THE JOURNAL OF EXPERIMENTAL ZOOLOGY 261:322-330 (1992)
The Mechanism of Suckling in Two Species of Infant Mammal: Miniature Pigs and Long-Tailed Macaques R.Z. GERMAN, A.W. CROMPTON, L.C. LEVITCH, AND A.J. THEXTON Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221 (R.Z.G.); Museum of Comparative Zoology, Harvard University, Boston, Massachusetts 02138 (A.W.C.); Department of Anatomical Sciences, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15266 (L.C.L.); United Medical and Dental Schools, University of London, London, England (A.J.T.) ABSTRACT
Suckling is the form of feeding unique to infant mammals. The mechanism used by infant mammals to withdraw liquid from the nipple is the subject of considerable debate. Suckling has been examined in two species of infant mammals: miniature pigs and long-tailed macaques. In both species radio-opaque markers were inserted into the tongue and jaws; the movements of the jaw and tongue (and also of specific regions within the tongue) plus the movement of milk containing barium were studied by high-speed cineradiography (100 and 150 framedsec). In the case of macaques, simultaneous pressure transducer recordings were also made. In both species, liquid moved out of the nipple as the intraoral space was expanded by a combination of tongue movement (negative pressure pumping) coupled with jaw opening. There was no evidence for expression (positive pressure on the nipple) in either species, strongly supporting the view that a suction mechanism is responsible for acquisition of milk from the nipple. Subsequent intraoral transport was different in the two species. The pigs used a second pump mechanism at the base of the tongue to transport liquid through the pillars of the fauces into the valleculae. The monkeys used a “squeeze-back” mechanism similar to the transport mechanism documented for adult macaques. Further work with other species can test our tentative hypothesis that all mammals use a negative pressure suction for acquisition, but, as is true for adult mammals, infants may use different transport mechanisms to form and move the bolus.
Suckling, “the behavior of the young contributing to the procurement of milk from a nipple or teat” (Hall et al., ’88) is unique t o infant mammals. The mechanism by which milk is obtained from the maternal nipple or feeding bottle is not well understood. Some of the most significant studies of tongue function during suckling were carried out by Ardran et al. (’58a,b),who recorded suckling in human infants, lambs, and kid goats with cineradiography. In a related study, Ardran and Kemp (’59) used transducers to measure pressure changes in the nipple and oral cavity during suckling in infant lambs and humans. They found that suckling in the species examined was primarily accomplished through expression, i.e., mechanical pressure on the teat by the tongue, and was accompanied by strong jaw movements. The role of suction in this activity was considered to be one of holding the nipple and refilling the teat. Ardran and Kemp (’59) found little correlation between changes in intraoral pressure and the flow of milk in human infants. There were, however, problems in obtaining records of pressures 01992 WILEY-LISS, INC.
in the mouth beyond the teat in both lambs and human infants. Pressure in the teat (and, by the authors’ own evidence, intraoral pressure) was described as falling “when the jaw and tongue were lowered”and as increasing “when the lowerjaw and tongue were raised.” However, somewhat confusingly, the lowest intraoral pressure is described as “coinciding with the highest in the teat.” Part of the problem may have been a reliance on the outline of the milk containing barium to characterize the tongue position; it is known that because of intense longitudinal furrowing the outline corresponding to the middle of the tongue can be confused with the outline of the raised edges in the absence of markers (Thexton and McGarrick, ’88). The opposite view is that suckling results from suction, or negative pressure (Colley and Creamer, ’58). Colley and Creamer (’58) recorded large negative pressure changes in the oral cavity, pharynx,
Received December 7,1990; revision accepted July 2,1991.
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and esophagus in normal human infants during bottle feeding but minimal pressure changes within the nipple. The minimal pressure changes in the bottle, in the face of large falls in external pressure, are potentially explicable on the basis of the resistance to fluid flow offered by the holes in the teat (Ardran and Kemp, ’59).Colley and Creamer (’58)acknowledged a similar shortcoming in their experimental procedure, but in this case it was their inability to record tongue movement. These authors postulate that the backwards movement of the tongue documented by Ardran et al. (’58a) is part of the mechanism to induce the negative pressure underlying the suction mechanism. The work of Ardran et al. (’58a,b)has been cited and used as the basis for almost all subsequent studies of infant suckling. Moyers (’641, in a study documenting ontogenetic changes in motor patterns, examined electromyographic (EMG)patterns of several muscles associated with swallowing and suckling. These observations neither support nor contradict the results of Ardran and his coworkers, as Moyers’ study does not include visualization of the flow of liquid or of the movements of the tongue. Bosma’s review (’72)of infant oral function includes the results of his cineradiographic study of suckling in normal infants. He describes the movement of the tongue as “stripping” the nipple, confirming the results of Ardran et al. (’58a,b). Gordon and Herring (’86) use EMG techniques to compare suckling in infant pigs to that in infant dogs, focusing on the activity pattern of the genioglossus muscle. They also analyze data collected previously by other workers to compare tongue movement in infant pigs and humans. They conclude that pigs, and possibly humans, have a greater “plasticity” of neuromotor patterns and suckling behavior in general than do dogs. However, as this study relies on previous work for data on cineradiologic movement, and as it seeks primarily to resolve neuromuscular questions, it addresses neither the mechanism of liquid acquisition from the nipple nor the mechanism for intraoral transport. The present study examined and tested two competing hypotheses of suckling mechanics in infant mammals using two species, miniature pigs and long-tailed macaques. Cineradiography (100-150 framedsec) recorded the specific movements of the tongue relative to the jaw and the flow of milk into the oral cavity. Radio-opaque markers in the body of the tongue made it possible t o differentiate between intrinsic changes in tongue shape, the movements of the tongue as a unit, and the move-
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ments of the tongue relative to the mandible. These data provided the basis for correlating specific sets of movements (comprising mechanisms potentially capable of causing fluid flow) with the observed movement of milk through the oral cavity and oropharynx prior to swallowing. The two species used for this study were selected for the following reasons. 1. Extensive data on adult feeding mechanisms exist for both species (pigs: Herring and Scapino, ’73; macaques: Franks et al., ’84; Hylander et al., ’87; German et al., ’89). 2. As adults, both animals use a sucking mechanism to acquire liquids (Herring and Scapino, ’73; J. Palmer, Johns Hopkins Medical School, personal communication). 3. The anatomy of pigs’ tongues resembles that of anthropoid primates, as both have a relatively vertically oriented posterior third. 4.Pigs are tractable laboratory animals, easy to train, and have been used in a number of ontogenic studies (Herring and Scapino,’73;Herring, ’85;Gordon and Herring, ’86). 5. Macaques can provide detailed information on the oral behavior of primates and thus yield information of clinical implication that is not easily obtained in humans.
MATERIALS AND METHODS Four 7-day-old infant pigs were obtained from Charles River Laboratories and two 3-week-old Maccaca fascicularis were provided by the New England Regional Primate Research Center. At these ages, the animals were still suckling, but not yet weaned. The pigs could live independently of their sows, and the macaques no longer required an incubator. Similar procedures were used to insert tongue markers into the two species. While the pigs were anesthetized with a mixture of oxygen and halothane, several sterilized metal markers (0.38 inch diameter wire, 1-3 mm long) were inserted into the body of the tongue with a hypodermic syringe and plunger. Two animals each received three markers along the midline-one in the anterior third, one in the middle third, and one in the posterior thirdand two differently shaped markers along the lateral edge. Two received three midline markers relatively deep in the tongue and three markers more superficially. Another short marker was placed in the soft palate of each animal. Except for the “needle teeth,” which are clipped at birth, no dentition had erupted. Two mandibular and two maxillary reference markers were also inserted
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using a syringe. One maxillary marker was inserted under the mucosa at the posterior end of the tooth row and the other under the mucosa anterior to the incisal gingiva. The mandibular markers were placed below the mucosa at the labial, posterior edge of the tooth row and anterior to the incisal gingiva. A small metal marker was attached to the ventral surface of the hyoid with surgical sutures in the anesthetized animal. Anesthesia was induced in the infant macaques with ketamine (10 mgkg) and was maintained with Nembutal(35 mg/ml, 0.4 cc over 3.5 hours) and atropine (0.1 cc/kg). Several sterilized metal markers, again made from 0.38 mm and 1-2 mm in length, were inserted into the body of the tongue with a hypodermic syringe. Another marker was placed in the soft palate, and two mandibular and two maxillary reference markers were also inserted at locations similar to those in the infant pigs. A small marker was attached t o the ventral surface of the hyoid with surgical sutures while the animal was completely anesthetized. After 24 hours for recovery, each animal was fed infant formula with pediatric barium added. The pigs drank a formula, Soweena, designed for pigs from bottles fitted with special soft pig nipples. The primates were fed SMA, a standard human infant formula, in small bottles (Pet).Movement was then recorded in lateral projection with 16 mm Kodak plus-X reversal film at 100 or 150 frames per second (fps) with a Siemens cineradiographic apparatus and an Eclair GV 16 high-speed cine camera. By observing feeding on formula that did not contain barium, we determined that barium did not affect the animal’s feeding behavior in rejection of formula, rate of suckling, or movement of markers in the tongue. In fact, both pigs and macaques appeared to prefer milk with barium. The recording procedures for individuals in both species included several controls. First, animals were filmed prior to any surgery. After surgery to insert tongue and reference markers and a subsequent 24 hour recovery period, the animals were filmed again to ensure that the markers did not interfere with normal feeding. To measure the pressure exerted on the liquid in the nipple durng suckling, a Millar micro-tip pressure transducer (SPR-249w/TCB 500 control box, Houston, TX) was introduced into the nipple of the bottle used by the infant macaques. Pressure was not recorded in every feeding session. When pressure was recorded, it was monitored on a Bell & Howell tape recorded together with a synchronization signal from the cine
camera. These data were then played out on a Gould Strip Chart Recorder, and the pressure data were integrated with the visual image and tongue movement. Twenty-one 100-footfilms were recorded for the infant pigs, and over 20 100-foot films were recorded for the infant macaques. The positions of the radio-opaque markers and of the liquid with barium were analyzed in each frame using a digital imaging system consisting of L&W 4500 projector and cine-chain, a Coho video camera, and a DataCube MaxVision image analysis system attached to a Zenith 386 microcomputer. Some data were digitized using a Vanguard/Sonic Graphpen digitizer and an Apple I1 computer. For each animal, several sequences of suckling and drinking were selected in which the animal did not turn its head out of the lateral plane. These clear X-ray images were digitized and then analyzed. For graphic analyses the movement of a radioopaque marker was examined as a function of time. The location of the tongue markers in Cartesian coordinates was relative to a horizontal axis drawn between the two lower reference markers, and a perpendicular vertical axis through the lower anterior marker, which was designated as the origin. The variable gape was measured as the linear distance between the lower and upper anterior markers.
RESULTS Mechanism o f acquisition and intraoral transport for suckling in infant pigs The basic posture of the infant pigs was t o have the tongue wrapped around the tip of the nipple. The tip of the tongue curled around the nipple was visible outside the oral cavity. The tongue was pressed against the hard palate and the anterior end of the soft palate (Fig. 1, frame 78). A small space existed in the anterior oral cavity, immediately posterior to the nipple. Between frames 80 and 87 the jaw opened slightly (Fig. 2) and the space between the tongue and hard palate expanded as follows: 1)the middle of the tongue, near marker three, moved strongly downwards; 2) the posterior contact between tongue and soft palate, as well as the positions of markers four and five, shifted in a posterior direction. These movements leave two seals, or potential seals, between tongue and palate: a) an anterior seal between hard palate and anterior tongue and b) a posterior seal between the soft palate and posterior tongue. Initially there was an increase in the space between the tongue and palate, which would imply the existence of reduced
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markers four and five, moved anteriorly and ventrally or downward (Fig. 2). This broke the posterior seal and formed a large space beneath the soft tooth palate. At this time, the aliquot of liquid, which had been lying in the space between the anterior and posterior seals underneath the hard palate, was moved through the pillars of the fauces and into the vallecular space above markers four and five (Fig. 1,frame 98). 92 The jaw continued to open between frames 98 and 107 (Fig. 2). The posterior tongue markers moved upward and backward and the liquid moved out of the valleculae. By frame 113, the liquid had passed through the piriform recesses and into the esophagus. These swallows were regular, occurring in every second cycle. Rarely, a swallow occurred in the third cycle, but this only happened when little or no milk was acquired in one of the preceding cycles. The two stage mechanism associated with milk movement was found consistently in repeated stud107 ies of all four animals. Suckling rates varied from 21.2 frameskycle (-- 212 msec) to 26.6 frameskycle (266 msec),with a standard deviation of 2.9 frames, or approximately four to five cycles per second (based on 48 cycles). The largest variation within 113 individuals appeared to be the frequency of feedings, which decreased as the individuals grew, and 7 amount of milk suckled at any feeding, which increased with growth. Variation among individuals was related to the finer details of movement such as amplitude of jaw or tongue movement, or differFig. 1. Suckling in infant miniature pig. Numbers are frame ences in rates of marker movement. All animals numbers from film taken at 100 fps. Anterior is on the right. The arrows indicate the direction of movement between each swallowed every other cycle. Occasionally, a swalframe and the next. The small boxes are radio-opaque mark- low occurred after three suck cycles, but usually ers, numbered from right to left. Scale is approximately one- little or no milk was acquired in one of the first third life size. two cycles.
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Mechanism of acquisition and intraoral pressure if the seals were complete.As marker three transport for suckling in infant macaques moved downward,the anterior seal broke in front of The macaque's tongue was initially elevated to the nipple, and milk moved into the space between the middle tongue and hard palate. The milk that contact a large area of the hard and soft palates, entered the oral cavity as the space was created had leaving a small space in front of the nipple at the a frothy appearance on the X-ray. By the time the anterior end of the oral cavity (Fig. 3, frame 254). jaw began to close and marker one (lying under- In the next five to seven frames the jaw opened and neath the nipple) began to rise, most of the space the middle of the tongue moved strongly downward, between palate and tongue was filled with milk, breaking its seal with the hard palate (Fig. 4). A and little, if any, more was seen to enter the cavity small portion of the anterior tongue remained ele(Fig. 1, frame 92). The tongue reformed the ante- vated without contacting the palate, leaving a small rior seal with the hard palate, just posterior to the gape through which liquid flowed (Fig. 3, frame 261). The posterior of the tongue remained firmly nipple. sealed to the posterior region of the hard palate and The second stage began as the jaw opened bemost of the soft palate. As milk passed through the tween frames 92 and 98, and the middle of the now incomplete anterior seal into the oral cavity, tongue, near marker three, rose to contact the hard it did not have a uniform radiodensity but appeared palate (Fig. 1, frame 98). The posterior tongue, near
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Fig. 2. Movement of tongue markers during infant pig suckling as a function of frame number for approximately one and a half cycles. Left: Movement in the anterior/posterior direction and jaw gape. Down is anterior and up is posterior. Opening
movement is downward on the gape plot. Right: Movement in the dorsahentral direction and jaw gape. The dotted lines represent the frames illustrated in Figure 1.Numbers (tl-45)correspond to markers numbered in Figure 1.Scale bracket = 1cm.
to contain bubbles. Milk continued to leave the nip-
Pressure change in a single cycle was a cyclic rise and fall that could be correlated with tongue movement and milk flow (Fig. 5). Change in pressure closely followed change in gape and middle tongue movement (Fig. 6). Pressure is relatively low at maximum gape, after liquid has been acquired from previous cycle (Figs. 5,6, frame 38). Pressure began to rise as the jaw moves upward and the milk is transported through the oral cavity (Figs. 5, 6, frame 40). At this time there was relatively little milk left in the nipple, and no additional milk entered the mouth while pressure is relatively high (Figs. 5, 6, frame 45). As the jaw began to open (Figs. 5,6, frames 45-60), pressure started to drop, but no milk was seen in the nipple or the oral cavity. Milk did not begin to enter the oral cavity until frame 70, near maximum gape. By this time the nipple was filled with milk, and a space was seen between the palate and tongue. Between frames 70 and 85 (Fig. 61, while pressure was minimal in the nipple, milk left the nipple and continued to enter the oral cavity. After frame 85, no further milk entered either the nipple or the oral cavity. The jaw now began to close, the tongue markers moved ventrally, and pressure began to rise (Fig. 6, frame 90). When tongue movement is measured relative t o mandible movement, as in Figure 6, anterior tongue markers (markers 1 and 21, lying underneath the
ple and enter the oral cavity for another six to eight frames (40-53 msec), until the space between the middle tongue and hard palate was filled (Fig. 3, frame 269). At frame 288 (Fig. 41, the jaw began to close, and milk no longer left the nipple. The anterior tongue moved upward and the posterior tongue downward and forward (Fig. 3, frame 282). Liquid transport continued with these movements for several frames as the jaw continued closing (Fig. 3, frame 296). At frame 300 (Fig.3),the anterior ofthe tongue was still rising and resealing with the hard palate. The posterior tongue changed direction and began to move upward and somewhat backward, moving the contact between it and the palate (Fig. 3, frames 300 and 303). Through these frames, and to the end of this sequence, the posterior tongue established a seal with the hard palate initially, and subsequently with the soft palate, suggestive of a squeezing action. At the same time the liquid moved into the valleculae and then through the piriform recesses, culminating in a swallow.Mean cycle length, based on 17 cycles, was 47.6 frames or 316.7 msec, with a standard deviation of 7.6 frames, or 51 msec. A subsequent analysis of 16 cycles from another individual (studied later) had an average duration of 330 msec, with a standard deviation of 22.8 msec. The monkeys swallowed every cycle.
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Fig. 3. Series of frames from lateral view cineradiologic film of an infant macaque suckling. Anterior is on the right. The numbers are frame numbers, and each frame is 6.67 msec apart (film speed = 150 fps). The locations of tongue markers are shown as small numbers in frame 254, and arrows indicate movement of regions of the tongue based on these markers. The stippled areas are the locations of the aliquot of radio-opaque milk. Scale is 40% lifesize.
nipple, moved very little relative to the lower jaw. However, marker 3, nearer the middle of the tongue, moved downward (dorsally)relative to the lower jaw, at the same time the jaw moved downward. The extent of upward movement of the anterior tongue was the extent of jaw movement, although, again, marker three had a large excursion of movement in addition to jaw movement.
DISCUSSION Suction vs. expression: the mechanism of suckling The initial conflict over the mechanism of suckling, either expression (Ardran et al., ’58 a, b; Bosma, ’67, ’72) or suction (Colley and Creamer, ‘58),could not be resolved with the data obtained from the techniques available at that time. As Colley and Creamer (’58)suggest, both pressure and cine-fluorographicdata are necessary, as are tongue markers and registration points, so that movements
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of the tongue can be accurately measured. Without spatial markers, it is extremely difficult to separate the movements of the tongue from the mandible, although Bosma (’72)states that the tongue and mandible move as a single unit. The “stripping” mechanism of Ardran et al. (’58a,b)and Bosma (’67, ’72) is also difficult to document without markers in the tongue t o indicate movement relative to the milk. Two recent studies attempted to resolve the “expression/suction”question by applying ultrasonographic technology to observe the nipple and oral cavity during suckling in human infants (Weber et al., ’86; Smith et al., ’88). Weber et al. (’86),using the term suck to mean “stripping action of the tongue without laryngeal movement,” confirmed the conclusion of Ardran et al. (’58a,b) that this movement causes milk to flow into the oral cavity. Although most interested in documenting nipple deformation during suckling, Smith et al. (’88) reported that the motion of the tongue is “undulant” rather than “pistonlike” as described by Weber et al. (’86). Furthermore, Smith et al. (’88)reported that milk ejection occurs after the maximal nipple deformation and coincides with the downstroke of tongue and jaw. They suggested that the jaw actually creates negative pressure by enlarging the oral cavity but that pressure measurements are needed t o confirm this hypothesis. The above studies have several limitations. Given that significant movements of the anatomical structures involved in feeding can occur in 10 msec (Hiiemae and Crompton, ’85; German et al., ’€is), a frame period lasting 33-40 msec must give rise t o blurred images of the structures taking part in that movement. The quality of video images of fast moving objects obtained by routine clinical fluoroscopy or by ultrasonography will consequently be limited not only by the intrinsic nature of the technique but also by design constraints of the apparatus. Without reference markers in the tongue and jaw it may be difficult (even impossible) to evaluate, with any accuracy, either the movement of the tongue relative to the jaws or the effect of the movement on liquid in the mouth. Although the data presented in this paper recorded data on pressure changes only in infant macaques, detailed analyses of tongue movement and intraoral movement of radio-opaque milk provided a precise demonstration of the role of the tongue during suckling for both species. While the tongue does move generally with a dorsal/ventral pumping motion, as described by Adran et al. (’58a,b)and Bosma (’67,’72),it is not a “stripping mechanism.” The tongue did press against the nip-
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Fig. 4. Movement of tongue markers during infant longtailed macaque suckling as a function offrame number for one cycle. Left:Movement in the anterior/posterior direction and jaw gape. Down is anterior, and up is posterior. Opening movement
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is downward on the gape plot. Right: Movement in the dorsal/ ventral direction and jaw gape. The dotted lines represent the frames illustrated in Figure 3. Scale bracket = 5 cm.
ple, but when that occurred the tongue was firmly sealed against the palate and no milk left the nipple. Our data showed that the tongue and mandible did not move as a unit in infant macaques and miniature pigs. Liquid entered the oral cavity only when the tongue was moving ventrally. This result strongly supports the idea that suction is the major mechanism for the acquisition of liquid during suck-
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Fig. 5. Series of frames from lateral view cineradiologic film of an infant macaque suckling, while pressure in the nipple was recorded. Anterior is on the right. Numbers are frame numbers, and each frame is 6.67 msec apart (film speed = 150 fps). The milk is shown as a stippled area in the oral cavity. The first three markers are numbered from right to left.
Fig. 6. Gape, movement of tongue markers, and change in pressure in bottle nipple as a function of frame number during macaque suckling. Down is dorsal movement, and up is ventral movement. Jaw opening and pressure decreases are downward, and jaw closing and pressure increases are upward. Numbers (tl-t3) correspond to markers numbered in Figure 5.
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(Herring and Scapino, ,731, and finally a squeezeback mechanism in primates (J. Palmer, JHMI, personal communication). The comparison of the results on infant suckling with known mechanisms of adult transport lead us to several evolutionary hypotheses that require further testing with additional species of mammals. The first suggests that initial acquisition of milk takes place as a negative pressure mechanism, as opposed to licking, expression, or other positive pressure mechanism, and all infant mammals use this mechanism during suckling, the act of procuring liquid from the teat. Second, this mechanism Differencesin suckling between infant probably arose as early as did suckling and is macaques and pigs related to the evolution of the mobility of the mamThe initial mechanisms of acquisition in the two malian tongue. Sucking exists in at least one monspecies is consistent with the operation of suction otreme without teats, the echidna (Griffths, '78). pumps. The ventral movement of the tongue is capa- Furthermore, as in adults, subsequent intraoral ble of causing the necessary drop in pressure in the transport in infants is more varied than the mechoral cavity to draw liquid out of the nipple, because anisms of acquisition. the posterior tongue contacts the soft palate and ACKNOWLEDGMENTS presumably forms a seal. The frothy appearance of the radio-opaque milk at this time is consistent We thank Ken Gordon, Susan Herring, David with bubbling and is therefore also consistent with Hertweck, Karen Hiiemae, Tina Rouse, and Jeff a negative pressure in the oral cavity. At the same Shultz for their assistance in this project. We also time, the pressure measured in the nipple was also acknowledge the assistance of the New England negative, but milk was flowing out of the nipple Regional Primate Research Center in providing us through a restricted orifice; the pressure must with the infant macaques. This work was supported therefore have been even lower in the oral cavity. by NIH grant DE-8697 to R.Z.G. and A.W.C. All the evidence therefore points to the production LITERATURE CITED of low pressure within the oral cavity. The subsequent transport mechanisms differed Ardran, G.M., and F.H. Kemp (1959) A correlation between in the two species. In pigs, a downward and forward sucking pressures and movement of the tongue. Acta Paediatr. 48:261-272. movement of the back of the tongue, which could create a lowered pressure, was associated with Ardran, G.M., F.H. Kemp, and J. Lind (1958a) A cineradiographic study of bottle feeding. Br. J. Radiol., 31:ll-22. movement of liquid through the pillars of the fau- Ardran, G.M., F.H. Kemp, and J. Lind (1958b) A cineradioces into the valleculae. The macaques, however, graphic study ofbreast feeding. Br. J. Radiol., 31:156-162. used a mechanism that closely resembled a mech- Bosma, J. (1967) Human infant oral function. In Symposium on Oral Sensation and Perception. J.F. Bosma, ed. C.C. anism used by adult macaques to transport either Thomas, Springfield, IL, pp. 98-110. well-masticated food (stage I1 transport; Franks et J. (1972) Form and function in the infant's mouth and al., '84)or liquid (J.Palmer, Johns Hopkins Medi- Bosma, pharynx. In Third Symposium on Oral Sensation and Percal Institutions, personal communication; German ception. J.F. Bosma, ed. C.C. Thomas, Springfield, IL, pp. 3-29. et al., unpublished data). Colley, J.R.T., and B. Creamer (1958) Sucking and swallowing infants. Br. Med. J.,2:422-423. A variety of mechanisms for acquisition and transport of liquid have been documented in adult Franks, H.A., R.Z. German, and A.W. Crompton (1984) Mechanism of intraoral transport in macaques. Am. J. Phys. mammals. Sucking (in pigs and primates) and lapAnthropol., 65:275-282. ping (in cats and opossums)are the primary mech- German, R.Z., S.A. Saxe, A.W. Crompton, and K.M. Hiiemae anisms of liquid acquisition (Gordon and Herring, (1989) Food transport through the anterior oral cavity in macaques. Am. J. Phys. Anthropol., 80:369-377. '86; Thexton and McGarrick '88; Hiiemae and Crompton, '85).Homologous mechanisms of trans- Gordon, K.R., and S.W. Herring (1986)Activity patterns within the genioglossus during suckling in domestic dogs and pigs: port include negative pressure in cats (Thexton and interspecific and intraspecific plasticity. Brain Behav. Evol., McGarrick, 'SS), posterior movement of the tongue 30:249-262. carrying liquid in opossums (Hiiemae and Cromp- Grifiths, M. (1978) The Biology of the Monotremes. Academic Press, New York. 367 pp. ton, '85),a pumping motion of the tongue in pigs ling in infant pigs and macaques. This conclusion is supported by the pressure transducer data obtained from the macaque feeding records, where reduced pressure in the nipple was recorded when milk left the nipple, and at no point were large increases in pressure recorded. This is entirely incompatible with any positive pressure or expression mechanism for suckling. However, this was an experimental situation using a bottle and therefore not equivalent to a maternal nursing situation. In the latter, maternal expression plays a role in the initial acquisition of milk.
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Hall, W.G., R. Hudson, and S.C. Brake (1988) Terminology for use in investigations of nursing and suckling. Dev. Psychobiol., 21 :89-91. Herring, S.W. (1985)The ontogeny ofmammalian mastication. Am. Zool., 25:339-349. Herring, S.W., and R.P. Scapino (1973) Physiology of feeding in miniature pigs. J. Morphol., 141 :427-460. Hiiemae, K.M., and A.W. Crompton (1985) Mastication, food transport and swallowing. In: Functional Vertebrate Morphology. M. Hildebrand, D.M. Bramble, K.F. Liem, and D.B. Wake, eds. Belknap Press of Harvard University Press, Cambridge, MA. pp. 262-290. Hylander, W.L., Johnson, K.R., and Crompton, A.W. (1987) Loading patterns and jaw movements during mastication. In:
Maccaca fascicularis: A bone-strain, electromyographic, and cineradiographic analysis. Am. J . Phys. Anthropol., 72: 287-314. Moyers, R.E. (1964) The infantile swallow. Eur. Orthod. SOC., 40:180-187. Smith, W.L., A. Erenberg, A. Nowak (1988) Imaging evaluation of the human nipple during breast-feeding. AJDC, 142:76-78. Thexton, A.J., and J.D. McGarrick (1988) Tongue movement of the cat during lapping. Arch. Oral Biol., 33:331-339. Weber, F., M.W. Woolridge, and J.D. Baum (1986) An ultrasonographic study of the organization of sucking and swallowing by newborn infants. Dev. Med. Child Neurol., 28: 19-24.
The Mechanism of Suckling in Two Species of Infant Mammal: Miniature Pigs and Long-Tailed Macaques R.Z. GERMAN, A.W. CROMPTON, L.C. LEVITCH, AND A.J. THEXTON Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio 45221 (R.Z.G.); Museum of Comparative Zoology, Harvard University, Boston, Massachusetts 02138 (A.W.C.); Department of Anatomical Sciences, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15266 (L.C.L.); United Medical and Dental Schools, University of London, London, England (A.J.T.) ABSTRACT
Suckling is the form of feeding unique to infant mammals. The mechanism used by infant mammals to withdraw liquid from the nipple is the subject of considerable debate. Suckling has been examined in two species of infant mammals: miniature pigs and long-tailed macaques. In both species radio-opaque markers were inserted into the tongue and jaws; the movements of the jaw and tongue (and also of specific regions within the tongue) plus the movement of milk containing barium were studied by high-speed cineradiography (100 and 150 framedsec). In the case of macaques, simultaneous pressure transducer recordings were also made. In both species, liquid moved out of the nipple as the intraoral space was expanded by a combination of tongue movement (negative pressure pumping) coupled with jaw opening. There was no evidence for expression (positive pressure on the nipple) in either species, strongly supporting the view that a suction mechanism is responsible for acquisition of milk from the nipple. Subsequent intraoral transport was different in the two species. The pigs used a second pump mechanism at the base of the tongue to transport liquid through the pillars of the fauces into the valleculae. The monkeys used a “squeeze-back” mechanism similar to the transport mechanism documented for adult macaques. Further work with other species can test our tentative hypothesis that all mammals use a negative pressure suction for acquisition, but, as is true for adult mammals, infants may use different transport mechanisms to form and move the bolus.
Suckling, “the behavior of the young contributing to the procurement of milk from a nipple or teat” (Hall et al., ’88) is unique t o infant mammals. The mechanism by which milk is obtained from the maternal nipple or feeding bottle is not well understood. Some of the most significant studies of tongue function during suckling were carried out by Ardran et al. (’58a,b),who recorded suckling in human infants, lambs, and kid goats with cineradiography. In a related study, Ardran and Kemp (’59) used transducers to measure pressure changes in the nipple and oral cavity during suckling in infant lambs and humans. They found that suckling in the species examined was primarily accomplished through expression, i.e., mechanical pressure on the teat by the tongue, and was accompanied by strong jaw movements. The role of suction in this activity was considered to be one of holding the nipple and refilling the teat. Ardran and Kemp (’59) found little correlation between changes in intraoral pressure and the flow of milk in human infants. There were, however, problems in obtaining records of pressures 01992 WILEY-LISS, INC.
in the mouth beyond the teat in both lambs and human infants. Pressure in the teat (and, by the authors’ own evidence, intraoral pressure) was described as falling “when the jaw and tongue were lowered”and as increasing “when the lowerjaw and tongue were raised.” However, somewhat confusingly, the lowest intraoral pressure is described as “coinciding with the highest in the teat.” Part of the problem may have been a reliance on the outline of the milk containing barium to characterize the tongue position; it is known that because of intense longitudinal furrowing the outline corresponding to the middle of the tongue can be confused with the outline of the raised edges in the absence of markers (Thexton and McGarrick, ’88). The opposite view is that suckling results from suction, or negative pressure (Colley and Creamer, ’58). Colley and Creamer (’58) recorded large negative pressure changes in the oral cavity, pharynx,
Received December 7,1990; revision accepted July 2,1991.
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and esophagus in normal human infants during bottle feeding but minimal pressure changes within the nipple. The minimal pressure changes in the bottle, in the face of large falls in external pressure, are potentially explicable on the basis of the resistance to fluid flow offered by the holes in the teat (Ardran and Kemp, ’59).Colley and Creamer (’58)acknowledged a similar shortcoming in their experimental procedure, but in this case it was their inability to record tongue movement. These authors postulate that the backwards movement of the tongue documented by Ardran et al. (’58a) is part of the mechanism to induce the negative pressure underlying the suction mechanism. The work of Ardran et al. (’58a,b)has been cited and used as the basis for almost all subsequent studies of infant suckling. Moyers (’641, in a study documenting ontogenetic changes in motor patterns, examined electromyographic (EMG)patterns of several muscles associated with swallowing and suckling. These observations neither support nor contradict the results of Ardran and his coworkers, as Moyers’ study does not include visualization of the flow of liquid or of the movements of the tongue. Bosma’s review (’72)of infant oral function includes the results of his cineradiographic study of suckling in normal infants. He describes the movement of the tongue as “stripping” the nipple, confirming the results of Ardran et al. (’58a,b). Gordon and Herring (’86) use EMG techniques to compare suckling in infant pigs to that in infant dogs, focusing on the activity pattern of the genioglossus muscle. They also analyze data collected previously by other workers to compare tongue movement in infant pigs and humans. They conclude that pigs, and possibly humans, have a greater “plasticity” of neuromotor patterns and suckling behavior in general than do dogs. However, as this study relies on previous work for data on cineradiologic movement, and as it seeks primarily to resolve neuromuscular questions, it addresses neither the mechanism of liquid acquisition from the nipple nor the mechanism for intraoral transport. The present study examined and tested two competing hypotheses of suckling mechanics in infant mammals using two species, miniature pigs and long-tailed macaques. Cineradiography (100-150 framedsec) recorded the specific movements of the tongue relative to the jaw and the flow of milk into the oral cavity. Radio-opaque markers in the body of the tongue made it possible t o differentiate between intrinsic changes in tongue shape, the movements of the tongue as a unit, and the move-
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ments of the tongue relative to the mandible. These data provided the basis for correlating specific sets of movements (comprising mechanisms potentially capable of causing fluid flow) with the observed movement of milk through the oral cavity and oropharynx prior to swallowing. The two species used for this study were selected for the following reasons. 1. Extensive data on adult feeding mechanisms exist for both species (pigs: Herring and Scapino, ’73; macaques: Franks et al., ’84; Hylander et al., ’87; German et al., ’89). 2. As adults, both animals use a sucking mechanism to acquire liquids (Herring and Scapino, ’73; J. Palmer, Johns Hopkins Medical School, personal communication). 3. The anatomy of pigs’ tongues resembles that of anthropoid primates, as both have a relatively vertically oriented posterior third. 4.Pigs are tractable laboratory animals, easy to train, and have been used in a number of ontogenic studies (Herring and Scapino,’73;Herring, ’85;Gordon and Herring, ’86). 5. Macaques can provide detailed information on the oral behavior of primates and thus yield information of clinical implication that is not easily obtained in humans.
MATERIALS AND METHODS Four 7-day-old infant pigs were obtained from Charles River Laboratories and two 3-week-old Maccaca fascicularis were provided by the New England Regional Primate Research Center. At these ages, the animals were still suckling, but not yet weaned. The pigs could live independently of their sows, and the macaques no longer required an incubator. Similar procedures were used to insert tongue markers into the two species. While the pigs were anesthetized with a mixture of oxygen and halothane, several sterilized metal markers (0.38 inch diameter wire, 1-3 mm long) were inserted into the body of the tongue with a hypodermic syringe and plunger. Two animals each received three markers along the midline-one in the anterior third, one in the middle third, and one in the posterior thirdand two differently shaped markers along the lateral edge. Two received three midline markers relatively deep in the tongue and three markers more superficially. Another short marker was placed in the soft palate of each animal. Except for the “needle teeth,” which are clipped at birth, no dentition had erupted. Two mandibular and two maxillary reference markers were also inserted
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using a syringe. One maxillary marker was inserted under the mucosa at the posterior end of the tooth row and the other under the mucosa anterior to the incisal gingiva. The mandibular markers were placed below the mucosa at the labial, posterior edge of the tooth row and anterior to the incisal gingiva. A small metal marker was attached to the ventral surface of the hyoid with surgical sutures in the anesthetized animal. Anesthesia was induced in the infant macaques with ketamine (10 mgkg) and was maintained with Nembutal(35 mg/ml, 0.4 cc over 3.5 hours) and atropine (0.1 cc/kg). Several sterilized metal markers, again made from 0.38 mm and 1-2 mm in length, were inserted into the body of the tongue with a hypodermic syringe. Another marker was placed in the soft palate, and two mandibular and two maxillary reference markers were also inserted at locations similar to those in the infant pigs. A small marker was attached t o the ventral surface of the hyoid with surgical sutures while the animal was completely anesthetized. After 24 hours for recovery, each animal was fed infant formula with pediatric barium added. The pigs drank a formula, Soweena, designed for pigs from bottles fitted with special soft pig nipples. The primates were fed SMA, a standard human infant formula, in small bottles (Pet).Movement was then recorded in lateral projection with 16 mm Kodak plus-X reversal film at 100 or 150 frames per second (fps) with a Siemens cineradiographic apparatus and an Eclair GV 16 high-speed cine camera. By observing feeding on formula that did not contain barium, we determined that barium did not affect the animal’s feeding behavior in rejection of formula, rate of suckling, or movement of markers in the tongue. In fact, both pigs and macaques appeared to prefer milk with barium. The recording procedures for individuals in both species included several controls. First, animals were filmed prior to any surgery. After surgery to insert tongue and reference markers and a subsequent 24 hour recovery period, the animals were filmed again to ensure that the markers did not interfere with normal feeding. To measure the pressure exerted on the liquid in the nipple durng suckling, a Millar micro-tip pressure transducer (SPR-249w/TCB 500 control box, Houston, TX) was introduced into the nipple of the bottle used by the infant macaques. Pressure was not recorded in every feeding session. When pressure was recorded, it was monitored on a Bell & Howell tape recorded together with a synchronization signal from the cine
camera. These data were then played out on a Gould Strip Chart Recorder, and the pressure data were integrated with the visual image and tongue movement. Twenty-one 100-footfilms were recorded for the infant pigs, and over 20 100-foot films were recorded for the infant macaques. The positions of the radio-opaque markers and of the liquid with barium were analyzed in each frame using a digital imaging system consisting of L&W 4500 projector and cine-chain, a Coho video camera, and a DataCube MaxVision image analysis system attached to a Zenith 386 microcomputer. Some data were digitized using a Vanguard/Sonic Graphpen digitizer and an Apple I1 computer. For each animal, several sequences of suckling and drinking were selected in which the animal did not turn its head out of the lateral plane. These clear X-ray images were digitized and then analyzed. For graphic analyses the movement of a radioopaque marker was examined as a function of time. The location of the tongue markers in Cartesian coordinates was relative to a horizontal axis drawn between the two lower reference markers, and a perpendicular vertical axis through the lower anterior marker, which was designated as the origin. The variable gape was measured as the linear distance between the lower and upper anterior markers.
RESULTS Mechanism o f acquisition and intraoral transport for suckling in infant pigs The basic posture of the infant pigs was t o have the tongue wrapped around the tip of the nipple. The tip of the tongue curled around the nipple was visible outside the oral cavity. The tongue was pressed against the hard palate and the anterior end of the soft palate (Fig. 1, frame 78). A small space existed in the anterior oral cavity, immediately posterior to the nipple. Between frames 80 and 87 the jaw opened slightly (Fig. 2) and the space between the tongue and hard palate expanded as follows: 1)the middle of the tongue, near marker three, moved strongly downwards; 2) the posterior contact between tongue and soft palate, as well as the positions of markers four and five, shifted in a posterior direction. These movements leave two seals, or potential seals, between tongue and palate: a) an anterior seal between hard palate and anterior tongue and b) a posterior seal between the soft palate and posterior tongue. Initially there was an increase in the space between the tongue and palate, which would imply the existence of reduced
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markers four and five, moved anteriorly and ventrally or downward (Fig. 2). This broke the posterior seal and formed a large space beneath the soft tooth palate. At this time, the aliquot of liquid, which had been lying in the space between the anterior and posterior seals underneath the hard palate, was moved through the pillars of the fauces and into the vallecular space above markers four and five (Fig. 1,frame 98). 92 The jaw continued to open between frames 98 and 107 (Fig. 2). The posterior tongue markers moved upward and backward and the liquid moved out of the valleculae. By frame 113, the liquid had passed through the piriform recesses and into the esophagus. These swallows were regular, occurring in every second cycle. Rarely, a swallow occurred in the third cycle, but this only happened when little or no milk was acquired in one of the preceding cycles. The two stage mechanism associated with milk movement was found consistently in repeated stud107 ies of all four animals. Suckling rates varied from 21.2 frameskycle (-- 212 msec) to 26.6 frameskycle (266 msec),with a standard deviation of 2.9 frames, or approximately four to five cycles per second (based on 48 cycles). The largest variation within 113 individuals appeared to be the frequency of feedings, which decreased as the individuals grew, and 7 amount of milk suckled at any feeding, which increased with growth. Variation among individuals was related to the finer details of movement such as amplitude of jaw or tongue movement, or differFig. 1. Suckling in infant miniature pig. Numbers are frame ences in rates of marker movement. All animals numbers from film taken at 100 fps. Anterior is on the right. The arrows indicate the direction of movement between each swallowed every other cycle. Occasionally, a swalframe and the next. The small boxes are radio-opaque mark- low occurred after three suck cycles, but usually ers, numbered from right to left. Scale is approximately one- little or no milk was acquired in one of the first third life size. two cycles.
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Mechanism of acquisition and intraoral pressure if the seals were complete.As marker three transport for suckling in infant macaques moved downward,the anterior seal broke in front of The macaque's tongue was initially elevated to the nipple, and milk moved into the space between the middle tongue and hard palate. The milk that contact a large area of the hard and soft palates, entered the oral cavity as the space was created had leaving a small space in front of the nipple at the a frothy appearance on the X-ray. By the time the anterior end of the oral cavity (Fig. 3, frame 254). jaw began to close and marker one (lying under- In the next five to seven frames the jaw opened and neath the nipple) began to rise, most of the space the middle of the tongue moved strongly downward, between palate and tongue was filled with milk, breaking its seal with the hard palate (Fig. 4). A and little, if any, more was seen to enter the cavity small portion of the anterior tongue remained ele(Fig. 1, frame 92). The tongue reformed the ante- vated without contacting the palate, leaving a small rior seal with the hard palate, just posterior to the gape through which liquid flowed (Fig. 3, frame 261). The posterior of the tongue remained firmly nipple. sealed to the posterior region of the hard palate and The second stage began as the jaw opened bemost of the soft palate. As milk passed through the tween frames 92 and 98, and the middle of the now incomplete anterior seal into the oral cavity, tongue, near marker three, rose to contact the hard it did not have a uniform radiodensity but appeared palate (Fig. 1, frame 98). The posterior tongue, near
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Fig. 2. Movement of tongue markers during infant pig suckling as a function of frame number for approximately one and a half cycles. Left: Movement in the anterior/posterior direction and jaw gape. Down is anterior and up is posterior. Opening
movement is downward on the gape plot. Right: Movement in the dorsahentral direction and jaw gape. The dotted lines represent the frames illustrated in Figure 1.Numbers (tl-45)correspond to markers numbered in Figure 1.Scale bracket = 1cm.
to contain bubbles. Milk continued to leave the nip-
Pressure change in a single cycle was a cyclic rise and fall that could be correlated with tongue movement and milk flow (Fig. 5). Change in pressure closely followed change in gape and middle tongue movement (Fig. 6). Pressure is relatively low at maximum gape, after liquid has been acquired from previous cycle (Figs. 5,6, frame 38). Pressure began to rise as the jaw moves upward and the milk is transported through the oral cavity (Figs. 5, 6, frame 40). At this time there was relatively little milk left in the nipple, and no additional milk entered the mouth while pressure is relatively high (Figs. 5, 6, frame 45). As the jaw began to open (Figs. 5,6, frames 45-60), pressure started to drop, but no milk was seen in the nipple or the oral cavity. Milk did not begin to enter the oral cavity until frame 70, near maximum gape. By this time the nipple was filled with milk, and a space was seen between the palate and tongue. Between frames 70 and 85 (Fig. 61, while pressure was minimal in the nipple, milk left the nipple and continued to enter the oral cavity. After frame 85, no further milk entered either the nipple or the oral cavity. The jaw now began to close, the tongue markers moved ventrally, and pressure began to rise (Fig. 6, frame 90). When tongue movement is measured relative t o mandible movement, as in Figure 6, anterior tongue markers (markers 1 and 21, lying underneath the
ple and enter the oral cavity for another six to eight frames (40-53 msec), until the space between the middle tongue and hard palate was filled (Fig. 3, frame 269). At frame 288 (Fig. 41, the jaw began to close, and milk no longer left the nipple. The anterior tongue moved upward and the posterior tongue downward and forward (Fig. 3, frame 282). Liquid transport continued with these movements for several frames as the jaw continued closing (Fig. 3, frame 296). At frame 300 (Fig.3),the anterior ofthe tongue was still rising and resealing with the hard palate. The posterior tongue changed direction and began to move upward and somewhat backward, moving the contact between it and the palate (Fig. 3, frames 300 and 303). Through these frames, and to the end of this sequence, the posterior tongue established a seal with the hard palate initially, and subsequently with the soft palate, suggestive of a squeezing action. At the same time the liquid moved into the valleculae and then through the piriform recesses, culminating in a swallow.Mean cycle length, based on 17 cycles, was 47.6 frames or 316.7 msec, with a standard deviation of 7.6 frames, or 51 msec. A subsequent analysis of 16 cycles from another individual (studied later) had an average duration of 330 msec, with a standard deviation of 22.8 msec. The monkeys swallowed every cycle.
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Fig. 3. Series of frames from lateral view cineradiologic film of an infant macaque suckling. Anterior is on the right. The numbers are frame numbers, and each frame is 6.67 msec apart (film speed = 150 fps). The locations of tongue markers are shown as small numbers in frame 254, and arrows indicate movement of regions of the tongue based on these markers. The stippled areas are the locations of the aliquot of radio-opaque milk. Scale is 40% lifesize.
nipple, moved very little relative to the lower jaw. However, marker 3, nearer the middle of the tongue, moved downward (dorsally)relative to the lower jaw, at the same time the jaw moved downward. The extent of upward movement of the anterior tongue was the extent of jaw movement, although, again, marker three had a large excursion of movement in addition to jaw movement.
DISCUSSION Suction vs. expression: the mechanism of suckling The initial conflict over the mechanism of suckling, either expression (Ardran et al., ’58 a, b; Bosma, ’67, ’72) or suction (Colley and Creamer, ‘58),could not be resolved with the data obtained from the techniques available at that time. As Colley and Creamer (’58)suggest, both pressure and cine-fluorographicdata are necessary, as are tongue markers and registration points, so that movements
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of the tongue can be accurately measured. Without spatial markers, it is extremely difficult to separate the movements of the tongue from the mandible, although Bosma (’72)states that the tongue and mandible move as a single unit. The “stripping” mechanism of Ardran et al. (’58a,b)and Bosma (’67, ’72) is also difficult to document without markers in the tongue t o indicate movement relative to the milk. Two recent studies attempted to resolve the “expression/suction”question by applying ultrasonographic technology to observe the nipple and oral cavity during suckling in human infants (Weber et al., ’86; Smith et al., ’88). Weber et al. (’86),using the term suck to mean “stripping action of the tongue without laryngeal movement,” confirmed the conclusion of Ardran et al. (’58a,b) that this movement causes milk to flow into the oral cavity. Although most interested in documenting nipple deformation during suckling, Smith et al. (’88) reported that the motion of the tongue is “undulant” rather than “pistonlike” as described by Weber et al. (’86). Furthermore, Smith et al. (’88)reported that milk ejection occurs after the maximal nipple deformation and coincides with the downstroke of tongue and jaw. They suggested that the jaw actually creates negative pressure by enlarging the oral cavity but that pressure measurements are needed t o confirm this hypothesis. The above studies have several limitations. Given that significant movements of the anatomical structures involved in feeding can occur in 10 msec (Hiiemae and Crompton, ’85; German et al., ’€is), a frame period lasting 33-40 msec must give rise t o blurred images of the structures taking part in that movement. The quality of video images of fast moving objects obtained by routine clinical fluoroscopy or by ultrasonography will consequently be limited not only by the intrinsic nature of the technique but also by design constraints of the apparatus. Without reference markers in the tongue and jaw it may be difficult (even impossible) to evaluate, with any accuracy, either the movement of the tongue relative to the jaws or the effect of the movement on liquid in the mouth. Although the data presented in this paper recorded data on pressure changes only in infant macaques, detailed analyses of tongue movement and intraoral movement of radio-opaque milk provided a precise demonstration of the role of the tongue during suckling for both species. While the tongue does move generally with a dorsal/ventral pumping motion, as described by Adran et al. (’58a,b)and Bosma (’67,’72),it is not a “stripping mechanism.” The tongue did press against the nip-
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Fig. 4. Movement of tongue markers during infant longtailed macaque suckling as a function offrame number for one cycle. Left:Movement in the anterior/posterior direction and jaw gape. Down is anterior, and up is posterior. Opening movement
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is downward on the gape plot. Right: Movement in the dorsal/ ventral direction and jaw gape. The dotted lines represent the frames illustrated in Figure 3. Scale bracket = 5 cm.
ple, but when that occurred the tongue was firmly sealed against the palate and no milk left the nipple. Our data showed that the tongue and mandible did not move as a unit in infant macaques and miniature pigs. Liquid entered the oral cavity only when the tongue was moving ventrally. This result strongly supports the idea that suction is the major mechanism for the acquisition of liquid during suck-
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Fig. 5. Series of frames from lateral view cineradiologic film of an infant macaque suckling, while pressure in the nipple was recorded. Anterior is on the right. Numbers are frame numbers, and each frame is 6.67 msec apart (film speed = 150 fps). The milk is shown as a stippled area in the oral cavity. The first three markers are numbered from right to left.
Fig. 6. Gape, movement of tongue markers, and change in pressure in bottle nipple as a function of frame number during macaque suckling. Down is dorsal movement, and up is ventral movement. Jaw opening and pressure decreases are downward, and jaw closing and pressure increases are upward. Numbers (tl-t3) correspond to markers numbered in Figure 5.
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(Herring and Scapino, ,731, and finally a squeezeback mechanism in primates (J. Palmer, JHMI, personal communication). The comparison of the results on infant suckling with known mechanisms of adult transport lead us to several evolutionary hypotheses that require further testing with additional species of mammals. The first suggests that initial acquisition of milk takes place as a negative pressure mechanism, as opposed to licking, expression, or other positive pressure mechanism, and all infant mammals use this mechanism during suckling, the act of procuring liquid from the teat. Second, this mechanism Differencesin suckling between infant probably arose as early as did suckling and is macaques and pigs related to the evolution of the mobility of the mamThe initial mechanisms of acquisition in the two malian tongue. Sucking exists in at least one monspecies is consistent with the operation of suction otreme without teats, the echidna (Griffths, '78). pumps. The ventral movement of the tongue is capa- Furthermore, as in adults, subsequent intraoral ble of causing the necessary drop in pressure in the transport in infants is more varied than the mechoral cavity to draw liquid out of the nipple, because anisms of acquisition. the posterior tongue contacts the soft palate and ACKNOWLEDGMENTS presumably forms a seal. The frothy appearance of the radio-opaque milk at this time is consistent We thank Ken Gordon, Susan Herring, David with bubbling and is therefore also consistent with Hertweck, Karen Hiiemae, Tina Rouse, and Jeff a negative pressure in the oral cavity. At the same Shultz for their assistance in this project. We also time, the pressure measured in the nipple was also acknowledge the assistance of the New England negative, but milk was flowing out of the nipple Regional Primate Research Center in providing us through a restricted orifice; the pressure must with the infant macaques. This work was supported therefore have been even lower in the oral cavity. by NIH grant DE-8697 to R.Z.G. and A.W.C. All the evidence therefore points to the production LITERATURE CITED of low pressure within the oral cavity. The subsequent transport mechanisms differed Ardran, G.M., and F.H. Kemp (1959) A correlation between in the two species. In pigs, a downward and forward sucking pressures and movement of the tongue. Acta Paediatr. 48:261-272. movement of the back of the tongue, which could create a lowered pressure, was associated with Ardran, G.M., F.H. Kemp, and J. Lind (1958a) A cineradiographic study of bottle feeding. Br. J. Radiol., 31:ll-22. movement of liquid through the pillars of the fau- Ardran, G.M., F.H. Kemp, and J. Lind (1958b) A cineradioces into the valleculae. The macaques, however, graphic study ofbreast feeding. Br. J. Radiol., 31:156-162. used a mechanism that closely resembled a mech- Bosma, J. (1967) Human infant oral function. In Symposium on Oral Sensation and Perception. J.F. Bosma, ed. C.C. anism used by adult macaques to transport either Thomas, Springfield, IL, pp. 98-110. well-masticated food (stage I1 transport; Franks et J. (1972) Form and function in the infant's mouth and al., '84)or liquid (J.Palmer, Johns Hopkins Medi- Bosma, pharynx. In Third Symposium on Oral Sensation and Percal Institutions, personal communication; German ception. J.F. Bosma, ed. C.C. Thomas, Springfield, IL, pp. 3-29. et al., unpublished data). Colley, J.R.T., and B. Creamer (1958) Sucking and swallowing infants. Br. Med. J.,2:422-423. A variety of mechanisms for acquisition and transport of liquid have been documented in adult Franks, H.A., R.Z. German, and A.W. Crompton (1984) Mechanism of intraoral transport in macaques. Am. J. Phys. mammals. Sucking (in pigs and primates) and lapAnthropol., 65:275-282. ping (in cats and opossums)are the primary mech- German, R.Z., S.A. Saxe, A.W. Crompton, and K.M. Hiiemae anisms of liquid acquisition (Gordon and Herring, (1989) Food transport through the anterior oral cavity in macaques. Am. J. Phys. Anthropol., 80:369-377. '86; Thexton and McGarrick '88; Hiiemae and Crompton, '85).Homologous mechanisms of trans- Gordon, K.R., and S.W. Herring (1986)Activity patterns within the genioglossus during suckling in domestic dogs and pigs: port include negative pressure in cats (Thexton and interspecific and intraspecific plasticity. Brain Behav. Evol., McGarrick, 'SS), posterior movement of the tongue 30:249-262. carrying liquid in opossums (Hiiemae and Cromp- Grifiths, M. (1978) The Biology of the Monotremes. Academic Press, New York. 367 pp. ton, '85),a pumping motion of the tongue in pigs ling in infant pigs and macaques. This conclusion is supported by the pressure transducer data obtained from the macaque feeding records, where reduced pressure in the nipple was recorded when milk left the nipple, and at no point were large increases in pressure recorded. This is entirely incompatible with any positive pressure or expression mechanism for suckling. However, this was an experimental situation using a bottle and therefore not equivalent to a maternal nursing situation. In the latter, maternal expression plays a role in the initial acquisition of milk.
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Hall, W.G., R. Hudson, and S.C. Brake (1988) Terminology for use in investigations of nursing and suckling. Dev. Psychobiol., 21 :89-91. Herring, S.W. (1985)The ontogeny ofmammalian mastication. Am. Zool., 25:339-349. Herring, S.W., and R.P. Scapino (1973) Physiology of feeding in miniature pigs. J. Morphol., 141 :427-460. Hiiemae, K.M., and A.W. Crompton (1985) Mastication, food transport and swallowing. In: Functional Vertebrate Morphology. M. Hildebrand, D.M. Bramble, K.F. Liem, and D.B. Wake, eds. Belknap Press of Harvard University Press, Cambridge, MA. pp. 262-290. Hylander, W.L., Johnson, K.R., and Crompton, A.W. (1987) Loading patterns and jaw movements during mastication. In:
Maccaca fascicularis: A bone-strain, electromyographic, and cineradiographic analysis. Am. J . Phys. Anthropol., 72: 287-314. Moyers, R.E. (1964) The infantile swallow. Eur. Orthod. SOC., 40:180-187. Smith, W.L., A. Erenberg, A. Nowak (1988) Imaging evaluation of the human nipple during breast-feeding. AJDC, 142:76-78. Thexton, A.J., and J.D. McGarrick (1988) Tongue movement of the cat during lapping. Arch. Oral Biol., 33:331-339. Weber, F., M.W. Woolridge, and J.D. Baum (1986) An ultrasonographic study of the organization of sucking and swallowing by newborn infants. Dev. Med. Child Neurol., 28: 19-24.
