Archs oral Biol. Vol. 30, No. 7, pp. 539-544, 1985 0003-9969/85 $3.00 + 0.00 Printed in Great Britain. All rights reserved Copyright 0 1985 Pergamon Press Ltd

MECHANISM OF INTRA-ORAL TRANSPORT IN A HERBIVORE, THE HYRAX (PROCA U/l SYRIACUS)

H. A. FRANKS,’ R. Z. GERMAN,’ A. W. CROMPTON*

and K. M. HIIEMAE~

‘School of Dental Medicine, Washington University, 4559 Scott Avenue, St Louis, MO 63110, *Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138 and ‘Department of Oral Anatomy,

University of Illinois at Chicago, Health Sciences Center, Chicago, IL 60637, U.S.A.

Summary-Movements in the jaw, tongue and hyoid during feeding behaviour were recorded with tine-X-ray. Food was moved through the mouth by anterior/posterior motion of the tongue surface relative to the hard palate. This was true for both stage I transport, from the front of the mouth to the molar tooth row and stage II transport, from the molar tooth row to the vallecular area of the oropharynx. During a series of chew cycles, processed food collected in the oropharynx prior to a swallow. Swallows occurred as discrete events punctuating chew sequences and were characterized by coordinated movements of tongue and soft palate. Similar mechanisms of transport have been observed in the opossum and the cat, indicating a common mammalian behaviour. Differences between this herbivore and anthropoid primates can be attributed to differences in anatomy of the oral apparatus.

INTRODUCTION

Although the anatomy of mammalian-feeding struc- tures is similar, differences have evolved in masti- catory strategies. Studies have focused mainly on the morphology of the jaws and teeth and their functions in the breakdown of food. Little attention has been given to the more fundamental aspect of feeding behaviour; for instance, the mechanism by which food is moved through the mouth and into the gut (Gans, DeVree and Gorniak, 1978; Hiiemae, Thexton and Crompton, 1978).

The tongue, in conjunction with the hard and soft palates, is primarily responsible for food transport in primates as shown by Abd-El-Malek (1955) and Miller (1982) for m,an and Franks, German and Crompton (1984) for macaques. In non-primates, descriptions exist for the bat (DeGueldre and DeVree, 1984) the pig (Herring, 1976), the goat (DeVree and Gans, 1’375), the rabbit (Ardran, Kemp and Ride, 1958), the rat (Weijs and Dantuma, 1975) and the cat (Thexton, 1981). Descriptions of cyclic jaw movements exist for several mammals (Hiiemae, 1978; Gans et al., 1978). However, the information reported does not document the temporal aspects of coordination of tongue movements with those of the jaw.

Hyraxes are small, tractable herbivores. They were chosen for comparison with opossums, tenrecs and cats. They have jaw musculature considered similar to the primitive condition of ungulates, and their cranial anatomy is unspecialized (Janis, 1983). Data on hyrax food transport are important for compara- tive studies because they could partially test the hypothesis that there is a common pattern of masti- cation and food transport (defined broadly to include tongue/jaw coordination and the mechanism of food transport) in mammals. That hypothesis can be tested only by examining animals which are phylo- genetically distinct and whose dietary habits differ.

MATERIALS AND METHODS

Seven hyraxes (Procaviu syriacus) were trained to feed in plexiglass boxes. Screws of approx. 1 mm diameter were inserted in the jaw, and amalgam fillings were put into molars while the animals were anaesthetized with halothane or a mixture of halo- thane and nitrous oxide. Two small metal markers were inserted into the tongue with a large-bore hypodermic syringe. These markers in the middle and the posterior third of the tongue were used to trace the movement of these parts of the tongue. Surgical thread was used to attach a metal marker to the hyoid under direct vision and general anaesthesia. After allowing 24 h or longer for recovery, 16mm cine- X-ray films were taken in lateral projection (100 exposures/s) while the animals fed in the plexiglass box.

Animals were usually fed carrot and apple, al- though lettuce, dried fruit and parsley were also used as food items. Some food items were injected or coated with barium to render them radio-opaque. Over 90 (100 ft) films were obtained and analysed. Films were analysed frame-by-frame using a Van- guard Motion analyser. Acetate overlays were used to trace successive frames of film from selected cycles in order to elucidate the mechanism of intra-oral food transport. Cycles with bariumized food were used because the position and movement of food in the mouth and the pharynx could be documented. These results were compared with cycles with non-barium- ized food to ensure that the presence of barium did not elicit atypical behaviour. Although the animals preferred non-bariumized food, movements of tht jaw, tongue and hyoid were not different for the types of food.

Cycles from three animals were further analysed to examine the constancy of behaviour between ex- periments and among different animals. Positions of metal markers relative to the hard palate were deter-

539

540 H. A. FRANKS et al.

laryngeal musculature

trachea (lumen)

Fig. 1. Bisected hyrax head.

mined for each frame of film by digitizing these points with a Vanguard Motion analyser in combination with a Graf/Pen Sonic digitizer and an Apple II computer. J. McGarrick wrote the programs for this analysis; they are available from us.

In general, the behaviour among different animals and/or different trials of the same animal was con- sistent. The behaviour was seen in all animals; the illustrations are representative of all that behaviour.

Anatomy RESULTS

Three major anatomical structures are involved in mastication: the tongue, the hyoid and the jaw (Fig. 1). Two parts of the tongue were considered: middle tongue, which lies under the hard palate along the length of the premolar and molar tooth row; posterior tongue, which lies under the soft palate posterior to the crista terminalis. Food transport, defined as movement of food through three anat- omical areas: (1) the mouth, extending from the lips to the tongue flexure; (2) the oropharynx, a space ventral to the soft palate, anterior of the epiglottis and dorsal to the posterior tongue surface; (3) the area behind the epiglottis and soft palate where the laryngeal pharynx meets the oropharynx and the nasopharynx. This third space existed as a compart- ment briefly as part of the process of swallowing. The oropharynx was separated from the remainder of the pharynx by the soft palate/epiglottal seal. Food transport through each of these areas was considered separately: Stage I transport, movement of food from the front of the mouth to the region of the cheek teeth or through the mouth to the front of the oropharynx; Stage II transport, movement of food from the region of the cheek teeth to the back of the oropharynx; and swallowing, movement of the bolus from the oro- pharynx to the oesophagus (Hiiemae et al., 1978).

Overview of hyrax mastication

Hyraxes, when habituated to the experimental setting in which data were collected, appeared to feed in the same manner as they did when they were in their more usual caged situation. When small items such as cubed or sliced carrot were presented, hyraxes took them either through the front or the side of the mouth. If items too large for intra-oral manipulation were taken, a part was sliced off with the cheek teeth and that portion retained in the mouth and the remainder dropped. The animals never used their caniniform incisors for food-processing. These teeth

were occasionally used, however. to bite the hand that fed them. Janis (1983) provides a detailed and comprehensive description of hyrax feeding behav- iour.

The literature on mastication has used the term masticatory sequence to describe all cycles from point of ingestion of a single bite until that food is clear of the mouth (reviewed by Hiiemae and Crompton, 1984). In these discussions, a sequence refers to the analysed portion of the series of chews and swallows stimulated by ingestion of a single piece of food. After a food item of suitable size had been ingested, a long series of chew cycles began. Single food items stimulated 20, 30, or more chewing cycles. Food began to collect in the oropharynx a few cycles after it reached the cheek teeth. Until late in the sequence, bariumized food was seen along the premolar/molar tooth row, on the tongue dorsum posterior to the cheek teeth and in the oropharynx. Food appeared to move back progressively with each cycle. So long as food remained in the mouth, the process continued.

Basic movement of jaw, hyoid and tongue

The movements of the major oropharyngeal struc- tures were cyclic. These cycles are divisible into two distinct phases: first, opening (for the jaw) or forward (for the tongue and hyoid) and second, a closing (jaw) or backward (tongue and hyoid) phase.

The two phases of the jaw cycle, jaw open and jaw close, are shown in Fig. 2. The open and close phases have been subdivided on the basis of various criteria (Gans et al., 1978; Hiiemae, 1978). These divisions are more relevant to descriptions of food processing than to intra-oral food transport; therefore we treat open and close as a single phase for our present purposes.

Hyoid movement in chewing cycles was biphasic (Fig. 2). The first phase, referred to as hyoid pro- traction, was a period of upward and anterior move- ment of the tongue base. Upward and forward move- ment began synchronously with the start of jaw opening. The second phase, hyoid return, was the reverse movement. During this phase, the hyoid initially moved down and back. When the jaw started to close, the hyoid often moved a slight distance forward but maintained a ventral position until the start of the next protraction phase (Fig. 2).

The middle and posterior regions of the tongue had a cycle of movement that was also divided into two phases. The first of these was forward movement of the tongue base, tongue protraction, and the second, tongue return, was the backwards movement. The protraction phase for both regions began at the same time as jaw opening and consisted mainly of anterior movement. The return phase of the posterior tongue consisted entirely of backwards movement. The re- turn phase of the middle tongue marker was more complex because it was affected by jaw movement in that jaw displacement introduced a vertical com- ponent to the movement. The functionally-important movement was posterior. There may have been some lateral movement, but this study does not include data to evaluate such movement.

This study introduces a new convention for cycle division to describe movement and is justified because this approach facilitates the study of coordination of

Intra-oral transport in a herbivore 541

JAW

HYOID ANTERIOR/POSTERIOR

HYOID UP/DOWN \

POSTERIOR TONGUE ANTERIOR/POSTERIOR

\

MID TONGUE ANTERIOR/POSTERIOR

A

n Fig. 2. Biphasic divisions Iof mastication cycles. A jaw cycle begins and ends at minimL.m gape. Jaw movement is divided into a jaw open and a jaw-close phase. Tongue and hyoid cycles begin at the same time as the start of the jaw cycle. The tongue and hyoid cyc:les are divided into a protraction and a return phase. Regions of the tongue also exhibit two phase cycles of activity: regional longitudinal expansion and

contraction.

movement among jaw, tongue and hyoid. The start of jaw opening, the beginning of upwards and for- wards phase of movement in middle and posterior tongue markers, were synchronous in each cycle. No such coordination occurred at any other point in the gape cycle. Maximum gape was not synchronous with the start of any backwards movement of any tongue or hyoid marker. Minimum gape was used as the start of a cycle. This convention also makes the divisions of cyclic movement of hyoid and tongue markers obvious; a (clear forward or protraction phase was followed by a backward or return phase. The terms hyoid protraction, hyoid return, tongue protraction and tongue return describe the two phases of cyclic movement in these structures.

Mechanism of stage I transport in the hyrax

The hyrax used coordinated jaw and tongue move- ments to transport food from the front of the mouth to the region of the cheek teeth (Figs 3 and 4). During the protraction phase as the tongue and hyoid moved forward, the food was held in place by the palatal ridges on the roof of the mouth. The tongue, lubri- cated with saliva, moved forward below the station- ary food. This movement caused more posterior regions of the tongue lo come into contact with food. Anterior movement of the tongue markers during

the protraction phase was in part due to upwards and forwards movement of the hyoid during the protraction phase and, in addition, to intrinsic longi- tudinal expansion of both the middle and posterior regions of the tongue as measured by the changing distance between markers.

During the return phase, the surface of the tongue was lowered so that food on the dorsal surface was no longer in contact with the palatal ridges above. At the same time, the hyoid moved down and the middle and posterior regions of the tongue contracted. Com- bined hyoid retraction and intrinsic tongue con- traction pulled the tongue surface posteriorly in the mouth moving the food posteriorly.

Mechanism of stage II transport in the hyrax

Stage II transport, the movement of food from the premolar/molar region to the oropharynx, was simi- lar to that of stage I transport. At the start of stage II transport (Figs 5 and 6) food on the dorsal surface of the tongue extended from the mouth into the oropharynx. The food within the oropharynx was sufficiently processed for swallowing but that in the

Fig. 3. Stage I transport. The hyrax was moving food from the front of the mouth to the cheek teeth. Numbers repre- sent the frame number in the cycle. The interval between successive frames was approx. 10 ms. Position of the hyoid and tongue markers for the frame is represented by a dark circle. Position of the markers for the previously-illustrated frame is an open circle. During the protraction phase (the first two tracings), the tongue moves forward under the relatively stationary food represented by the dark rectangle. During the return phase, the tongue is pulled posteriorly in the mouth and the food item is moved in that direction (bottom). Movement of the food in the mouth can be seen by comparing food position relative to the arrow in the

illustrated frames.

542 H. A. FRANKS et al.

l-J HYOID 1%

Fig. 4. Orbits of movement for tongue and hyoid markers for stage I transport cycle. During protraction phase (dotted line), the markers move forward. During the return phase, they move back. Frames shown in Fig. 3 are circled and

numbered.

Fig. 5. Stage II transport. In this cycle, the hyrax moves food from the cheek teeth to the oropharynx. Conventions the same as thost in Fig. 3. The heavy broken lines represents the soft palate. Position of the food in each frame is shaded area. When food is moved between frames, its position in the previous frame is shown as a light dotted line.

mouth was still in the process of being broken down. During the protraction phase, both tongue markers and the hyoid moved up and forward bringing the posterior tongue dorsum into contact with the soft palate/hard palate junction to form a mouth/ oropharynx seal. The probable contraction of the paiatoglossal muscles and the raising of the tongue prevented anterior displacement of the food. Slight forward movement did occur but not as part of transport.

At the beginning of the tongue/hyoid return phase, a depression formed in the centre of the tongue surface. This depression and the food, seen lying below the surface of the tongue in Fig. 5.5, began moving posteriorly; the start of jaw closing followed. Throughout the jaw-closing phase, tonguelhyoid return continued with further movement of food into the oropharynx. As the bolus formed, it was stored in the valleculae, a region at the back of the oro- pharynx. At the end of the cycle, the posterior tongue was positioned downwards and backwards relative to the palate, so that upwards and forwards movement in the next protraction phase added more food to the bolus that was collecting behind the tongue flexure.

Food transport with swallowing

When a swallow occurred, it began at the end of the previous chew-transport cycle, after a bolus had collected in the oropharynx from stage II transport (Figs 7 and 8). At the start of the swallow, the leading edge of the food held in the oropharynx began to move around the epiglottis at the same time as the soft palate began to elevate. It is probable that posterior movement of the back of the tongue (be- tween the posterior marker and the hyoid) created

MIDDLE TONGUE

FORWARD

Fig. 6. Stage II orbits of movement. Conventions the same as those in Fig. 4.

Intra-oral transport in a herbivore 543

At the beginning of the tongue/hyoid protraction phase of the swallow cycle, the middle tongue marker and the hyoid moved up and forward as they did in chew cycles with stage II transport but the posterior tongue marker moved up without moving forward. The reduction of anterior movement at this time in a swallow cycle reflects continued posterior movement of the tongue dorsum in the region behind the posterior tongue marker. The changed shape of the bolus showed that the tongue, in conjunction with activity of the pharyngeal constrictors, was con- tinuing to force the bolus towards the oesophagus. As the bolus continued to move down and back into the oesophagus, the tongue markers remained almost stationary. The continued movement of the bolus through the posterior region of the oropharynx was, therefore, largely the result of activity of the pharyn- geal constrictors. As the entire bolus moved into the oesophagus, the hyoid moved posteriorly. The hyoid movement reflected activity of the region of the tongue that is directly attached to the hyoid which assisted in pushing food into the oesophagus. After the bolus moved into the oesophagus, the soft palate re-established contact with the epiglottis sealing off the oesophagus.

Fig. 7. A series of tracings depicting the swallow cycle. Each cycle starts with frame number one. Frame 21-29 are from the cycle prior to swallowing. Frames numbered 5-34 are from the next cycle during which swallowing occurs. Con-

ventions the same as Figs 3 and 5. At this point, typical tongue and hyoid protrac-

PRE-SWALLOW CHEW CYCLE

pressure on the bolus stored in the valleculae pushing the food in a posterior direction. As the leading edge of the stored bolus moved further down and back, the tongue markers and the hyoid remained stationary though the region between the hyoid and the posterior tongue marker changed in shape. The concavity, in which the food was held, smoothed out so that the bolus moved posteriorly.

SWALLOW CYCLE

_~~~

FORWARD MIDDLE TONGUE

I-l

POSTERIOR TONGUE

HYOID

1z-n

Fig. 8. Orbits o:T movement for the swallow cycle. These orbits are the cycle before and during a swallow illustrated in Fig. 7. Conventions the same as in Figs 4 and 6.

544 H. A. FRANKS ef al

tion, as described here for chew cycles with stage II transport, resumed. The hyoid moved forward, and the posterior one-third of the tongue expanded so that both tongue markers moved forward. The dorsal surface of the tongue moved forward under the food which remained in the mouth, preparatory for stage II transport. The tongue/hyoid return phase of cycles that include a swallow were the same as those in cycles with stage I or II transport.

DISCUSSION

Stage I and II transport are mechanisms for mov- ing food through two distinct anatomical areas. The same cycles of tongue protraction and return, hyoid protraction and return and jaw open and close, was observed in both stage I and II transport. The essential characteristics of food transport in hyraxes was that (1) during a tongue/hyoid protraction phase, food was held more or less stationary in the mouth; and (2) during a period of posterior tongue and hyoid movement, food moved in a posterior direction also. In stage I transport, food was moved to the region of the molar teeth for trituration. Anterior movement was prevented by the rugae of the hard palate. In stage II transport, muscle action probably prevented anterior movement of food and the food was col- lected in a bolus at the back of the oropharynx until a swallow occurred.

No previously published study of swallowing has examined swallowing in the context of the chew cycles that proceed and follow it. Our study demon- strated that a swallow occurred as a discrete event during the protraction phase of a cycle and was what may be called a punctuation of an otherwise typical transport cycle. As the soft palate was lifted, pos- terior movement of the pharyngeal tongue carried the food past the seal between the soft palate and epiglottis and then to the oesophagus.

These mechanisms of food transport are similar to those observed in other non-primate mammals. Opossums use the same mechanism of tongue move- ment relative to the hard palate and rugae in conjunc- tion with jaw opening for stage I transport (J. Weijs-Boot, personal communication). Stage II transport appears essentially the same in hyrax and opossum although further studies of the opossum may reveal some differences. Hiiemae ef al. (1978) documented hyoid movement and food transport in the cat. They suggested that a similar mechanism is responsible for transport although their data are not directly comparable to ours. The movements that they illustrate are, however, almost identical to those of a hyrax for cycles that include food transport.

The similarities in these mechanisms can be traced to a basic common mammalian anatomy of the structures involved in mastication. All these mam- mals have a somewhat long mouth, a hard palate

with pronounced rugae, and a vallecular area in the oropharynx for storing processed food prior to swal- lowing. In contrast, primates, particularly macaques and man, have smooth palates, short mouths and little or no storage area in the oropharynx which precludes the use of the mechanism of intra-oral transport seen in the hyrax (Franks et al., 1984). Without rugae to hold food during a tongue forward phase, the pull-back mechanism is impossible. An animal that cannot store a bolus in the oropharynx swallows more frequently, and swallows may not be only a punctuation of cycles of stage II transport.

Acknowledgements-We thank J. McGarrick, M. Reynolds, D. Sponder, L. Mueller, J. Rosovsky, K. Smith, D. Mc- Cleam, C. Janis, W. Greaves, S. Herring, L. Richter and an anonymous referee. This work was supported by N.I.H. grant DE 05738-04 to A.W.C. and K.M.H.

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