The movement of the cat hyoid during feeding

CW3-9969:81/020065-17502.00/O Pergamon Press Ltd

Archs owl Biol. Vol. 26, pp. 65 lo 81. 1981 Printed m Great Ilritam

THE MOVEMENT OF THE CAT HYOID DURING FEEDING KARENH. H~EMAE’.~, A. THEX~ON’.~, J. MCGARRICK’ and A. W. CROMPTON~ ‘Department of Oral Anatomy, College of Dentistry, University of Illinois at the Medical Center, 801 South Paulina Street, Chicago, IL 60612, U.S.A. *Department of Physiology, Royal Dental Hospital School of Dental Surgery, Cranmer Terrace, London SW17 ORE, England 3Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, U.S.A. Summary-The

hyoid has generally been regarded as a basically static element in the jaw apparatus, moving only in swallowing. A regular patterned hyoid movement directly correlated with jaw movement occurs during feeding on soft food in the American opossum; the present study sought 1:oestablish whether: (i) hyoid movement was always linked to jaw movement and (ii) the pattern of hyoid movement could be correlated with jaw movement cycles associated with (a) transport and (b) chewing of food. Cats were fed foods varying in consistency from liquid (milk) lo hard solids (cooked liver) and cinefluorographic recordings made of complete feeding sequences. The results showed that the hyoid not only moved continuously during feeding but had a generally upwards and forwards movement during early jaw opening (SO phase of jaw movement) and a generally backwards movement during later jaw opening (FO phase). This rl:lationship was associated with movement of food through and within the mouth. In contrast, the hyoid orbit was attentuated and its phase relationship with that of the jaw movement cycle altered in some jaw movement cycles with short SO phases which occurred in the middle of sequences in which hard food was being processed. These changes are associated with a shift from a transport to a non-transport or chew function of the tongue and therefore a change in the behaviour of the hyoid in its base.

able shift in the position of the tongue base and, with it, its oropharyngeal surface. Hiiemae, Thexton and Crompton (1978) demonstrated in the cat that, long before a bolus is formed on the oropharyngeal surface of the tongue in preparation for swallowing, ingested food is moved through the mouth in two stages; first, to bring it to the post-canine area for mastication and, second, to the oropharyngeal surface. This food transport system was shown to depend on a combination of tongue base and tongue surface movements. However, in the absence of a clear definition of tongue and hyoid movement, the behaviour of these structures during feeding has so far only been related experimentally to certain characteristics of jaw movement (Thexton, Hiiemae and Crompton, 1980). Jaw movement cycles have been divided (Hiiemae, 1976; McGarrick and Thexton, 1978; Thexton et al., 1980) into four main phases based on the rate of change of gape during closing and opening: FC (fast close); SC (slow close); SO (slow open) and FO (fast open). Single complete masticatory cycles in the cat have also been classified into two groups: transport and non-transport or chew cycles, depending on whether intra-oral transport of food was visible in cinefluorographs. This categorization into transport and chew cycles correlates with the classification of masticatory cycles on the basis of the relative duration of the SO phase (Thexton et al., 1980). The correlation between the long SO phase of cycles in which transport takes place and the reduction in length of the SO phase in those cycles in which no transport takes place suggests a link between the actual movements of the jaws and the movements of the hyoid.

INTRODUCTION In mammals, the larynx, hyoid and epiglottis are parts of a cartilaginous and bony complex linking the upper end of the airway with the base and oropharyn-

geal surface of the tongue (Plate, Fig. 1A). The uppermost of these elements, the hyoid, is essentially a C-shaped bone suspended from the lower jaw and from the cranium; it is connected to the pectoral girdle by three distinct groups of muscles. In addition, it provides attachment for a major extrinsic muscle of the tongue (hyoglossus), the muscle controlling the position of the floor of the mouth (mylohyoid) and the middle constrictor of the pharynx. It is generally agreed that in man the hyolaryngeal complex is moved upwards in swallowing, the muscles connecting it to the pectoral girdle returning it to its previous position. The hyoicl has also conventionally been regarded as the linking element in the mechanical system opening the jaws. However, until recently, the possibility that the whole hyolaryngeal complex might also move during mastication had been !argely ignored. A synchronous cinefluorographic and electromyographic study of the American opossum showed that the hyoid has a regular movement during feeding on soft food (Crompton, et al., 1977). A pilot study showed cinefluorogr,lphically that comparable hyoid movement occurs during chewing in man (Thexton, Wallace and Ebbs, 1976). In both cases, the hyoid moved upwards and forwards during the early stages of jaw opening. Given the anatomical relationships of the hyoid, such movement must result in a compar0.~.26/2-A

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Karen H. Hiiemae et al.

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When solid food is moved through the mouth towards the oropharynx, the mobile tongue appears to act against the hard palate. This may not be the primary mechanism in the transport of liquids; nevertheless the relationship of the hyoid, as the base of the tongue, to the palate has functional importance. This study was therefore designed to examine two specific but related questions: (a) Given its anatomical relationships, are the movements of the hyoid directly linked to those of the jaw? (b) Is the pattern of hyoid (i.e. tongue base) movement in individual jaw movement cycles consistent with a division of those cycles into the two categories of transport and non-transport or chew cycles? METHODS

Experiments were carried out on 5 adult cats. The animals were fed on the following items: (a) milk with added barium, (b) commercial tinned catfood mixed to a semi-solid consistency with added barium, (c) calf liver. The liver was presented in 6 forms: 3 different consistencies (raw, medium and hard) each given in lumps of 2 different sizes (small and medium). The medium and hard grades of liver were prepared by cooking thick slices in a conventional oven at 204°C (400°F) for 20 and 45 min respectively. The unevenly cooked surface layers were then removed and the slices cut into cubes of mean linear dimension 0.6 and 1.1 cm, i.e. small and medium lumps. The raw liver was frozen and thick slices cut into equivalent-sized cubes which were then allowed to thaw. The mean linear dimensions of the cubes were obtained from scaled photographs of random samples of the foods. Under general anaesthesia, a small ring of platinum wire was attached to the dense fascia overlying the antero-inferior aspect of the body of the hyoid to act as a radio-opaque marker. The position of this marker relative to the body of the hyoid remained the same over a period of months when checked by conventional radiographs. After being trained to feed between the fluoroscope and the tube of an X-ray machine so that the sagittal plane of the animal’s head was, at least initially, perpendicular to a line between the anode of the tube and the fluoroscope, the cats were fluoroscoped at approx. 37 kV and lOOmA and the image recorded on 16 mm cinefilm (Eastman Plus X negative) at camera speeds varying from 30 to 80 frames/s. The film was subsequently displayed using an analysing projector (Specto Mark III). Film not taken in true lateral view was rejected; only about 30 per cent was accepted for analysis. This amounted to several thousand feet of film in which both individual cycles and, less frequently, complete sequences could be analysed. Only data from the latter, amounting to several hundred cycles, are reported here. A tracing was made of each frame of film at approximately actual size, i.e. the cinefilm image was enlarged until the antero-posterior length of the skull and lower jaw corresponded with those from a conventional still radiograph of the animal. Gape and hyoid position were measured on each frame of film. Gape was defined as the angle between (a) the palatal line (pl, Fig. 1B) and (b) the mandibular line (ml, Fig. lB), a line drawn through the mandibular condyle, the contact points of the lower cheek teeth and

the upper margin of the alveolar bone distal to the cervical margin of the lower canine. The position of the hyoid marker was measured in the vertical and horizontal planes with reference to the cranial base and the hyoid reference line (hrl, Fig. 1B). The distance of the marker from the cranial base parallel to the hyoid reference line defined its vertical position (Y coordinate, Text Figs 3 and 4). The horizontal distance of the marker measured from the reference line (forwards +; backwards -) and parallel to the cranial base defined its antero-posterior position (X coordinate, Figs 3 and 4). When the position of the hyoid was plotted, taking the horizontal distance (hh in Fig. 1B) as the X coordinate and the vertical distance (hv in Fig. 1B) as the Y coordinate for each frame of film in each cycle of jaw movement, then the path of movement or orbit of the hyoid during that cycle was obtained (Figs 3 and 4). In all the cats examined, the angle between the palatal line (extended to the cranial base) and the cranial base was in the range 8-9”. For present purposes, these have therefore been regarded as essentially parallel. The numerical data were entered into a computer for plotting and processing (McGarrick and Thexton, 1978). Before detailed statistical analysis could be carried out, it was necessary to simplify the raw data by filtering out minor oscillations and measurement errors. The criteria for filtering were based on two assumptions: first, that any measurement error was randomly distributed; second, based on examination of the graphed raw data, that hyoid movement was essentially rhythmic. As the movement of the hyoid and tongue cannot be wholly disassociated from that of the jaws, the frequency components of hyoid movement of concern in this study were considered to be within the range CL12 Hz, i.e. up to the 2nd harmonic of the fundamental frequency of jaw movement. This range was selected, based on the finding that the periodicity of jaw movement in the cat is, on average, 30@350ms or approx. 3 Hz (Thexton et al., 1980). The hyoid data was therefore filtered by carrying out a Fourier transform, setting the components above 12 Hz to zero and then carrying out the inverse Fourier transform so that the hyoid vertical and horizontal position data were reconstituted with the omission of high-frequency components (Text Fig. 2). Each cycle of jaw movement was defined as starting from the most depressed position of the jaw, i.e. the maximum gape. The jaw movement cycle was then divided into the four phases: fast close (FC), slow close (SC), slow open (SO) and fast open (FO) using methods previously described (McGarrick and Thexton, 1978; Thexton et al., 1980). However, although the low-amplitude cycles of lapping can be similarly divided, the rate changes between the FC and SC phases and between the SO and FO phases are not strictly comparable with those seen in cycles where the animals feed on solid or semi-solid food (Thexton et al., 1980). In fact, the FC phase does not occur as a rapid closing movement in lapping. Similarly, a true rapid opening or FO phase does not follow the SO, slow open, phase. These two components can, nevertheless, be identified as distinct elements in the lapping cycle. Until electromyographic studies clarifying the exact nature of the 4 phases in lapping can be

67

Movements of cat hyoid Time sequence RAW

of hyoid positions

X.Y

Plots

DATA Upward

UPWARD l

.-•.

.

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.

l

.

.

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t

Vertical FORWARD

t

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.

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Horizontal

FILTERED

DATA

Vertical

Horizontal

Forward

-

Fig. 2. The efl’ect of digital filtering (see Methods) on the raw data plotted against time (left) and as an hyoid orbit (right))) When the two filtered data streams were plotted as XY coordinates, the resultant orbit was simpler and less erratic but showed the same general movement pattern as did the raw data.

completed, the current divisions of the cycle, and their acronyms, are retained. In each jaw cycle, the movement of the hyoid was plotted for that cycle and the data analysed. The total distance travelled bf the hyoid (TRV mm) in the sagittal plane was calculated for each cycle and also for each of the 4 phases (FC, SC, SO, FO) within that cycle. As the hyoid travelled along a very curved path (in the sagittal plan(:), a figure was derived for the actual net progress made by the hyoid during each cycle or phase thereof. This progress had a linear dimension (PRG mm) and a direction which was measured clockwise on a 360” scale (ANG) in which dorsal (palatal) was o”, caudal 90”, ventral 180” and rostra1 270” (see Fig. 6). The mean position vertically (MPV) and horizontally (MPH) was calculated for each cycle and for each phase within each cycle. In addition, the most elevated (ME), most depressed (MD), most anterior (MA) and most posterior (MP) positions of the hyoid were obtained for each cycle.

RESULTS

Throughout all feeding sequences, the hyoid continued to move in the vertical plane (towards and away from the palate/cranial base, Fig. 1B) and in the horizontal plane (forwards and backwards in parallel with the palate/cranial base). The actual profile of movement, viewed in the sagittal plane, during each period of jaw movernent, was obtained by using the horizontal and vertical positions of the hyoid as XY coordinates (Figs 3 and 4). Each plot was taken, for convenience, as starting from the position occupied

by the hyoid at the time of the initial maximum gape for that jaw movement cycle and ending at the position the hyoid reached at the time of the terminal maximum gape. To distinguish this hyoid movement path from that of the jaws, it is referred to as an orbit, reflecting the generally loop-like movement involved (Figs 3 and 4). It follows that successive orbits for all cycles in a complete feeding sequence (defined as the period between initial ingestion and final swallowing of a unit of food) represented a continuous path of movement (see Hiiemae et al., 1978, Fig. 7). This is reflected by the open nature of the orbits shown in Figs 3 and 4: the hyoid rarely returned to a position close to that which it occupied at the start of the cycle. Nevertheless, if the direction, rate and amplitude of hyoid movement are to be quantified and correlated with the same parameters of jaw movement during a single jaw cycle, the path of hyoid movement must be considered as a series of discrete, if incomplete, orbits. As can be seen from Figs 3 and 4, the shape of the orbit varied widely from a very narrow ellipse (Fig. 3A) to a complete figure-of-eight (Fig. 4). This variation occurred both within single sequences (Fig. 4B) and also between sequences relating to different types of non-liquid foods. However, during lapping of radio-opaque milk (an activity in which the backwards movement of the liquid from the incisors to the oropharyngeal surface of the tongue appeared almost continuous in cinefluorographs), the hyoid movements in successive cycles were all similar except when swallowing occurred. In lapping, the hyoid orbit had a very much larger amplitude of movement in the horizontal axis than it had in the vertical (Fig. 3A). The orbit was similarly antero-posteriorly elongated

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Karen H. Hiiemae et al.

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Fig. 3A. (see also caption below). Liquid: bariumized milk. Six cycles from a lapping sequence. Cycle 9 includes a swallow which occurs as an upwards and backwards movement of the hyoid (cross-hatched arrows) during the SO phase. The orbits are narrow anteroposteriorly oriented ellipses, the hyoid moving upwards and forwards (black arrows) during the SO and FO phases and downwards and backwards (black line) during the FC and SC phases of jaw movement. Fig. 3. Successive hyoid orbits (as XY coordinate plots) drawn from filtered hyoid position data (see Fig. 2) for successive cycles in specific single sequences. The number of each orbit is shown both at its start point (6, 7, 8 etc.) and at the corners of the XY axes. Not all the cycles in each jaw movement sequence are shown. For clarity, the successive orbits are staggered. The fine dashed line connects the terminal position of the hyoid in one orbit with its starting position in the next. These points are the same, as the jaw movement cycle is taken as beginning at the terminal maximum gape for the previous cycle. See Key for explanation of symbols.

69

Movements of cat hyoid

33. 3. 35. 36. 37.

-37

Fig. 33. (see also caption on facing page). Semisolid: bariumized catfood. The jaw movement cycie has distinct FC and FO phases (see Fig. SB). This is reflected in the change in orbit profile. Hyoid travel continues to he upwards and forwards during the SO phase but downwards or downwards and hackwards during the FO phase. In this case, the bolus was swallowed in the 9th cycle of the sequence. Note that the dimensions of the X and Y axes are not the same in the two cases.

KEY TO FIGS 3 AND 4 LIQUIDS -o-o-o)

FC and SC phase ))

SO and FO phase

SEMISOLID FOODS )m)) DD D

AND SOLID FC SC SO FO

phase phase phase phase

The actual position of the hyoid in each frame of film is indicated by the (closing m~avements) or by the gap between the arrows (opening movements)

dot

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Karen H. Hiiemae et al.

SOLID (SOFT) MEDIUM SIZED RAW LIVER

Fig. 4A (see also Key on p. 69). Solid food (soft; medium-sized raw liver). Hyoid movement during the SO phase was generally upwards and forwards as found in feeding on milk or soft food, except in cycle 7. This atypical orbit occurred as the animal began but did not complete a swallow. The bolus was retained during orbit 8 in which the tongue was protruded and the face licked. Orbit 8 therefore represents the path of the hyoid during simple tongue protrusion and retraction and is drawn to the same convention as Fig. 3A.

in those sequences when the animal was feeding on semi-solid food (Fig. 3b). Similar elongafed hyoid orbits were also found when the animal was feeding on raw liver (Fig. 4A) and in the early stages of feeding on cooked liver (Fig. 4B, cycle 3). The pattern of hyoid movement in all the above cases was characterized by a tendency for the hyoid to move in a broadly elliptical orbit with its long axis at an angle to the palate. In these elliptical orbits, movement of the hyoid was slightly upwardly directed and the return (pharyngeally directed) movement had a downwards component. When the animal was feeding on cooked liver, the shape of the hyoid orbit changed markedly

in mid-sequence cycles (Fig. 4B, cycles 4-7). These mid-sequence hyoid orbits were frequently much shorter in their antero-posterior excursion and were almost always more complicated. In some jaw cycles, the hyoid moved in an orbit which had the same general direction of movement as that found when the animal was feeding on soft food, but in other cycles the direction of the orbital movement was completely reversed (Fig. 4B, cycle 8); in yet others, it assumed a form similar to a figure-of-eight (Fig. 4B, cycles 5, 7). The question of the total distance travelled by the hyoid in these cycles is dealt with in a later sectionHyoid Travel.

Movements of cat hyoid

71

l4

I-

7

Fig. 4B. (see :also Key on p. 69). Solid food (hard; medium-sized cooked liver). Orbits during cycles 1 and 2 of this sequence (not shown) conformed to the general pattern seen for soft and liquid foods as does orbit 3. Orbits 48 show the attenuation and complexity of hyoid movement found in mid-sequence cycles on hard foods. The bolus was swallowed in cycle 11.

Relationship between hyoid orbit and jaw movement Given that the profile of jaw movement differs between early and mid-sequence cycles when the animal is feeding on cooked liver (Thexton et al., 1980), the question arose whether the differences in the hyoid orbit in early and mid-sequence cycles were in any way related to the differences in the jaw movement profiles. The converse considerations applied, in view of the differences in jaw movement profile when the similarity in hyoid orbits associated with feeding on milk, semi-solid food and raw liver were considered. It was therefore necessary to consider the

general relationship between the movement of the hyoid and each phase of movement of the jaw. Lapping. Figure 3A shows that, throughout the period of jaw closing during lapping, the hyoid moved backwards and downwards. During jaw opening, the hyoid moved largely forwards and upwards. The only exception to this basic pattern (Text Fig. 6) was seen when a bolus was swallowed (Fig. 3A, cycle 9). As has been argued elsewhere (Thexton et al., 1980), the division of the low-amplitude jaw movement during lapping into 4 separate phases is probably not appropriate, although for purposes of comparison sometimes convenient. Given that the rate of jaw move-

Karen H.

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Hiiemae

et al.

Gape

Hyoid horizontal

(40 mm)

.*.

’

Fig. 5. Sections of gape and hyoid position data obtained from cinefhtorographic recordings of cats feeding on 4 types of food: A, milk, B, semi-solid catfood; C, medium-sized lumps of raw liver and D, E and F, medium-sized lumps of cooked liver. The cycles shown in A, B and C were characteristic of the cycles found throu~out such feeding sequences whereas those in D were found only in the early part of sequences when the animals were fed cooked liver. The cycles shown in E and F were characteristic of mid-sequence cycles when the animal was feeding on resistant food. The FO/FC complex has been outlined in each jaw cycle in B-F. Note that the most anterior elevated position of the hyoid is associated with a gape of about 20” in every opening movement in A-D. In mid-sequence cycles, that

hyoid position is reached during jaw closing (E) although in some cycles the hyoid may move forward twice in 1 cycle (F). Time is shown by the dashed line. The vertical bars define 500 ms intervals.

ment is used as a criterion for phase recognition, the movement profile of lapping is better considered, for present purposes, as consisting of a slow close movement (SC phase) followed by a slow open movement (SO phase) with an insignificant fast open/fast close (FO/FC) component. Solid and semi-solid food. When medium-sized raw liver was being eaten, the hyoid moved forwards and in most cycles, upwards during the SO phase of jaw movement (Fig. 4A, cycles 3-5 and Fig. 6). The direction of movement in the greater part of the FO phase was then fairly consistently backwards and downwards. The reversal of the direction of the hyoid movement (from anterior to posterior) occurred during either the late SO or the early FO phase as defined from gape data (Fig. 5C). The subsequent backwards movement of the hyoid during the FO phase then continued into the FC movement of the succeeding jaw movement cycle with a backwardsforwards reversal of direction either at the FC/SC transition or slightly earlier at maximum gape. Simi-

lar hyoid orbits were found during the consumption of semi-solid catfood (Fig. 3B, cycles 5, 6 and Text Fig. 5C) and also during the early cycles of feeding sequences involving cooked liver (Fig. 4B, cycles 6, 7 and Fig. SD). In summary, during cycles previously shown to be of a type involved in intra-oral food transport (Hiiemae et a[., 1978; Thexton et al., 1980), the hyoid movement was of large antero-posterior amplitude and was directed in an upwards and forwards direction during the SO phase (or entire opening period in the case of lapping) and in the reverse direction in the FO/FC period (or entire closing period in the case of lapping). Such hyoid movement was not only found when milk, soft catfood or raw liver was being eaten but also in parts of those sequences in which the animals were fed hard solid food. In the last case, such movements occurred at the beginning and end of in midsequences ; they occurred infrequently sequence cycles. In contrast, mid-sequence cycles were associated with highly variable hyoid movement

Movements of cat hyoid

73

Gape

HyCki

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Hyoid horizontal (40mm)

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Fig. SD-F. See caption on facing page.

paths and, usually, s:mall antero-posterior (Fig. 4B and Fig. 5E, F).

excursions

Relationship between jaw and hyoid movement projles

Given, first, the connections between the hyoid and the lower jaw and, secondly, the observation that in the majority of the c:ycles examined, the hyoid orbit could be described as an approximate ellipse with its long axis oriented antero-posteriorly and varying in width, it was expected that the points at which major reversals of hyoid direction occurred would have some systematic rela:tionship to jaw movement. Such points are, for example: the most forward position of the hyoid in any c,ycle which represents the turn between a forwards and backwards movement; the most elevated position, which represents the turn between an upwards and a downwards, movement. It should be noted that the more circular an orbit, the greater the separation in time between these horizontal and vertical turn points. If hyoid movement was directly linked to jaw movement, the reversals seen in either the antero-posterior or the vertical axes of hyoid movement would be expected to show a fixed relationship to either the major reversals of the direction of jaw movement or to some other feature (e.g. the FC-SC or the SO-F0 transition) in the profile of jaw movement. The siequential values from each frame of film for (a) gape, (b) hyoid position in the vertical axis and (c) hyoid position in the horizontal axis were

therefore plotted to show the position and direction of reversals in hyoid movement in relation to jaw movement (Fig. 5A-F). Vertical relationships

In lapping, the hyoid reached its most elevated (ME) position at about the same time as the jaw reached maximum opening, while the most depressed (MD) position of the hyoid corresponded with the minimum gape (Fig. 5A). Two reversals of hyoid direction therefore occurred in each cycle, corresponding to reversals in the jaw movement. However, when data for solid food were examined, the ME position of the hyoid was found to occur in one or other of two positions, either (a) in opening at approximately the transition between SO and FO phases of opening (Fig. SC, D) or (b) less frequently in mid-closing at approximately the transition between the FC and SC phases of closing (Fig. 5E). When the ME position of the hyoid occurred during the opening phases of the cycle, the MD position occurred during the SC or early SO phases (Fig. 5C, D). Conversely, when the ME position was associated with the FC phase, the MD position of the hyoid tended to follow during the late SO phase or during the FO phase. Occasionally, 4 reversals of direction occurred within a single cycle. The domain of the hyoid, i.e. the zone within which it moved as demonstrated by the XY plots (Figs 3 and 4), changed with the type of food. This change is re-

74

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MILK

SOFT

FOOO

COOKED

LIVER

Fig. 6. This figure shows phase of jaw movement.

the frequency with which the hyoid moved in a given direction during each The angle of hyoid travel (ANG; see Methods) was expressed in degrees (G36O”C) and the frequency was then expressed as a percentage of the total sample size (in this case n = 22 for milk, 24 for soft food and 47 for cooked liver). The hatched segments are drawn to scale and identify (i) the range of angles within which the hyoid travelled during each phase, (ii) the actual percentage frequency of that movement. The concentric circles indicate frequencies of 15, 25 and 35 per cent. When lapping milk, the direction of hyoid movement is very similar throughout closing (FC and SC) and again throughout opening (SO and FO). In contrast, the predominant direction of hyoid movement during all 4 phases of cycles for soft food and cooked liver differ; this difference is most clearly shown by the general reversal of direction between the SO and FO phases. SO movement occurred in a downwards and backwards direction in I9 per cent of cycles on cooked liver. These cases correspond to orbits such as those shown in Fig. 4B, cycles 7 and 8.

fleeted in the mean values obtained from measurements of the most depressed (MD) positions of the hyoid in all cycles when the animals were (a) lapping milk (MD values 30.9 + 0.8 SE, n = 27) and (c) cooked liver (MD value 34.7 + 0.4SE, n = 83). Horizontal relationships In lapping cycles, the most posterior (MP) position of the hyoid occurred at about the minimum gape whereas the maximum forward (MF) position occurred at about maximum gape (Fig. 5A). Reversals of hyoid direction in both the horizontal and vertical planes therefore coincided with reversals in jaw move-

ment direction. However, when the animals were feeding on solid or semi-solid food, the MP position corresponded to maximum gape or occurred soon afterwards during jaw closure (Fig. 5BE). In most of such cycles, the MF position of the hyoid coincided with the latter part of the SO phase or with the SO/F0 transition. Occasionally, completion of an initial forwards movement coincided with the FC/SC transition followed by a slight backwards movement and then by a second forward movement in the opening phases of jaw movement (Fig. 5E, F). When feeding on solid food, the MF position of the hyoid always occurred towards the end of the SO

Movements of cat hyoid

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Table 1. The jaw positions most commonly found to correspond to the most elevated (ME), forward (MF), depressed (MD) and posterior (MP) positions of the hyoid when feeding on liquid and solid foods Milk Hyoid position

Lapping

Solid food Cycles with long Cycles with short SO phases SO phases

ME

.Maximum gape

SO/F0 transition

MF

Maximum gape

MD

Miminum gape

MP

Minimum gape

Late SO phase or SO/F0 transition SC or early SO, i.e. close to min gape Maximum gape or in FC

phase in those cycles where the SO phase was of long duration. In those cycles, the hyoid reached its ME and MF positions at about the same time and when the gape was about 20”. However, in other cycles, the ME and MF positions of the hyoid corresponded to the FC/SC transition or occurred within the SC phase. The relationships between hyoid position and jaw position are summarized in Table 1. Characteristics of hycid movement

Three parameters were used to quantify the variable movement of the hyoid during feeding: (a) Hyoid travel: that is the total distance moved by the hyoid along its path during a single phase or a single cycle. (b) Hyoid progress: which is a measure of the net effect of hyoid travel during a phase or cycle and is a vector drawn between the initial and final positions of the hyoid in that phase or cycle. It is expressed as distance at a measured angle to a reference plane (see Methods). (c) Angle: the angle subtended by the direction of the hyoid progress from the reference plane (roughly at right angles to the palate) and measured clockwise in degrees (see Methods). Hyoid travel

The mean values of hyoid travel during each complete cycle (maximum gape-maximum gape) in the cases of milk (X = 25.8 mm) and raw liver (X = 25Smm) were not slatistically different. Despite the extensive protrusive
FC/SC transition or SC phase FC/SC transition or SC phase FO or late SO

Hyoid velocity

The velocity of hyoid movement during the various phases or cycles of jaw movement was calculated by dividing hyoid travel by the duration of the phase or the cycle in question. The average velocity of hyoid movement during about 130 cycles of jaw-hyoid movement on mixed solid and semi-solid foods was The average hyoid velocity was 108 mm s-l. 106 mm s- ’ in those hyoid orbits in which the bone moved forward at an angle of 23@344”, i.e. forwards, during the SO phase (Fig. 6). This angle should reflect the situation in those cycles having the more regular and broadly elliptical orbits. However, the overall velocity changed only insignificantly to 117 mm s-l when the data were selected for cycles in which the hyoid movement during the SO phase was in the reverse direction (SO angle = 57-230”); this angle should reflect the situation in the reversed or figureof-eight orbits. The velocity of hyoid movement in the individual phases, when the data for all foods (excluding milk) were pooled, was calculated as 121 mm s- ’ in the FC phase, as 99.5 mm s- 1 in the SC phase, as 92.7 mm s-l in the SO phase and as 139 mm s- ’ in the FO phase. The difference in velocity of hyoid movement in the SO and FO phases was statistically significant (p < O.OOl), irrespective of whether food was classified into 2 groups on the basis of consistency or of size. Hyoid progress

In order to facilitate comparisons, lapping cycles were divided into phases homologous with those found in all other feeding cycles, although this procedure may not be entirely appropriate (Thexton et al., 1980; A. W. Crompton, unpublished). On the basis of these subdivisions (see Methods), the greatest hyoid progress in lapping was made in the FC phase, less was made in the SO (slow open) phase and least in the SC and FO phases. This was rather different from the pattern seen for soft foods (raw liver and catfood) and for cooked liver, where the average progress in FO was usually greater than in any other phases. Angle of progress

The frequency with which the hyoid progress occurred within each of twelve 30” segments during

Karen H. Hiiemae et ul.

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each phase is shown in Fig. 6 based on pooled data from a number of cats. In lapping, the direction of movement in the early parts of closing (FC phase) was always backwards and almost always downwards. The reverse direction, i.e. forwards and upwards, was always found during opening (SO and FO phases). The major differences in the angle of progress between lapping cycles and those in which soft food was eaten were found in the SC and FO phases (Fig. 6). Movement during the SC phase was then predominantly forwards, and in the FO phase sharply backwards. A similar pattern was found for these 2 phases in cycles in which cooked liver was eaten, although in some such cycles movement during the SC phase was downwards rather than forwards. There was, however, a distinct difference in the angle of progress in the FC phase between the 2 classes of solid food; the hyoid moved predominantly downwards and/or backwards in cycles on soft food but predominantly upwards and forwards when cooked liver was eaten (Fig. 6). DISCUSSION

The assumption that the hyoid of the cat would prove to be in continual motion throughout all feeding activity formed the basis for the specific questions asked in this study. As the results show, this assumption proved justified. The cat hyoid had a continual orbital motion during feeding irrespective of the original consistency of the food. This was expected given the results of previous studies, one of which examined hyoid-tongue base behaviour in a primitive mammal (Crompton rt al., 1977). What was not expected was the observation that some, although a minority of, hyoid orbits in the cat would differ from the general pattern that had been reported in the American opossum (Crompton et al., 1975, 1977) and had been found subsequently in studies of the tenrec, hyrax and macaque (U. Arons, A. W. Crompton, H. Franks, W. L. Hylander, C. Janis, and J. Weijs-Boot. personal communication) as well as in the rabbit (Anapol, 1979). It follows that mammals with widely differing dietetic adaptations (Turnbull. 1970) show closely similar patterns of hyoid movement. It can. therefore, reasonably be infeired that while the details of hyoid orbital motion may vary between mammals, the basic pattern will be found in all Eutheria including man. Nevertheless. we would regard as significant the observations that. first. hyoid movement in the cat is not stereotyped and, secondly, it varies with the type of food and the stage in the masticatory sequence. Such variation has not previously been reported, except in lizards (Smith, 1980). This variation, given the anatomical relationships of the hyoid, is pertinent in the context of the two aspects of hyoid behaviour examined in our study, namely: the degree to which hyoid movement was directly linked to jaw movement; and whether hyoid movement during specific jaw movement cycles was consistent with a division of those cycles into transport and chew categories. The first question might be re-phrased to ask whether the anatomical relationships of the hyoid apparatus are such that all hyoid movement must have a constant relationship to that of the jaw. The results clearly demonstrate that this is not always the case; it is therefore important to examine the nature of the jaw-hyoid

linkage. Thexton et a[. (1980) classified jaw movement cycles, on internal criteria, into two categories: transport cycles with a long SO phase, and chew cycles in which the SO phase was shortened and food movement was apparently suppressed. Given that the hyoid forms the osteological base for the tongue and that its movement must necessarily affect overall tongue position, it was expected that some difference in hyoid movement, reflecting a change in tongue function, would be observed in the two types of jaw movement cycle. Figures 3B and 4B show that such differences do exist, but the question remains as to whether these differences can be correlated with different tongue behaviours in the two cases. These two aspects of hyoid function are, to some extent, independent of each other; the results relating to them are therefore best discussed separately. It should, however, be noted that it was not our purpose to explore the mechanical relationships of jaw and hyoid movement which must underlie the jaw-hyoid linkage nor the relationships between the food, the surface of the tongue and its base. Given the results presented here, those already reported (Crompton et al., 1977; Hiiemae et al., 1978) and data from studies in progress, it should be stated that, first, extensive and patterned movements of the tongue surface occur during feeding and secondly, that the mechanics of jaw and hyoid movement, expecially during jaw opening, are by no means as simple as usually described. It became clear during the early stages of the analysis of the experimental data that some quantification of hyoid position relative to both jaw position and time would be essential if the results were to be properly reported and to serve as a basis for future comparisons iyith data obtained from comparable studies using different experimental animals. Measures of actual hyoid movement during each phase or complete cycle of jaw movement (hyoid travel) and net hyoid movement as a vector (hyoid progress) were therefore developed. The correlation

ofjaw

and hyoid movement

A previous study (Crompton et al., 1977) showed so consistent a relationship between jaw and hyoid movement in the opossum that the two patterns could reasonably be regarded as linked, resulting in an apparently stereotyped pattern of behaviour. No such close correlation was consistently found in the cat; the movement patterns were, however, not completely independent. In lapping, the hyoid always reached its most upward and forwards position at or close to the time of maximum jaw opening and its most backwards and downwards position at, or close to, the time of minimum gape, or maximum jaw closure. In general, a similar relationship was found in those cycles in which soft food was being eaten (as shown by the similarities between Fig. 5A and Fig. 5B and C, and in Table 1) and in some cycles in which the animals were eating hard food. Thexton et al. (1980) showed that the maximum gape attained in lapping (about 20”) at the end of the FO phase corresponds to the gape attained at the end of the SO phase when animals are fed semi-solid or solid food. However, cycles in which non-liquid foods are consumed are characterized by the presence of true FO and FC

Movements of cat hyoid phases. The results we obtained show that the basic relationship between jaw and hyoid position at about 20” of gape persists despite the changes in jaw movement profile following the introduction of fast open and fast close movements. This relationship holds for all cycles in which the time taken for the jaws to open through the initial 20” (the SO phase) was relatively long, amounting to at least 50 per cent and often rather more of the total cycle time. In contrast, when the duration of the SO phase was short, i.e. 2&50 per cent of total cycle time (as found in cycles on solid food), the jaw and hyoid had a different relationship. In these cycles, the hyoid was most likely to have reached its most upwards and forwards position early in the cycle when the jaw was still moving upwards. Such short-duration !
71

Hyoid movement and food handling

It has previously been argued, on theoretical grounds (Hiiemae et al., 1978), that the fundamental mechanism of feeding is not so much the reduction of food by chewing as the transport of food through the mouth for bolus formation and further transport to the stomach. It was further suggested that the retention of inadequately triturated food in the post-canine region of the mouth might require the partial or complete suppression of the transport mechanism. Implicit in these arguments is the assumption that the transport mechanism is tongue-based and depends on a combination of bodily movements, reflected by hyoid movement, and surface or intrinsic movements of the tongue. Thexton et al. (1980) have shown that the jaw movement profile in cycles in which transport was seen to occur was markedly different (with a long SO phase) from those in which transport was suppressed (with a short SO phase). One of the purposes of our present study was. therefore, to examine the pattern of hyoid movement in each type of jaw movement cycle (transport and chew) to determine whether the hyoid orbit was not only different, as the results immediately demonstrated, but whether that difference could be related to the function of the tongue in each. In our experiments, the cats were fed foods of varying consistency of which only one. milk, was passed through the mouth without processing, and without any apparent alteration in consistency other than the possible addition of saliva. We therefore regard the pattern of jaw and hyoid movement in lapping as epitomizing their activity in simple food transport through the mouth (Hiiemae et al., 1978: Thexton et al., 1980). Food handling in mastication is rather more complex; food has to be transported and it must be reduced to a particle size/consistency acceptable for swallowing. The progressive reduction of solidfood particle-size by mastication and the consequent change in its consistency produced by the action of the cheek teeth (Sheine. 1979) requires that particles reduced to a size suitable for swallowing be segregated from the remainder, transported to the back of the mouth and collected together to form a bolus. The residuum must then be reprocessed. The alternative, that particles of all sizes remain mixed together until all reach the size required for swallowing is discounted, since in all the animals so far examined and certainly in the cat, material begins to accumulate to form a bolus well before mastication is completed. In each cycle in which food is mechanically reduced, the residuum must be replaced between the working surfaces of the cheek teeth. In the cat and the opossum. the major bulk of the food, or large particles, is displaced forwards during each power stroke (Hiiemae, 1976). In the opossum, with its long post-canine tooth row, in each cycle the residuum is moved from the anterior part of the post-canine region to the surfaces of the molars during part of the jaw-opening movement (Hiiemae, 1976). In contrast to all other mammals in which intra-oral food handling is or has been examined (opossum, tenrec, hyrax and macaque), the post-canine tooth row in the cat is extremely short, effectively consisting of one large (the carnassial) and a smaller adjacent tooth in each jaw quadrant. It fol-

78

Karen H. Hiiemae et al.

lows that re-placement of food on the carnassials between successive power strokes occurs over much shorter distances in the cat than in longer-jawed mammals. In animals such as the opossum, the transport mechanism which moves adequately triturated food through the mouth towards the oropharynx can also act to replace larger pieces of food between the cheek teeth; this may not be the case in the cat. Instead, the transport mechanism may have to be suppressed or even reversed to maintain the bulk of the inadequately reduced food in relation to the working surfaces of the cheek teeth. Bodily movements of the tongue base, or hyoid, are not, of course, the only mechanism involved in intra-oral food transport (Hiiemae et nl., 1978). Changes in tongue surface profile, resulting from contractions of the intrinsic musculature must also be involved. A tongue surface phenonomen which can be reflexly elicited resembles a series of peristaltic waves on the tongue (Thexton, 1973; McGarrick and Thexton, 1980). Indications of the combined operation in food transport of the tongue base and tongue surface mechanisms have been obtained from cinefluorographic studies of cats lapping (Hiiemae rt a[., 1978) and from studies of food transport and deglutition in the opossum (A. W. Crompton and J. Weijs-Boot, unpublished). In order to examine the question of whether the pattern of hyoid movement in individual cycles was consistent with their categorization as transport or chew cycles, it was assumed that intra-oral handling of liquids involved no processing and therefore both jaw and hyoid movements were related to a purely transfer function. In this situation the orbit of the hyoid approximated to an elongated ellipse the long axis of which was at an angle to the palatal line (Fig. 3A). Such a cam-like movement of the hyoid relative to the palate would be appropriate to the transport of food intra-orally because the elevation and subsequent backwards movement of the hyoid would tend to displace food backwards towards the pharynx. Hyoid orbits, with the same very general elliptical shape as those seen in lapping, also occurred when semi-solid food and raw liver were eaten. The simple elliptical orbit was, however, modified to a varying degree by the introduction of the FO/FC complex into the jaw movement pattern. For example, in cases where the amplitude of the FO/FC complex was minimal (such as raw liver, Figs 4A and SC), little disturbance of the hyoid ellipse was seen. Where a large FO/FC complex occurs, as in feeding on bariumized catfood (Fig. 5B), the ellipse is modified (Fig. 3B) although all orbits retain the upwards and forwards movement of the hyoid in the SO phase (Fig. 6). This movement is then followed by a generally backwards directed movement in the FO phase of jaw tn >vement (a phase not strictly present as such in lapping, see Methods). As in most cycles, reversals from an upwards and forwards to a backwards movement of the hyoid occurred at or close to the time of the SO/F0 transition (or in relation to maximum opening in lapping), it follows that any upwards and forwards progress of the hyoid will be dependent on the duration of the SO phase. This upwards and forwards progress of the hyoid is a relatively slow movement, so that reduction in the length of the SO phase will result in a corresponding reduction in the for-

wards movement, and so in the potential for a subsequent backwards movement of the hyoid or of a bolus. In lapping, posterior movement of the food is facilitated because liquids flow, but it must be pointed out that head posture in lapping is such that this flow occurs, as it were, uphill. Consequently the posterior movement of the hyoid at a time when the jaws are closing in lapping cycles is in a sense useful. However, when dealing with solid foods, the posterior movement of the hyoid at its highest velocity occurs during the FO phase. In that case, it can be argued that it is solely the frictional interface between the tongue and the food that enables the substance to be moved posteriorly towards the pharynx. This food movement may result from a combination of bodily tongue movement (i.e. of its base) coupled with waves of contraction within its musculature (see Hiiemae et nl., 1978; McGarrick and Thexton, 1980). The pattern of jaw and hyoid movement in cycles with long SO phases is consistent with an intra-oral food transport phenomenon whether used (a) to move larger lumps of food to the working surfaces of the post-canine teeth, as in the early cycles of sequences when the animals were fed lumps of cooked liver, or (b) to transport processed material posteriorly to form a bolus, as in late sequence cycles for cooked liver and in all cycles when the animals were fed liquids, semisolid or soft foods. The much-reduced, reversed, or figure-of-eight hyoid orbits recorded in mid-sequence cycles when the animals were fed cooked liver cannot be seen as appropriate for transport of food through the mouth. Reversed orbits may also indicate a short period of reversed direction transport. All such orbits occurred only when the SO duration of the jaw movement cycle was much reduced. These attenuated hyoid orbits, which occur only in mid-sequence cycles on solid food, could be interpreted as reflecting a suppression of the normal transport mechanism in order to facilitate the retention of the residual particles between the working surface of the short post-canine tooth row. Hyoid movement and feeding behavior On anatomical grounds, it was anticipated that the greatest hyoid movement would occur in either or both of two situations: first, when extensive tongue protrusion occurred, as in lapping; second, in association with a large maximum gape (and a large FO/FC complex) as in mid-sequence cycles on cooked liver. In the first case, it was thought that a large forwards movement of the hyoid would facilitate the protrusion of the tip and anterior part of the tongue and the return hyoid movement would assist the rapid retraction of the tongue which occurs in each cycle. In practice, hyoid travel in lapping was less than for other foods. Nevertheless, when the horizontal position of the hyoid during lapping cycles is considered (i.e. hyoid position measured on the X axis, see Figs 3 and 4), it is clear that the most posterior position of the hyoid in lapping is generally further forwards than is normally the case for other foods. It therefore appears likely that hyoid movement contributed a little to tongue protrusion by moving forwards over a comparatively short distance in each cycle but from a more anterior starting position.

79

Movements of cat hyoid In the second case. we believe that, given that the hyoid is an essential component in the jaw opening mechanism, wide jaw opening would be associated with a significant downwards or backwards movement of the hyoid. Such a backwards movement did occur (Figs 3, 4 and 6). Nevertheless, hyoid travel in those cycles in which the cats were eating cooked liver (an activity associated with a large maximum gape) was not such that one might be led to argue that wide jaw opening is necessarily associated with large hyoid excursions. The large amount of hyoid travel in cycles where the cats were feeding on semi-solid catfood appears anomalous. I[n practice, this finding may reflect both the forward movement of the hyoid in tongue protrusion (analogous to lapping) and the backward movement associated with the wide jaw opening which is also a consistent feature of this feeding behaviour. It is possible to draw some specific conclusions. First, our findings, taken together with those on other experimental animals, suggest that the hyoid apparatus in mammals is a highly active component of the orofacial system and does not simply act as a suspensory system for the larynx or an inert and fixed base for the muscles of thse tongue. Second, the behaviour of the hyoid reflects its anatomical connections: it functions as the tongue base in food-processing activities, such as transport, and as a linking element in jaw opening. These two roles are elegantly combined in the utilization of the backward movement associated with jaw opening as an intrinsic element in the food transport mechanism for semi-solid and solid foods. Third, there is a basic relationship between the path of jaw movement and the path of hyoid movement which is characterized by an upwards and forwards movement of the hyoid during the early part of jaw opening. In certain circumstances, this relationship can change significantly, confirming the view that hyoid movement and jaw movement are to some extent independently controlled. Acknowledgements~This work was in part supported by NIH Grant DE-03219. Paulette Ligon typed the manuscript more times than she or the authors care to

remember and W. Winn worked over the illustrations. Our thanks

to them both.

REFERENCES Anapol F. 1979. The descriptive and functional anatomy of the hyoid apparatus in Oryctolagus cuniculus, MA Thesis, University of Illinois at Chicago Circle. Crompton A. W., Cook P., Hiiemae K. M. and Thexton A. J. 1975. The movement of the hyoid apparatus during chewing. Nature 258, 69-70. Crompton A. W., Thexton A. J., Parker P. and Hiiemae K. M. 1977. The activity of the jaw and hyoid musculature in the Virginian opossum, Didelphis uirginiana. In: Biology ofMarsupials (Edited by Gilmore D. and Stonehouse B.) pp. 287-305. Macmillan, New York. Hiiemae K. M. 1976. Masticatory movements in primitive mammals. In: Mastication (Edited by Anderson D. and Matthews B.) pp. lo>1 17. Wright, Bristol. Hiiemae K. M., Thexton A. J. and Crompton A. W. 1978. Intra-oral food transport-a fundamental mechanism of feeding? In: Muscle Adaptation in the Craniofacial Region (Edited by Carlson D. and MacNamara J.), Monograph No. 8, Craniofacial Growth Series, pp. 181-208. University of Michigan. McGarrick J. and Thexton A. J. 1978. A computer aided analysis of jaw and hyoid movement. J. Physiol. 275, 9%IOP. McGarrick J. and Thexton A. W. 1980. A radiographic study of a rhythmic lingual reflex. J. dent. Res. (Abstract; in press). Scheine W. 1979. The effect of variations in molar morphology on masticatory effectiveness and digestion of cellulose in prosimian primates. Ph.D. Thesis, Duke University. Smith K. 1980. The functional morphology of feeding in lizards. Ph.D. Thesis, Harvard University. Thexton A. J. 1973. Reflexes elicited by mechanical stimulation of the palatal mucosa in the cat. Archs oral Biol. 17, 513-523. Thexton A. J., Hiiemae K. M. and Crompton A. W. 1980. Food consistency and bite size as regulators of mastication in cats. J. Neurophysiol. 44, 456-474. Thexton A. J.. Wallace J. and Ebbs S. 1976. Human iaw and hyoid movement. J. Dent. Res. 55, Special Issu; D,

125. Abstract 79. Turnbull W. D. 1970. Mammalian masticatory apparatus. Fieldiana Geol. 18, 153-356.

Plate 1 overleaf.

80

Karen H. Hiiemae er nt.

Plate I. Fig. 1. (A) Post-operative lateral skull radiograph of a cat immediately after insertion of the hyoid marker (hm). Note that separation of the shadows of the mandibular rami and tympanic bullae indicates a slight deviation from true lateral. pi: line of hard palate; sp: soft palate; ts: shadow of posterior tongue surface; crnj: craniomandibular joint; oc: occipital condyles; op: oropharynx. SO*%of actual size (B) Tracing of A to show measurements taken from cineffuorographic recordings. Gape (degrees) is measured as the angle between the palatal and mandibular lines (ml). Hyoid position is measured either parallel (hyoid vertical, hv) or at right angles (hyoid horizontal, hh) to the hyoid reference line (hrl). Hv measures are always positive, hh measures anterior to the reference line are positive, posterior to it negative. All hyoid measures are in mm. (cb, cc and cca refer to the cranial base, cervical column and craniocervical angle. These measures were not used in the present study.)

Movements

of cat hyoid

cca

?Y cc

B Plate 1, Figs 1A and B.