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.

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.

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.

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.

Determinants of rhythm and rate in suckling.

Suckling was studied in infant miniature pigs to determine (a) the necessary stimulus for eliciting rhythmic behavior and (b) whether the rhythm of the feeding movements could be entrained with a rhythmic pulsed delivery of milk. The animals fed on an automated milk delivery system, which supplied pulses of milk either at fixed, predetermined rates or on demand. The rhythm of the suckling response was quantified from the teat pressure changes produced by the animal, which were highly correlated with jaw movement. Suckling frequency was measured as the dominant frequency in the teat pressure wave, determined by fast Fourier transform. When each animal was allowed to determine its own rate of milk delivery, the preferred frequency of suckling was approximately 3.8 Hz. When animals attempted to suckle on the teat but milk was not delivered, suckling was erratic and arrhythmic. The first aliquot of milk delivered to the animal elicited rhythmic suckling at approximately 4.6 Hz, which was maintained when milk was delivered at a range of fixed rates (0.2-0.56 Hz) an order of magnitude below the preferred suckling frequency. When milk was delivered at a fixed rate (2.0-5.6 Hz) close to the animals' preferred rhythm, suckling proceeded at a lower frequency (3.9 Hz) than when the milk was delivered at the much lower rate. However, variation in the delivery rate (2.0-5.6 Hz) did not cause a significant difference in the suckling frequency. These findings provided evidence against entrainment. The higher suckling frequency elicited by the slower delivery rate was suggestive of a negative feedback loop; in the infant/sow relationship, such a mechanism could favor a particular volume delivery per unit time.

A randomisation method for discriminating between signal and noise recordings of rhythmic electromyographic activity.

A method is described which enables an amplitude threshold level to be derived from previously recorded rhythmic electromyographic activity, or from other rhythmic physiological data, so that the signal and noise components can be best separated. The method utilises randomisation of the original data and a non-parametric measure of the resultant information loss; this avoids any assumptions about the amplitude density function. The probability that the division into signal and noise is no better than chance may also be calculated.

Coordination between respiration and deglutition in a preterm infant mammal, Sus scrofa.

In adult mammals, the path of a swallowed bolus of solid food crosses the laryngeal opening, so that coordination between respiration and deglutition is critical for airway protection. The nature of such coordination in preterm, low-birth-weight infants with immature nervous systems, is not clear. Using preterm pigs as a model, two measures of respiration were recorded and then coordinated with a high-resolution cineradiographic record of swallowing. Swallows, divided into three distinct events, began before inhalation ended, but expiration did not start until after the milk had passed around the laryngeal opening. These results support the idea that a high degree of coordination between swallowing and respiration exists in preterm infant pigs, although other aspects of the nervous system have not fully matured.

Latency of the jaw-opening reflex in the premature, preweaning and adolescent pig (hanford strain miniature pig, Sus scrofa).

The jaw-opening (digastric) reflex was elicited by electrical stimulation of oral mucosa in miniature pigs (Sus scrofa) varying in age from 5 days premature to 101 days post-term. The latency of reflex electromyographic activity varied between 12-14 ms in the most immature animals and 9-11 ms in the oldest animals. The very long-latency digastric responses found in the immature young of nesting mammals were not seen in the relatively precocious young of this species.

The electromyographic activities of jaw and hyoid musculature in different ingestive behaviours in the cat.

Electromyographic (EMG) activity in the muscles moving the jaw, hyoid and tongue of the cat was recorded during the intake of solid and liquid foods; the nature of the movements of the jaw, hyoid, tongue and food were recorded and identified cineradiographically. Synergy was evident in muscles with similar anatomical orientation. However, most muscles were activated more than once during each jaw cycle and some of these additional periods of activation occurred at times not predicted by the anatomical arrangement of the muscles. The pattern of EMG activity was the same during all lapping cycles (excluding lap/swallow cycles) but was characteristically different from that occurring during the ingestion of solid food. With solid food the EMG pattern changed during the course of the ingestive sequence and was characteristic for each of the four successively different types of jaw cycle, i.e. transport cycles moving food back from the front of the mouth to the cheek teeth, chewing cycles, transport cycles moving food through the fauces and, following the accumulation of a bolus in the vallecula, swallowing cycles. In these data, provided that the EMG activities of a complete ingestive sequence were available (from food pick-up to swallow), the cycle type could be identified from the intracycle timings and amplitudes of the bursts of EMG activity occurring in the fibres of temporal, posterior digastric and geniohyoid muscles alone. Two variable components of the cyclical EMG pattern could be identified, one relating to tongue movement, the other to jaw movement.

Recovery of the jaw-opening reflex after lesions of the lingual nerve in the rat.

In three groups of rats, lesions were produced in the right lingual nerves near the base of the tongue; the three types of injury inflicted (cryogenic, crush, and stretch) are reputed to spare the epineurium but produce different degrees of intraneural damage. In regular assessments of recovery, an electrical stimulus (sufficient to elicit the jaw-opening reflex) was applied to either side of the tongue in turn; the amplitude of the reflex was measured as the isometric force of jaw opening. The size of the reflex response to stimulation of the injured side was followed up to 4 months post-lesion, with the response elicited from the control side used as the reference level. The reflex was absent when the experimental side was stimulated immediately after creation of a lesion; the first sign of reflex recovery was found at about 15 days post-operative. Subsequently, in 84% of the animals, the reflex activity elicited from the experimental side increased until it exceeded that elicited from the reference side; this relative hyperreflexia started 1-4 months post-lesion and had a highly variable duration. There was no difference in the incidence, latency, or duration of the hyperreflexia following any of the three types of lesion. The hyperreflexia found in this study is not readily explained by existing hypotheses of the mechanisms underlying post-lesion hyperesthesia or central neuronal hyperexcitability.

Mastication and swallowing: an overview.

The cycles of jaw and tongue movement during feeding produce not only the breakage of food but its intra-oral transport; which activity predominates depends upon the physical characteristics of the food. When hard food is eaten and tooth-food-tooth contact is made during jaw closure, the velocity of closing is suddenly reduced, producing two clearly different phases of closure; during the second phase the activity of the jaw closing muscles is much increased. Conversely, in cycles with a mainly transport function (eating soft food), the antero-posterior movements of the tongue are much greater; this alters the time and rate at which the jaw opens. The pattern of jaw movement during closing and during opening consequently varies with food consistency. The evidence suggests that sensory input controls the form of the cyclical tongue and jaw movements. However the basic plan of movement is produced by the activity of a brainstem pattern generator which receives input from both cerebro-cortical and peripheral sources. The swallow that occurs in normal feeding consists of the equivalent of the classical second stage of swallowing inserted into the occlusal or initial jaw opening phase of an otherwise standard cycle. Although leakage of traces of food or saliva into the vallecula appears to be a peripheral sensory input of major importance in inducing such a swallow, the execution of the swallow is due to a pattern generator in the brainstem.

The mechanism of suckling in two species of infant mammal: miniature pigs and long-tailed macaques.

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 frames/sec). 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.

Effect of sensory input from the tongue on jaw movement in normal feeding in the opossum.

Opossums were presented with solid and liquid foods. The movements of the jaw and tongue were recorded cineradiographically together with recordings of the EMG activity in muscles opening the jaw and moving the base of the tongue (hyoid). The jaw opening in each cycle was in two stages--01 and 02; 01 had a constant amplitude irrespective of the food ingested. Ingestion of liquid (which involved continuous accumulation of a liquid bolus in the valleculae prior to swallowing) was associated with cycles of oral movement in which 02 was small; tongue retraction was associated with this opening. In contrast, solid and semisolid food ingestion was associated with large angles of jaw opening in 02 that also coincided with the tongue retraction. In this latter case a characteristic pattern of EMG activity, in which all the muscles moving the hyoid were simultaneously active, was added to the pattern seen in lapping; this additional activity had an EMG pattern that was consistent with a jaw opening reflex. The findings contrast with other reports that the jaw opening reflex is suppressed in mastication. Experimentally induced tongue contact with a variety of solid surfaces during lapping (an activity involving accumulation of a liquid bolus in the valleculae) induced neither increased jaw opening nor the additional EMG pattern. However, in situations when there was no bolus in the valleculae, additional jaw opening activity was elicited when the tongue contracted solids intra- or extra-orally. It is suggested that the ability of sensory input, from the anterior tongue, to elicit a jaw opening reflex and to change the type of jaw/tongue cycle was dependent upon the extent of bolus accumulation in the valleculae and therefore indirectly upon the consistency of the food.

Tongue movement in the cat during the intake of solid food.

During feeding, solid food in the mouth progresses towards the pharynx during transport cycles, but it does not do so in chewing cycles. In the cat, the two cycle types differ with respect to jaw and hyoid movement but it is not known if, or how, any differences in tongue movement arise. This study sought to quantify the tongue movements in the different cycle types. Radio-opaque markers were placed in the midline of the cat tongue. While the animals ate solid food, the marker movements (viewed in the sagittal plane) were recorded by cine-radiography. The movement of the tongue relative to the palate could be split into three components derived from (a) movement of the mandible, (b) movement of the hyoid, (c) movement produced within the body of the tongue itself. Although the differences in jaw movement between transport cycles and chewing cycles produced some differences in tongue movement relative to the palate, differences in the movements produced within the tongue itself were of greater significance. Transport cycles were characterized by rhythmic extensions of the tongue; the protracted tongue was about 60% longer than the retracted tongue. In chewing cycles, rhythmic length changes (viewed in the sagittal plane) were reduced and could be partly explained by an associated rotation of the tongue. In transport cycles the tongue, with food on it, was elevated to the palatal rugae as it extended, but when it shortened it was out of contact with the palate. It is suggested that these movements form the basis of a transport mechanism.

Rhythmic digastric activity in the naloxone-treated decerebrate rabbit pup.

In decerebrate rabbit pups (greater than 1 and less than 7 days postnatal), exhibiting a digastric reflex with a latency of 20-25 ms, the administration of naloxone was followed by depression of the 25 ms latency reflex and the appearance of rhythmic EMG activity (10-18 Hz) with a latency of 45-90 ms. Such a frequency is not consistent with the normal rhythms of feeding but may relate to tooth grinding behaviour. In contrast, spontaneous rhythmic activity occurring after naloxone had a lower frequency, consistent with the normal rhythm of feeding.

Pharmacologically induced changes in the latency of digastric reflexes in 1-7 day old rabbits.

1. The naturally occurring change in latency of the digastric reflex from long (40-70 msec) to short (15-35 msec) in the first week of life was studied in rabbits using drugs known to affect GABAergic and glycinergic transmission. 2. Usually the long or the short latency reflex response appeared alone but after strychnine both appeared together. 3. The long latency responses were favoured by the GABA blockers bicuculline and picrotoxin; periodically rhythmic activity was also elicited. 4. The short latency responses were favoured by the GABA agonists pentobarbitone and diazepam.

Tongue movement of the cat during lapping.

The movements of radio-opaque markers in the tongue were recorded cine-radiographically. The animals were fed bariumized milk, with or without a thickening agent to increase the viscosity. The movements of the tongue markers relative to the palate were roughly elliptical and resulted from the summation of at least three components: simple movement produced within the tongue, movement imposed on the tongue by hyoid movement and movement imposed on the tongue-hyoid complex by jaw movement. Relative to the palate, the anterior markers protracted high and retracted low, whereas the posterior markers did the reverse. The movements could be explained as having utility for the intra-oral transport of liquid by two mechanisms. The transported liquids then accumulated between the soft palate and the tongue prior to swallowing. The swallow appeared as a brief interruption in the jaw-opening phase of otherwise standard lapping cycles.