Cetacean tongue mobility and function: A comparative review.

Cetaceans are atypical mammals whose tongues often depart from the typical (basal) mammalian condition in structure, mobility, and function. Their tongues are dynamic, innovative multipurpose tools that include the world's largest muscular structures. These changes reflect the evolutionary history of cetaceans' secondary adaptation to a fully aquatic environment. Cetacean tongues play no role in mastication and apparently a greatly reduced role in nursing (mainly channeling milk ingestion), two hallmarks of Mammalia. Cetacean tongues are not involved in drinking, breathing, vocalizing, and other non-feeding activities; they evidently play no or little role in taste reception. Although cetaceans do not masticate or otherwise process food, their tongues retain key roles in food ingestion, transport, securing/positioning, and swallowing, though by different means than most mammals. This is due to cetaceans' aquatic habitat, which in turn altered their anatomy (e.g., the intranarial larynx and consequent soft palate alteration). Odontocetes ingest prey via raptorial biting or tongue-generated suction. Odontocete tongues expel water and possibly uncover benthic prey via hydraulic jetting. Mysticete tongues play crucial roles driving ram, suction, or lunge ingestion for filter feeding. The uniquely flaccid rorqual tongue, not a constant volume hydrostat (as in all other mammalian tongues), invaginates into a balloon-like pouch to temporarily hold engulfed water. Mysticete tongues also create hydrodynamic flow regimes and hydraulic forces for baleen filtration, and possibly for cleaning baleen. Cetacean tongues lost or modified much of the mobility and function of generic mammal tongues, but took on noteworthy morphological changes by evolving to accomplish new tasks.

Animal Models for Dysphagia Studies: What Have We Learnt So Far.

Research using animal models has contributed significantly to realizing the goal of understanding dysfunction and improving the care of patients who suffer from dysphagia. But why should other researchers and the clinicians who see patients day in and day out care about this work? Results from studies of animal models have the potential to change and grow how we think about dysphagia research and practice in general, well beyond applying specific results to human studies. Animal research provides two key contributions to our understanding of dysphagia. The first is a more complete characterization of the physiology of both normal and pathological swallow than is possible in human subjects. The second is suggesting of specific, physiological, targets for development and testing of treatment interventions to improve dysphagia outcomes.

EMG activity in hyoid muscles during pig suckling.

Infant suckling is a complex behavior that includes cycles of rhythmic sucking as well as intermittent swallows. This behavior has three cycle types: 1) suck cycles, when milk is obtained from the teat and moved posteriorly into the valleculae in the oropharynx; 2) suck-swallow cycles, which include both a rhythmic suck and a pharyngeal swallow, where milk is moved out of the valleculae, past the larynx, and into the esophagus; and 3) postswallow suck cycles, immediately following the suck-swallow cycles. Because muscles controlling these behaviors are active in all three types of cycles, we tested the hypothesis that different patterns of electromyographic (EMG) activity in the mylohyoid, hyoglossus, stylohyoid, and thyrohyoid muscles of the pig characterized each cycle type. Anterior mylohyoid EMG activity occurred regularly in every cycle and was used as a cycle marker. Thyrohyoid activity, indicating the pharyngeal swallow, was immediately preceded by increased stylohyoid and hyoglossus activity; it divided the suck-swallow cycle into two phases. Timed from the onset of the suck-swallow cycle, the first phase had a relatively fixed duration while the duration of the second phase, timed from the thyrohyoid, varied directly with cycle duration. In short-duration cycles, the second phase could have a zero duration so that thyrohyoid activity extended into the postswallow cycle. In such cycles, all swallowing activity that occurred after the thyrohyoid EMG and was associated with bolus passage through the pharynx fell into the postswallow cycle. These data suggest that while the activity of some muscles, innervated by trigeminal and cervical plexus nerves, may be time locked to the cycle onset in swallowing, the cycle period itself is not. The postswallow cycle consequently contains variable amounts of pharyngeal swallowing EMG activity. The results exemplify the complexity of the relationship between rhythmic sucking and the swallow.

How dogs lap: ingestion and intraoral transport in Canis familiaris.

It has recently been suggested that the mechanism for lifting liquid from a bowl into the oral cavity during lapping is fundamentally different in cats and dogs: cats use adhesion of liquid to the tongue tip while dogs 'scoop' with their backwardly curled tongue. High-speed light videos and X-ray videos show that on the contrary, both cats and dogs use the mechanism of adhesion. Liquid is transported through the oral cavity to the oesophagus, against gravity, on the surface of the tongue as it is drawn upwards, then a tight contact between the tongue surface and palatal rugae traps liquid and prevents its falling out as the tongue is protruded. At least three cycles are needed for intraoral transport of liquid in the dog.

Regional differences in length change and electromyographic heterogeneity in sternohyoid muscle during infant mammalian swallowing.

A complex sling of muscles moves and stabilizes the hyoid bone during many mammalian behaviors. One muscle in this sling, the sternohyoid, is recruited during food acquisition, processing, and swallowing, and also during nonfeeding behaviors. We used synchronous sonomicrometry and electromyography to investigate regional (intramuscular) changes in length and electromyographic (EMG) activity of the sternohyoid during swallowing in the infant pig. The simple straplike architecture of the sternohyoid led us to hypothesize that limited regional variation in length and muscle activity would be present. We found statistically significant regional differences in EMG activity, and, with respect to length dynamics, the sternohyoid did not behave homogeneously during swallowing. The midbelly region typically shortened while the anterior and posterior regions lengthened, although in a minority of swallows (12.5%) the midbelly lengthened simultaneously with the end-regions. Despite its nonpennate architecture and evolutionarily conservative innervation, the mammalian sternohyoid appears to contain previously unrecognized populations of regionally specialized motor units. It also displays differential contraction patterns, very similar to the sternohyoid of nonmammalian vertebrates.

Integration of the reflex pharyngeal swallow into rhythmic oral activity in a neurologically intact pig model.

Mammalian swallowing involves the coordinated and sequential activity of many oropharyngeal muscles. Using synchronous electromyography (EMG) and videofluorography, we recorded the pattern of EMG activity for 12 muscles during swallowing in neurologically intact suckling pigs. We tested the hypothesis that this EMG pattern corresponded to the established pattern of activity for the isolated, reflexive pharyngeal swallow of the decerebrate infant pig. The EMG activity associated with the normal swallow of the intact animal had two components: a staggered pattern of single EMG bursts that were prominent in the stylohyoid, thyrohyoid, cricothyroid, and omohyoid muscles and double bursts of activity in some muscles, including geniohyoid and genioglossus, with the same underlying periodicity as suckling. Most of the staggered activity pattern, a linear sequence of progressively delayed activities in different muscles, was not statistically different from that previously found in the reflexive pharyngeal swallow of the decerebrate. However, not all components of the linear sequence of the reflexive swallow were inserted unchanged into the intact swallow. Some components appeared to be delayed or advanced, bringing them into phase with the underlying rhythmic activity. The difference between swallows of intact and of decerebrate animals was not solely due to the presence of rhythmic activity in the former. The timing of some EMG activities in intact animals also differed from the same activities in the few decerebrates that exhibited rhythmic tongue and jaw activity. These results suggest cerebral function influences the EMG pattern of the pharyngeal swallow, which has traditionally been considered a purely reflex pattern.

Impact of rhythmic oral activity on the timing of muscle activation in the swallow of the decerebrate pig.

The pharyngeal swallow can be elicited as an isolated event but, in normal animals, it occurs within the context of rhythmic tongue and jaw movement (RTJM). The response includes activation of the multifunctional geniohyoid muscle, which can either protract the hyoid or assist jaw opening; in conscious nonprimate mammals, two bursts of geniohyoid EMG activity (GHemg) occur in swallow cycles at times consistent with these two actions. However, during experimentally elicited pharyngeal swallows, GHemg classically occurs at the same time as hyoglossus and mylohyoid activity (short latency response) but, when the swallow is elicited in the decerebrate in the absence of RTJM, GHemg occurs later in the swallow (long latency response). We tested the hypothesis that it was not influences from higher centers but a brain stem mechanism, associated with RTJM, which caused GHemg to occur earlier in the swallow. In 38 decerebrate piglets, RTJM occurred sporadically in seven animals. Before RTJM, GHemg had a long latency, but, during RTJM, swallow related GHemg occurred synchronously with activity in hyoglossus and mylohyoid, early in the swallow. Both early and late responses were present during the changeover period. During this changeover period, duplicate electrodes in the geniohyoid could individually detect either the early or the late burst in the same swallow. This suggested that two sets of geniohyoid task units existed that were potentially active in the swallow and that they were differentially facilitated or inhibited depending on the presence or absence of rhythmic activity originating in the brain stem.

Variation in EMG activity: a hierarchical approach.

Recordings of naturally occurring Electromyographic (EMG) signals are variable. One of the first formal and successful attempts to quantify variation in EMG signals was Shaffer and Lauder's (1985) study examining several levels of variation but not within muscle. The goal of the current study was to quantify the variation that exists at different levels, using more detailed measures of EMG activity than did Shaffer and Lauder (1985). The importance of accounting for different levels of variation in an EMG study is both biological and statistical. Signal variation within the same muscle for a stereotyped action suggests that each recording represents a sample drawn from a pool of a large number of motor units that, while biologically functioning in an integrated fashion, showed statistical variation. Different levels of variation for different muscles could be related to different functions or different tasks of those muscles. The statistical impact of unaccounted or inappropriately analyzed variation can lead to false rejection (type I error) or false acceptance (type II error) of the null hypothesis. Type II errors occur because such variation will accrue to the error, reducing power, and producing an artificially low F-value. Type I errors are associated with pseudoreplication, in which the replicated units are not truly independent, thereby leading to inflated degrees of freedom, and an underestimate of the error mean square. To address these problems, we used a repeated measures, nested multifactor model to measure the relative contribution of different hierarchical levels of variation to the total variation in EMG signals during swallowing. We found that variation at all levels, among electrodes in the same muscle, in sequences of the same animal, and among individuals and between differently named muscles, was significant. These findings suggest that a single intramuscular electrode, recording from a limited sample of the motor units, cannot be relied upon to characterize the activity of an entire muscle. Furthermore, the use of both a repeated-measures model, to avoid pseudoreplication, and a nested model, to account for variation, is critical for a correct testing of biological hypotheses about differences in EMG signals.

Control of jaw movements in two species of macropodines (Macropus eugenii and Macropus rufus).

The masticatory motor patterns of three tammar wallabies and two red kangaroos were determined by analyzing the pattern of electromyographic (EMG) activity of the jaw adductors and correlating it with lower jaw movements, as recorded by digital video and videoradiography. Transverse jaw movements were limited by the width of the upper incisal arcade. Molars engaged in food breakdown during two distinct occlusal phases characterized by abrupt changes in the direction of working-side hemimandible movement. Separate orthal (Phase I) and transverse (Phase II) trajectories were observed. The working-side lower jaw initially was drawn laterally by the balancing-side medial pterygoid and then orthally by overlapping activity in the balancing- and working-side temporalis and the balancing-side superficial masseter and medial pterygoid. Transverse movement occurred principally via the working-side medial pterygoid and superficial masseter. This pattern contrasted to that of placental herbivores, which are known to break down food when they move the working-side lower jaw transversely along a relatively longer linear path without changing direction during the power stroke. The placental trajectory results from overlapping activity in the working- and balancing-side adductor muscles, suggesting that macropods and placental herbivores have modified the primitive masticatory motor pattern in different ways.

Electromyographic activity during the reflex pharyngeal swallow in the pig: Doty and Bosma (1956) revisited.

The currently accepted description of the pattern of electromyographic (EMG) activity in the pharyngeal swallow is that reported by Doty and Bosma in 1956; however, those authors describe high levels of intramuscle and of interindividual EMG variation. We reinvestigated this pattern, testing two hypotheses concerning EMG variation: 1) that it could be reduced with modern methodology and 2) that it could be explained by selective detection of different types of motor units. In eight decerebrate infant pigs, we elicited radiographically verified pharyngeal swallows and recorded EMG activity from a total of 16 muscles. Synchronization signals from the video-radiographic system allowed the EMG activity associated with each swallow to be aligned directly with epiglottal movement. The movements were highly stereotyped, but the recorded EMG signals were variable at both the intramuscle and interanimal level. During swallowing, some muscles subserved multiple functions and contained different task units; there were also intramuscle differences in EMG latencies. In this situation, statistical methods were essential to characterize the overall patterns of EMG activity. The statistically derived multimuscle pattern approximated to the classical description by Doty and Bosma (Doty RW, Bosma JF. J Neurophysiol 19: 44-60, 1956) with a leading complex of muscle activities. However, the mylohyoid was not active earlier than other muscles, and the geniohyoid muscle was not part of the leading complex. Some muscles, classically considered inactive, were active during the pharyngeal swallow.

Correlation between intraoral pressures and tongue movements in the suckling pig.

The objective was to clarify the relationship between tongue movements during suckling and the pressures in different parts of the oral cavity. A modified teat allowed a miniature pressure transducer to be passed through into the mouth. Intraoral pressures were recorded in piglets suckling on the teat attached (1) to a non-vented bottle or (2) to an automated milk delivery system. The movements of the tongue, of the milk and the transducer position were recorded by cine-radiography. In both modes of feeding, waves of elevation on the tongue moved in a pharyngeal direction and rose to contact the mid-posterior palate. Each wave corresponded to a jaw (suck) cycle in which milk was moved into and through the oral cavity. After each wave passed the transducer in the anterior part of the mouth, cyclical negative pressures were recorded. In bottle feeding, the intraoral pressure fluctuations (+/-2 mmHg) occurred against a background of a gradually developing negative pressure but, when feeding on the automatic delivery system, the same or smaller fluctuations occurred as changes from atmospheric pressure. Where the elevations contacted the mid-posterior palate in each cycle, a seal was formed (contact pressure >40 mmHg), so producing two functional antero-posterior compartments within the mouth; in these compartments pressures were generated independently. With the transducer in the valleculae, no general increase in pressure was recorded as milk accumulated there in each suck cycle but large positive pressures were recorded during the less frequent cycles when the vallecular space was emptied.

The role of animal models in understanding feeding behavior in infants.

The common evolutionary history humans share with mammals provides us with a solid basis for understanding normal oropharyngeal anatomy and functions. Physiologically, feeding is a cycle of neurophysiologic activity, where sensory input travels to the CNS which sends motor signals out to the periphery. Research with animal models is valuable because it is possible to disrupt this cycle, and develop predictive models on the causal basis of deviation from normal. Based on work with animal models, normal mammalian infant feeding behavior consists of the tongue functioning as a pump. First, the tongue assists in acquisition of milk from the nipple into the oral cavity, and then it pumps milk from the oral cavity into the valleculae prior to the pharyngeal swallow. Starting with this basic model, feeding in infant pigs was manipulated to determine the impact of variation in sensory input on behavioral output. One set of experiments suggested that chemo- or liquid sensation, in the form of milk is necessary to elicit continuing rhythmic activity. However, the rates of rhythmic suckling are intrinsic to an animal, and variation in rate cannot be entrained. Another set showed that initiation of the swallow does not purely depend on the volume of milk delivered, but also on the sensory stimulation at the mouth. These results support the idea that feeding behavior involves complex sensory integration.

Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs.

How bones respond dynamically to mechanical loading through changes in shape and structure is poorly understood, particularly with respect to variations between bones. Structurally, cortical bones adapt in vivo to their mechanical environments primarily by modulating two processes, modeling and Haversian remodeling. Modeling, defined here as the addition of new bone, may occur in response to mechanical stimuli by altering bone shape or size through growth. Haversian remodeling is thought to be an adaptation to repair microcracks or prevent microcrack propagation. Here, we examine whether cortical bone in sheep limbs modulates periosteal modeling and Haversian remodeling to optimize strength relative to mass in hind-limb midshafts in response to moderate levels of exercise at different growth stages. Histomorphometry was used to compare rates of periosteal growth and Haversian remodeling in exercised and sedentary treatment groups of juvenile, subadult and young adult sheep. In vivo strain data were also collected for the tibia and metatarsal midshafts of juvenile sheep. The results suggest that limb bones initially optimize responses to loading according to the varying power requirements associated with adding mass at different locations. In juveniles, exercise induces higher rates of periosteal modeling in proximal midshafts and higher rates of Haversian remodeling in distal midshafts. Consequently, distal element midshafts experience higher strains and, presumably, have lower safety factors. As animals age, periosteal modeling rates decline and Haversian remodeling rates increase, but moderate levels of mechanical loading stimulate neither process significantly.

A new mammaliaform from the early Jurassic and evolution of mammalian characteristics.

A fossil from the Early Jurassic (Sinemurian, approximately 195 million years ago) represents a new lineage of mammaliaforms, the extinct groups more closely related to the living mammals than to nonmammaliaform cynodonts. It has an enlarged cranial cavity, but no postdentary trough on the mandible, indicating separation of the middle ear bones from the mandible. This extends the earliest record of these crucial mammalian features by some 45 million years and suggests that separation of the middle ear bones from the mandible and the expanded brain vault could be correlated. It shows that several key mammalian evolutionary innovations in the ear region, the temporomandibular joint, and the brain vault evolved incrementally through mammaliaform evolution and long before the differentiation of the living mammal groups. With an estimated body weight of only 2 grams, its coexistence with other larger mammaliaforms with similar "triconodont-like" teeth for insectivory within the same fauna suggests a great trophic diversity within the mammaliaform insectivore feeding guild, as inferred from the range of body sizes.

Why fuse the mandibular symphysis? A comparative analysis.

Fused symphyses, which evolved independently in several mammalian taxa, including anthropoids, are stiffer and stronger than unfused symphyses. This paper tests the hypothesis that orientations of tooth movements during occlusion are the primary basis for variations in symphyseal fusion. Mammals whose teeth have primarily dorsally oriented occlusal trajectories and/or rotate their mandibles during occlusion will not benefit from symphyseal fusion because it prevents independent mandibular movements and because unfused symphyses transfer dorsally oriented forces with equal efficiency; mammals with predominantly transverse power strokes are predicted to benefit from symphyseal fusion or greatly restricted mediolateral movement at the symphysis in order to increase force transfer efficiency across the symphysis in the transverse plane. These hypotheses are tested with comparative data on symphyseal and occlusal morphology in several mammals, and with kinematic and EMG analyses of mastication in opossums (Didelphis virginiana) and goats (Capra hircus) that are compared with published data on chewing in primates. Among mammals, symphyseal fusion or a morphology that greatly restricts movement correlates significantly with occlusal orientation: species with more transversely oriented occlusal planes tend to have fused symphyses. The ratio of working- to balancing-side adductor muscle force in goats and opossums is close to 1:1, as in macaques, but goats and opossums have mandibles that rotate independently during occlusion, and have predominantly vertically oriented tooth movements during the power stroke. Symphyseal fusion is therefore most likely an adaptation for increasing the efficiency of transfer of transversely oriented occlusal forces in mammals whose mandibles do not rotate independently during the power stroke.

Regulation of Tiam1 nucleotide exchange activity by pleckstrin domain binding ligands.

Rho family GTPases play roles in cytoskeletal organization and cellular transformation. Tiam1 is a member of the Dbl family of guanine nucleotide exchange factors that activate Rho family GTPases. These exchange factors have in common a catalytic Dbl homology and adjacent pleckstrin homology domain. Previous structural studies suggest that the pleckstrin domain, a putative phosphoinositide-binding site, may serve a regulatory function. We identified ascorbyl stearate as a compound that binds to the pleckstrin domain of p120 Ras GTPase-activating protein. Furthermore, ascorbyl stearate appears to be a general pleckstrin domain ligand, perhaps by mimicking an endogenous amphiphilic ligand. Tiam1 nucleotide exchange activity was greatly stimulated by ascorbyl stearate. Certain phosphoinositides also stimulated Tiam1 activity but were less potent than ascorbyl stearate. Tiam1 contains an additional N-terminal pleckstrin domain, but only the C-terminal pleckstrin domain was required for activation. Our results suggest that the pleckstrin domains of Dbl-type proteins may not only be involved in subcellular localization but may also directly regulate the nucleotide exchange activity of an associated Dbl homology domain. In addition, this paper introduces ascorbyl stearate as a pleckstrin domain ligand that can modulate the activity of certain pleckstrin domain-containing proteins.

The coordination and interaction between respiration and deglutition in young pigs.

The anatomical pathways for inspired air and ingested food cross in the pharynx of mammals, implying that breathing and swallowing must be separated either in space or in time. In this study we investigated the time relationship between swallowing and respiration in young pigs, as a model for suckling mammals. Despite the high morphological position of the larynx in young mammals, allowing liquid to pass in food channels lateral to the larynx, respiration and swallowing are not wholly independent events. Although, when suckling on a veterinary teat, the swallows occurred at various points in the respiratory cycle, there was always a period of apnea associated with the swallow. Finally, an increase in the viscosity of the milk altered this coordination, changing respiratory cycle length and also restricting the relative rate at which swallows occurred in some parts of the respiratory cycle. These results suggest that the subsequent changes in respiratory activity at weaning, associated with passage of a solid bolus over the larynx, is preceded by the ability of the animal to alter coordination between respiration and swallowing for a liquid bolus.

Transition from suckling to drinking at weaning: a kinematic and electromyographic study in miniature pigs.

The movements of the tongue, hyoid, and jaw were recorded cineradiographically in preweaning pigs as they suckled bariumized milk from a veterinary teat or drank it from a bowl. The movements were quantified by measuring the X, Y coordinates of radioopaque markers embedded in the tongue and attached to both jaws and to the hyoid. EMG activity in masseter, anterior digastric, geniohyoid, genioglossus, hyoglossus, sternohyoid, stylohyoid, and omohyoid muscles was recorded synchronously with cineradiography at 100 frames/sec. In both suckling and drinking, the movements were characterized by minimal movements of the jaw and hyoid but extensive movements of the tongue. In suckling, the movements were largely confined to the midposterior part of the tongue. A seal was formed between the posterior tongue and soft palate while a depression formed in the mid-tongue; this was associated with fluid moving into the depression probably because of a reduced intraoral pressure. The depression was associated with increased EMG activity in the genioglossus muscle and overlapping activity in digastric, geniohyoid, hyoglossus, and sternohyoid muscles. In drinking cycles, significant movement occurred in all parts of the tongue; milk ingestion was associated with tongue movements that combined elements characteristic both of suckling (mid-tongue depression with a posterior seal) and of lapping (extensive anteroposterior movements within the tongue itself). In drinking, compared to suckling, there was a major reduction in EMG activity in masseter, digastric, geniohyoid, and sternohyoid muscles. After milk had accumulated in the valleculae, swallows usually occurred in every other cycle during suckling and in every third or fourth cycle during drinking. The emptying of the valleculae was an event that was embedded in the early jaw-opening phase of an otherwise normal suckling or drinking cycle. Emptying of the valleculae was associated with posteriorly directed movement of the back of the tongue and increased EMG activity in hyoglossus, styloglossus, and omohyoid muscles. No differences were noted in the kinematics associated with swallowing in the two activities, but, in the normalized and averaged EMG data, there were significant differences in the timing of genioglossus activity and in the relative balance of hyoglossal and stylohyoid activity.