and C show reversal of velocity, and acceleration closely resemble orbital direction. those derived from frontal views. Fig. 14 M. auratuu. Mastication of seed. Graphs of tions are generally three times peak opening displacement, velocity, and acceleration plotted from a serieu of masticatory orbitu, resolved into vertical and Both ‘losing and Opening horizontal components for the mean movement at the tip of accelerations are greater for seeds than for the mandible (w recorded at 38 fm.). The arrows indicate pellets. Opening accelerations peak near the the direction of lateral and vertikl movements. R, desig bottom o&-third of the downs&ke and then nates lateral translation to the right; L, to the left. Each orbit shows reversals in orbital direction. Note particularly decrease rapidly; ,.losing acceleration peaks the smooth transition from closing to opening on the verti- when the mandible changes direction. When cal displacement curver and shifts in acceleration during the jaw is about half closed, closing accelera- the orbit. FEEDING IN GOLDEN HAMSTERS 445

152 W v)-

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FRAME "'""'"''"""'25 30 35 40 45 '"" 50 NUMBER

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38- Acceleration mm/sec2

c 38- LL WJ 76-

4 I (3- 3s a 38- 0 Velocity 4 A

Figure 14 446 GERARD C. GORNIAK

Propalinal acceleration graphs show that thirds of the way through the opening stroke. peak amplitudes in the anterior direction are During most of the upstroke, inconsistent low- generally twice those of peak posterior accel- level activities of both muscles are seen. eration. Peak acceleration and velocity in the Toward the end of closure, these muscles may posterior direction correspond well with the stop firing, or when the orbit continues to the sharp increase in posterior displacement dur- right, the ipsilateral lateral pterygoid may ing the lower half of the downstroke. Peak an- simply continue to fire, increasing in ampli- terior acceleration is reached at the start of tude as lateral translation at the top of the the upstroke as expected, as the teeth nearing orbit begins. occlusion will be affected by the energy the The anterior digastrics also act asymmetri- mandible then imparts to the food being cally (figs. 17A,E). The ipsilateral anterior di- reduced. gastric starts to fire when the jaw begins to Electromyography shift laterally at the top of the orbit. Both anterior digastrics fire in concert at the start It is clear that hamsters have an active and of the downstroke. The contralateral anterior passive side during chewing, though they may digastric then shows an increase in amplitude chew simultaneously on both sides about 10% as lateral translation (left) returns to mid- of the time. This asymmetry was determined line; the amplitude of the ipsilateral digastric only after analyses of the data. However, to remains unchanged. During the downstroke, clarify the subsequent description of the elec- the two anterior digastrics become inactive at tromyographic activity which accompanies nearly the same time, concurrent with the end jaw movements, I refer to the active side as ip- of activity in the contralateral lateral ptery- silateral and the passive side as contralateral. goid. I also adopt the convention of describing only clockwise orbits in which the orbital direction The posterior digastrics fire symmetrically and the passive side are on the right and the and start later than their corresponding ante- active side is on the left. rior digastrics. This lag in the start of poste- The major muscle groups are generally rior digastric activity between the ipsilateral active symmetrically during the closing anterior and posterior digastrics is more stroke of mastication. They fire asymmet- noticeable than between the contralateral rically during lateral translation when the muscles. The posterior digastrics become mouth is closed and during opening. Electro- active at the start of the downstroke and stop myograms are correlated with masticatory firing simultaneously with the anterior di- movement during typical orbits, reversing as gastrics. the orbital direction reverses (see fig. 17 for The posterior and deep heads of the tempo- electromyographic sequences accompanying ralis muscle on the same side fire nearly in these reversals). concert (fig. 17B). Bilaterally, however, these The lateral pterygoids typically fire asym- muscles are active asymmetrically (fig. 17C). metrically (fig. 17A, for a right orbit; a left Lateral translation to the right at the start of orbit shows a mirror image). With the mouth the upstroke is accompanied by initial firing closed, the start of lateral movement (right) is on the right side, although the left side be- accompanied by strong activity from the ip- comes active shortly thereafter. The posterior silateral lateral pterygoid. Activity, if any, is and deep heads of the temporalis continue to very weak from the contralateral muscle. fire bilaterally until the upstroke ends. Activ- Near the end of this lateral translation, ities from the ipsilateral muscles then stop horizontal acceleration decreases concurrent while the contralaterals continue to fire dur- with the initiation of strong firing from the ing lateral translation (right) at the top of the contralateral lateral pterygoid; the amplitude from the ipsilateral muscle decreases (i.e., Fig. 15 M. ouratus. Mastication of pellet. Grapha of displacement, velocity, and acceleration plotted from a weaker than that on the right). Both lateral series of masticatory orbits, resolved into vertical and pterygoids are active at the start of the down- horizontal components for the mean movement at the tip of stroke. However, as the jaw begins its return the mandible (an recorded at 35 fps.). The arrows indicate toward midline, (i.e., to the left) the contralat- the direction of lateral and vertical movements. R, big- nates lateral translation to the right; L, to the left. The era1 muscle continues to fire strongly but ac- third and fourth orbits show reversals in orbital direction. tivity ends from the ipsilateral pterygoid. The In contrast to figure 14, notice the plateauing of the verti- contralateral muscle stops firing about two- cal displacement graph. FEEDING IN GOLDEN HAMSTERS 447

mm/stc'

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Figure 15 440 GERARD C. GORNIAK orbit. Contralateral heads stop firing as the ing the upstroke and the digastrics only dur- jaw begins its downward motion. ing the downstroke, but the lateral pterygoids The anterior temporales (fig. 17D) are are active during both strokes. Only the super- usually active symmetrically. Only occasion- ficial masseters fire asymmetrically. The ally are they active asymmetrically, and then superficial masseter on one side still shows they fire in concert with asymmetric activity stronger relative amplitudes during the up- from their respective posterior temporalis. stroke. In contrast, the deep masseters and ap- Symmetrical activities from the anterior tem- parently zygomaticomandibulares fire sym- porales coincide with the upstroke and ordi- metrically. narily continue into lateral translation at the Some electromyograms from animals dur- top of the orbit. Both sides become silent when ing gnawing are available (fig. 18). Gnawing the downstroke begins. behavior involved a scraping or chipping The medial pterygoids (figs. 17E, 18A) begin motion of the lower incisors. The adductor to fire at the start of the upstroke. Firing is muscles are noticeably less active when these symmetrical when the upstroke proceeds animals are gnawing, whereas the anterior along the midline. However, numerous records and posterior digastrics as well as the lateral show asymmetric activity at the start of clos- pterygoids fire more strongly and for longer ing. A short lead in activity on the left side ac- periods of time. Electromyograms are also companies lateral translation to the right. available from the temporalis, masseter and During the rest of the upstroke, the muscles medial pterygoid muscles when hamsters are on both sides fire in concert. At the top of the biting kernels of sunflower seeds. These rec- orbit, continued activity from only the ipsilat- ords suggest that the adductors fire strongly era1 medial pterygoid accompanies lateral ex- (as during chewing) when hamsters bite. cursion to the right. Neither of the medial pterygoids is active during the downstroke. DISCUSSION The superficial masseters (fig. 17F,G) fire Feeding behavior asymmetrically. The ipsilateral muscle begins Rodents chew in distinct ways (cf. Woods, to fire at the start of closing while the contra- ’76; for the patterns used by hystricomorphine lateral side starts at a low level a short time rodents). In rats (Weijs, ’75) and “textbook” later. Although both muscles are active dur- rodents (Peyer, ‘68; Turnbull, ’70), only a sim- ing the rest of the upstroke, the ipsilateral ple anteroposterior motion accompanies open- superficial masseter fires more strongly ing and closing. However, hamsters exhibit a throughout the closing stroke even in those marked lateral movement, coupled with this orbits which lack significant lateral transla- strong propalinal translation. tion. The ipsilateral muscle continues to fire The interlocking molar cusps of hamsters strongly during lateral excursion at the top of restrict protrusive, retrusive and true trans- the orbit, but contralateral superficial masse- verse movements. Manipulations show that a ter activity ends. twisting movement in the horizontal plane The deep masseters (fig. 17D,G) begin to will unlock this occlusion. Thus, lateral trans- fire at the start of the closing stroke. Firing is lation observed at the top of the orbit appar- symmetrical during the upstroke and into lat- ently results from rotation of the mandible eral translation at the top of the orbit, regard- about a vertical axis, possibly through the less of orbital direction. Consequently, the ip- condyle (cf. de Vree and Gans, ‘76, for goat). silateral superficial and deep masseters fire in The inward slant and roomy mediolateral ex- concert (fig. 17G), but activity from the con- tent of the mandibular fossae suggest that tralateral deep masseter starts earlier and such rotation must be accompanied by a pro- ends later than that of the contralateral su- trusive and medial condylar movement on the perficial masseter. Both deep and superficial opposite side. masseters are silent during the downstroke. Lateral translation observed at the top of The few electromyograms available from the anterior zygomaticomandibularis muscle Fig. 16 M. ouratus. Mastication of pellet. Graphs of show that it fires at the same time as the deep displacement, velocity, and acceleration plotted from a masseter. seriee of masticatory orbits, resolved into vertical and pro- palinal components for the mean movement at the tip of the In chewing orbits without marked lateral mandible (an recorded at 36 fps.). The arrows indicate the translation, bilateral records are generally direction of antempterior and vertical movement. P. pos- symmetrical. Adductor muscles fire only dur- terior; A, anterior; 0, open; C, close. FEEDING IN GOLDEN HAMSTERS 449

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Figure 16 450 GERARD C. GORNIAK the orbit merits emphasis. First, when the ments involve (1) an anteroposterior sliding molars are near occlusion, the lower incisors, movement between the articular disc and the which are parallel and slightly posterior to the mandibular fossa, and (2) a rotational motion upper incisors, cross the midline. This incisal about a transverse axis between the mandibu- position would restrict the kind of protrusive lar condyle and the articular disc. movement described in albino rats (Weijs, '75) The upstroke in hamsters tends to be on as the incisors would be brought into contact. midline. Lateral movements at the start However, the position of the incisors permits rotation of the mandible about a vertical axis Fig. 17 M. auratua. Representative electromyograms recorded during chewing. Each record shows simultaneous or a nearly straight vertical opening move- activity from four muscles. All traces proceed in time from ment along the midline. When comparison is left to right. One-second markers (T) indicate the time base made to a vertical scissor-like motion, rota- for all traces. The first letter of each muscle label indicates tion about a vertical axis imposes additional it is right (R) or left (L). Frame markers (FRM) allowed cor- relation between masticatory events and electromyograph- shearing forces upon the food. Thus, lateral ic activities. Orbital direction refers to the direction of lat- translation appears to increase trituration. eral translation at the top of the orbit. Secondly, hamsters store food in their cheek A Activities from both anterior digastrics (AD) pouches. Lateral movements may be advanta- and lateral pterygoids (Lpt). The sequence begins with right orbital direction. The arrows, here and elsewhere, geous during this process as buccal move- indicate reversals in orbital direction disclosed by simulta- ments of the teeth might assist them in neous cinematography. All four muscles are active at the maneuvering food towards a cheek pouch. start of opening. The slight lead shown by the right lateral Furthermore, lingual movements may help pterygoid at the end of the first burst of firing accompanies lateral translation to the left during the downstroke. return food from the pouch to the oral cavity. B Activities from the deep masseter (DM), and an- Hamsters can also pouch impressively large terior (AT) posterior (PT)and deep (DT) heads of the tem- foods. However, a midline position of the lower poralis on the same side. The posterior and deep heada of the incisors partially blocks the entry of large temporalis essentially fire symmetrically. The anterior head, however, fires more nearly in concert with the deep solid food objects, such as whole pellets. A lat- masseter. eral shift of these teeth would enlarge this en- C Activities from both posterior temporales (PT), trance, permitting larger food items to be unilateral deep masseter (DM) and medial pterygoid (Mpt). stored. With small foods, such as sunflower The posterior temporales usually fire asymmetrically. The lead shown by these closing retrusora accompanies lateral seeds, a lateral incisal movement appears to excursion to that side. Symmetric activities from the deep be less advantageous during pouching. But, a masseter and posterior temporalis of the same side produce rapid lateral thrust produced by these teeth a rotational force couple which swings the mandible up may help propel small food items from be- ward. The reduced activities shown for the medial pterygoid result from insufficient signal amplification as numerous tween the incisors towards a cheek pouch. other electromyographic traces of this muscle exhibit When lateral rotation at the top of the orbit amplitudes comparable to those seen in other closing mus- ends to the right of midline, the left condyle is cles. protruded with respect to the right. During D Activities from bilateral deep masseters (DM) and anterior temporales (AT). Deep masseter activities are the subsequent downstroke the mandible re- symmetrical. Symmetric activities from the deep maaseters turns to midline, suggesting that the right and anterior temporales produce a unilateral force couple condyle moves forward for a greater distance on both sides during closure. than the left. However, at the start of the E Activities from both medial pterygoida (Mpt) and anterior digastrics (AD). This record shows medial downstroke, the tip of the jaw shows only pterygoid activities to be symmetrical, although numerous slight posterior and lateral movement, which records also show asymmetric activities accompanying lat- suggests that the condyles are initially eral translation. Bilateral anterior digastric activities show rotated about a transverse condylar axis in asymmetry. The leads shown by these opening retrusors correspond to transverse movement across the top of the order to clear the incisors. The mandible then orbit. moves toward midline and posteriorly, which F Activities from anterior (AT) and posterior (PT) increases the vertical distance between the temporales on the same side and both superficial masseters molars and permits food to be placed more (SM). Stronger firing amplitudes shown from the tem- poralis and opposite superficial masseter (first arrow) ac- readily between the teeth. Therefore, condylar company orbital direction to the right, a bilateral force cou- movements during the downstroke appear to ple. involve an initial bilateral rotation about a G Activities from the superficial (SM) and deep transverse axis, which is then followed by (DM) masseters, medial pterygoid (Mpt) and anterior di- gastric (AD) all of the same side. Stronger amplitudes marked bilateral but asymmetric condylar shown from the superficial masseter and medial pterygoid protrusion. Examination of the temporoman- accompany orbits to the right. Deep masseter activities dis- dibular joint suggests that these gross move- play a consistent amplitude regardless of orbital direction. FEEDING IN GOLDEN HAMSTERS 45 1

Figure 17 452 GERARD C. GORNIAK apparently are final adjustments which align rodents grow throughout life (Peyer, ‘681,and the isognathic teeth on both sides of the jaws. this continual growth requires constant wear Food reduction occurring at the end of the up- (and constant sharpening) in order for the ani- stroke may involve both crushing of food mal to survive. It has been suggested that the wedged between the molar cusps (compression lower incisors are sharpened by movements forces) and shearing forces generated as the across the labial surfaces of the uppers, and lower molars move forward during closure. that the uppers are sharpened by normal wear Different food types affect the chewing pat- during ingestion (Hiiemae and Ardran, ’68). tern. Graphs of displacement resolved in verti- In hamsters, the labial surfaces of the incisors cal and horizontal components show dif- are covered by enamel and the lingual sur- ferences between mastication of soft sunflow- faces by cementum (Keys and Dale, ‘44). er seed kernels and hard laboratory pellets. Hence, only the lingual surfaces of the in- The most noticeable difference is observed cisors wear. Condylar manipulations suggest when the mouth is closed. Consequently, foods that the lingual surfaces of the lower incisors of different textures apparently have a great- may be sharpened by moving them across the er effect on masticatory movements during enamel surfaces (labial) of the uppers. How- the period of actual trituration than they do ever, it is difficult to believe that the during the rest of the orbit. In addition, these hollowed-out wear pattern of the upper inci- differences suggest that trituration of rela- sors results during ingestion. Rather, it ap- tively soft foods involves primarily shearing pears more plausible that the upper incisors forces, and hard foods are broken down by a are sharpened by movement of the lower teeth combination of compressive and shearing across their lingual surfaces. Therefore, tooth- forces. sharpening seems to involve a consistently Different foods also affect the movement changing labial and then lingual movement of patterns involved in pouching and gnawing. the lower incisors. However, it was not record- In pouching, the size of the food appears to be ed during these experiments. critical. Pouching behavior is different for large pellets than for small sunflower seeds. Electromyograp hy These changes in the movement pattern in- Electromyograms recorded from mastica- volve the degree of mouth opening, use of the tory muscles of hamsters are in good agree- forepaw and incisors, and the amount of head ment with the motion analysis and show both movement. As for gnawing, jaw movement ap- symmetric and asymmetric activity patterns pears to differ with the texture of the food. as well as a silent period at the end of the Hiiemae and Ardran (‘68)describe “biting” downstroke (fig. 19). Activities from the deep and “true gnawing” in rats as two separate masseters, anterior temporales, anterior zygo- processes, depending upon the food type. Thus, maticomandibulares and posterior digastrics it might be preferable to differentiate be- are usually bilaterally symmetrical. As in rats tween biting and gnawing among rodents. Bit- (Weijs and Dantuma, ’75), these symmetric ing involves a straight closure of the mouth. As the tips of the lower incisors approach Fig. 18 M. auratus. Representative electromyograms those of the uppers, the food object is cut recorded during first chewing and then gnawing of a pellet. Each chewing and gnawing record shows simultaneous ac- between them. However, gnawing involves tivities from the same animal. The top three recorda are scraping or chipping movements of the lower continuow; the bottom one was recorded on the ~ameday incisors along food objects stabilized by the but in different sessions at the same amplification.One-aec- uppers. Both processes would appear benefi- ond markers CT) indicate the time baee for all traces. The Fist letter of each muncle label designates it as right G) or cial in rodents with omnivorous diets, such as left (1). Frame markers are shown (FRM). Electromyo- hamsters and rats. Biting movements may be graphic records A, B, C, show reduced amplitude from the used on soft plant material and the fleshy food adductor muscles during gnawing. of a vertebrate carcass. In the latter case, both A Activities from both medial pterygoide CMpt) upper and lower incisors could cut deeply into and anterior digastrics (AD). B Activities from unilateral posterior temporalis the meat, which could then be torn away by (PT) and medial pterygoid (Mpt) and both anterior di- head and body movements. A gnawing motion gastrics (AD). may be more useful for shaving hard, solid C Activities from bilateral anterior digastrice plant material and scraping remnants of meat (AD) and unilateral superficial masseter (9M) and lateral pterygoid (Lpt). from bones. D Activities from both anterior digastrice (AD) An additional comment on the incisors and lateral pterygoida (Lpt). All four muscles show an in- seems appropriate here. The incisors of crease in duration of activity during gnawing. FEEDING IN GOLDEN HAMSTERS 453

P) a m iE 454 GERARD C. GORNIAK

FRONTAL VIEW

R. Sup. Moarotor

1. Sup. Marrotor

LATERAL VIEW LATERAL VIEW

1. (I 1. Cost. Digortri

1.. 1. hop Marrokr, Ant. lomporolir ond

R. Mod. horygoid &

Fig. 19 Diagram summarizing a typical sequence of jaw muscle activities for continuing masticatory orbits in the same direction. In frontal view (center),lateral translation at the top of the orbit is right; the downstroke shows a lateral component of motion to the left. The upatroke begins to the left of midline but then proceeds ini- tially to the right to close on midline. In lateral view, propalinal movements are shown during the upstroke (viewers right) and the downstroke (viewers left).

activities tend to move the jaw along the mid- silateral (left) lateral pterygoid would pro- line. However, the other muscles studied duce a protrusive and medial force, rotating usually fire asymmetrically during a typical the jaw to the right (as described in bats, chewing orbit. Asymmetric activities accom- Kallen and Gans, '72); retrusive forces gen- pany lateral movements at the top of the orbit, erated by the ipsilateral anterior digastric during the downstroke, and at the start of the would appear to counteract this condylar pro- upstroke. trusion. However, the anterior digastric in- Electromyograms indicate that the lateral serts on the ventral limit of the mandible, translation at the top of the orbit is produced which is well medial of the condyle. As a re- by a bilateral force couple which pits closing sult, a medial retrusive force applied at the tip retrusors (deep and posterior temporales) on of the mandible may rotate it about an axis the contralateral side against closing protru- passing vertically through the condyle. This sors (superficial masseter and medial ptery- condylar rotation, acting together with the goid) on the ipsilateral side. In concert with protrusive and medial forces induced from the these closing muscles, the ipsilateral anterior lateral pterygoid on the same condyle, may digastric and lateral pterygoid muscles fire then generate lateral translations in the oppo- before the contralateral, producing a unilater- site direction. al force couple which accompanies lateral ex- As the downstroke begins, the anterior di- cursion to the contralateral side. One might gastrics and lateral pterygoids are bilaterally expect, for example, that activity from the ip- active. The anterior digastrics apparently FEEDING IN GOLDEN HAMSTERS 455 generate a retrusive force ventral to the con- During gnawing, electromyographic activi- dyles and the lateral pterygoids a protrusive ties show a marked reduction in activity of force at the condyles. Together, these forces closing protrusors and retrusors. This reduc- allow the incisors to clear by a rotation of the tion of adductor activity differs from that de- mandible about a transverse axis, which pass- scribed in rats during biting (Weijs and Dan- es through both condyles. As opening pro- tuma, '75). Thus, it appears that biting and ceeds, activity ends initially in the ipsilateral gnawing are two mechanically different proc- lateral pterygoid; the contralateral lateral esses at least among rodents, and that the pterygoid continues to fire. This continued ac- scraping and chipping movements during tivity from the contralateral side apparently gnawing require less of a closing force than generates an unbalanced protrusive force on those of a bite. that side returning the mandible to midline. Thus, it appears that the jaw is translated lat- Trituration erally during the downstroke by unilateral ac- Most studies on mammalian mastication re- tivity from the lateral pterygoid and that the fer to an active chewing side (Ardran et al., mouth is opened by the pull of the digastrics, '58; Becht, '53; Crompton and Hiiemae, '68; de acting ventral to the instant center of rota- Vree and Gans, '76; Kallen and Gans, '72; tion. Smith and Savage, '59). However, the pres- Even though the jaws move in a downward ence andlor absence of an active side is still an and posterior direction through the bottom open question for animals with isognathic one-fourth of the opening stroke, all the ob- dentitions, such as hamsters. Hiiemae and vious masticatory muscles studied are silent. Ardran ('68) note that rats had food simulta- It might be possible that this motion is a prod- neously between the molars of both sides as uct of momentum and gravity. However, in well as on one side only, suggesting to them rats (Weijs and Dantuma, '751, miniature pigs that rats occasionally exhibit an active side (Herring and Scapino, '73), and Virginian while chewing otherwise occurs bilaterally. opossums (Crompton et al., '771, the supra- On the other hand, Weijs ('75) only noted a bi- hyoid muscles are very active at the end of lateral reduction of food in rats. Herring and opening. These muscles may also help to gen- Scapino ('73) report that electromyography of erate the final phase of the opening movement the masseter suggests a "dominant side" in in hamsters. miniature pigs and note that this dominance In hamsters, the upstroke is along the mid- is not necessarily an indicator of an active line with all the adductor muscles taking part side. They suggest that chewing may be bilat- in this motion. A unilateral force couple on eral and involve a more efficient breakdown of both sides is produced by closing protrusors, food on one side than the other. However, their which act vertical to the condyle, and closing results are uncertain because they were un- retrusors acting dorsal to it. This combination able to tell at any instant the side on which moves the mandibular tip dorsally along mid- the animal was chewing. line as in rats (Weijs and Dantuma, '75). As The present study suggests that hamsters the jaw is moved laterally at the top of the have an active chewing side. Even though the orbit, bilaterally symmetric activities from main axis of the closing stroke is vertical as in the deep masseters and anterior temporales cats, cats definitely reduce food on only one continue to produce a closing force. This force side at a time (Gorniak, '77). Thus, a midline is apparently responsible for maintaining the closing stroke does not necessarily mean that teeth in contact with the food and continuing the animal chews bilaterally. efficient reduction. Although hamsters have the potential for Therefore, chewing in hamsters involves a bilateral food reduction, this process would lateral translation superimposed over a sim- not appear to be for very efficient. Lateral ex- ple rotational force couple. Lateral move- cursion at the top of the orbit always moves ments are generated by asymmetric activities, the mandibular molars buccally on one side generally pitting protrusors on one side and lingually on the opposite side. If reduction against retrusors on the opposite side. Sym- were to occur bilaterally, food lying on the side metric vertical protrusive and dorsal retru- of buccal movement would then be pushed to- sive forces from the adductors then produce a wards a cheek pouch. While this food might be pair of unilateral force couples, which rotate pouched, cine films show no indication that the jaw on midline during the upstroke. hamsters store food between chewing orbits. 456 GERARD C. GORNIAK

It would seem that an active chewing side excursion. Sherrington's classical study might be more efficient, but only if it was on showed that stimulation of the periodontal the side in which the molars move lingually at structures produces rapid mouth opening, fol- the top of the stroke. Most triturated food may lowed immediately by closing; the antag- then be deposited directly into the oral cavity, onistic muscles reciprocally inhibited. Conse- decreasing the time and energy otherwise quently, lateral translation across the top of needed to retrieve food pushed bucally be- the orbit may involve reciprocal inhibition, tween the teeth and cheek pouch. triggered by pressure on the periodontal struc- Data suggest not only that hamsters have tures as the teeth contact the food. Differen- an active and passive side, but also that an tial outputs from periodontal receptors may active side might be typical of trituration. In explain the differences observed in mastica- orbits with and without significant lateral tory movement at the top of the orbit when a translation, the superficial masseter muscle particular animal chews foods varying in con- consistently fires more strongly on one side sistency (de Vree and Gans, '76). than the other during midline closure. As food 2. Masticatory orbits of -hamsters reverse resists closing, this strong activity from the after one to three cycles. These reversals may superficial masseter suggests that trituration relate to the jaw-opening reflex, which can be in hamsters is concentrated on that side. Fur- triggered by stimulation of the periodontal thermore, the majority of orbits observed in structures (Sherrington, '17; Hannam and hamsters show lateral translation. Similar Matthews, '69) and influenced by higher corti- lateral components of motion occur in bats cal levels (Kawamura, '67;Chase and McGin- (Kallen and Gans, '72), rabbits (Ardran et al., ty, '70). Thus, changes in pressures on the pe- '58) and ungulates (Beckt, '57;de Vree and riodontal structures, produced by changes in Gans, '76;Smith and Savage, '59).In all these vertical resistance to food, might be inte- species, lateral excursion at the top of the grated at higher nervous levels and might con- orbit proceeds from the active to the passive tribute to triggering of a reversal in orbital side. This excursion pattern suggests that direction. The same concept may be used to ex- hamsters typically have an active side which plain changes observed in masticatory move- is opposite the direction of lateral translation ment when the same animal chews different at the top of the orbit and during which food is food types (de Vree and Gans, '76). Foods of deposited into the oral cavity by lingual move- hard consistency, such as pellets, probably ment of the mandibular molars and strong ac- produce more resistence to breakdown than tivity recorded from the superficial masseter. the softer kernel and would tend to generate greater pressure on the periodontal structures Control of mastication during trituration. In turn, this periodontal It was not the purpose of this study to exam- input may facilitate responses at a higher cor- ine the nervous control of mastication. How- tical level to maintain tooth-to-food contact, ever, the results permit comments regarding explaining the nearly horizontal path followed several aspects of nervous activity. by the mandible at the top of the orbit. On the 1. Sherrington ('17) and Kawamura et al. other hand, the softer kernel would offer less ('60) documented reciprocal inhibition be- resistance and induces less pressure on the pe- tween antagonistic muscles for opening ver- riodontal structures. The absence of closing sus closing activity, a concept that also ap- signals may allow the mouth to open slightly, plies to the mastication of hamsters. Kallen as observed during lateral translation. and Gans ('72, in little brown bats) extended 3. Karamura et al. ('67) suggest that mech- the concept of reciprocal inhibition to include anoreceptors in the temporomandibular joint lateral translation during chewing. The pres- regulate biting strength. Kallen and Gans ent study provides additional evidence in sup- ('72) further suggests that these receptors port of this latter concept. serve an important protective function. Be- In hamsters, lateral translation across the cause the mandibular fossae of hamsters are top of the orbit starts with the tip of the man- free of anterior and posterior bony limits, this dible on midline. Although the respective latter suggestion leads to the prediction that muscles on both sides would be stretched the mechanoreceptors of rodents must be high- equally in this starting position, asymmetric ly concentrated along the anterior and posteri- activities from protrusors on one side and or limits of the joint. Furthermore, an anterior retrusors on the other accompany this lateral concentration of receptors might also regulate FEEDING IN GOLDEN HAMSTERS 457 the maximum size of food hamsters are capa- attach directly to the hyoid apparatus. Conse- ble of storing in their cheek pouches. quently, the anterior digastrics are mechani- 4. The length of the incisors in rodents cally capable of moving the mandible, inde- must be continually monitored in order to pendent of the posterior digastrics. adjust sharpening rate to compensate for Hiiemae and Ardran ('68) describe both an growth minus wear. X-rays and prepared active side and bilateral chewing in rats, specimens of hamsters show that the lower in- whereas Weijs and Dantuma ('75) refer only cisors nearly abut the floor of the palate when to bilateral chewing. However, the latter the mouth is fully closed. Possibly, both authors did mention that they observed some lingual and palatal touch receptors monitor asymmetric activity, but these were not such length and influence the sharpening pat- analysed. Furthermore, they show electro- tern. myograms from the superficial masseters Comparison which resemble those recorded from the same Hamsters chew differently than rats. Both muscle in hamsters. Perhaps such asymmetric rodents may utilize the same food types, and activities are in the nature of a fine control mechanism which maintains a vertical chew- both have essentially the same general mus- ing stroke when the consistency or amount of cular configuration as well as a characteristic food differs between the left and right tooth- temporomandibular joint. However, the occlu- rows. This activity may, in fact, support the sal surfaces of the molars are very different in suggestion of Hiiemae and Ardran that these two myomorph rodents (figs. 3, 41, and ('68) rats chew occasionally on only one side (active each reflects a particular masticatory move- ment. Thus, as suggested by Kallen and Gans side). ('721, the occlusal pattern of the dentition has Of the literature available on mammalian a greater influence on that aspect of mastica- mastication, only a small proportion involves tory movement when reduction takes place the reduction of foods of varying consistencies Luschei and Goodwin, than do the corresponding muscles, joints, or (de Vree and Gans, '76; '74). These studies and the present one show bony elements which are often used to define that a noticeable change in the chewing orbit chewing motion. occurs with different foods when the jaws are Both rats (Weijs and Dantruma, '75) and in closest approximation. hamsters show symmetric muscular activities This study then confirms that rodents use accompanying symmetrical movements of different masticatory orbits, even when their both sides of the mandible during closing. In diets and anatomy are superficially similar. hamsters and bats (Kallen and Gans, '721, Some species may exhibit strong propalinal asymmetric muscular activities occur during movements without significant lateral trans- the clearly asymmetric lateral translation. lation. However, other species, such as ham- However, asymmetric activity from the super- sters, may show a prominent lateral compo- ficial masseter of hamsters demonstrates that nent of motion upon essentially the same, asymmetric activity may be seen accompany- strong propalinal movement. Furthermore, ing a seemingly symmetric motion. Further- the present study notes the possible advan- more, it emphasizes that the resistance tage of lateral translatory movement in an against which an element is traveling should animal which stores food in cheek pouches. be considered. For instance, although car- Additional studies, specifically on pouching nivores are purported to exhibit a scissors-like and mastication in other animals which pouch masticatory movement (Smith and Savage, foods, such as squirrels or old world monkeys, '59; Turnbull, '70), asymmetric muscle activ- should increase our outer base of information ity might be observed during closing when the for drawing conclusions regarding the evolu- vertical resistance imparted by the food is tionary development of mammalian mastica- much greater between the carnassials of one tion systems. side than those of the other (such as dogs chewing on bones). ACKNOWLEDGMENTS In contrast to rats (Weijs and Dantuma, I am indebted to Professors Frank C. Kallen '75) and little brown bats (Kallen and Gans, and Carl Gans for their advice and assistance '721, the anterior and posterior digastrics of during this study. I also wish to thank Doctors hamsters do not fire in concert. The connec- Beverly Bishop, Harold Brody, E. Russell tive tissues between the origin of the anterior Hayes. Norman D. Mohl, H. I. Rosenberg, and and the insertion of the posterior digastrics Frances M. Sansone for their helpful com- 458 GERARD C. GORNIAK ments. Illustrations were prepared by Rose- in response to stimulation of periodontal mechanorecep- ann Hebeler and Don Luce. This project was tors in the cat. Archs. Oral Biol., 14: 415-419. Herring, S. W., and R. P. Scapino 1973 Physiology of feed- supported by the Graduate Resources De- ing in miniature pigs. J. Morph., 141: 427-460. velopment Project, SUNYAB Graduate Stu- Hiiemae, K. M. 1967 Masticatory function in the mam- dent Assoc., as well as The Department of mals. J. Dent. Res.. 46 (Suppl. to No. 5): 883-893. Anatomical Sciences, SUNY at Buffalo, and Hiiemae, K., and G. M. Ardran 1968 A cinefluorographic study of mandibular movement during feeding in the rat NSF Grant BMS 71 01380. (Rattus noruegicusl. J. Zool. 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