Primate experiments on oral sensation

Egil P. Harvold, D.D.S., Ph.D., Karin Vargervik, D.D.S., and George Chierici, D.D.S.; Primate experiments on oral sensation and dental malocclusions. Am J Orthodontics, Vol. 63, Number 5 May 1973.

From the Section of Orofacial Anomalies, University of California, San Francisco, Calif. This study is supported by United States Public Health Service Grant DE-02739.

Abstract:
In contrast to the vast array of metric observations on human skulls during the growth period, there is a paucity of information regarding the physiologic correlates: the factors controlling growth at the mandibular condyles, the pressure and tension systems determining bone apposition and modeling on the surfaces of the jaws, and the functional systems regulating tonus in the musculature which positions the mandible relative to the maxilla.

Pilot studies1 have demonstrated that the rhesus monkey can serve as an experimental model in research on the etiology of dental malocclusions. With the use of this model, it has been possible to test certain hypotheses on the interrelationships of muscle function, skeletal form, and dental malocclusion by inductive inference rather than by surveillance. Alternative hypotheses are
formulated and subjected to testing.

Recent experiments have been designed to test certain theories regarding functional factors which affect the suspension of the mandible as well as the position of the teeth. The relationship of factors which influence the establishment of dental occlusion is illustrated in Fig. 1, in which A and B represent the maxilla and the mandible; C, the tongue; D and E, the muscles suspending
the jaw; and P and G, the erupting or extruding teeth.

The model illustrates the possible effects of changes in the relative tonus of the muscle groups (D and E) upon the distance between the jaws (A and B) as well as the space available for the tongue (C) and the extruding teeth (P and G). The question becomes: Can significant changes in muscle tonus occur in response to common environmental stimuli ? Obviously, strong orthodontic
forces, muscle exercises, and selective destruction of neuromuscular components can produce dramatic morphologic changes. 2-5 However, observations based on such conditions are not relevant to the problems discussed in this article.

Our findings have demonstrated that certain oral sensory inputs provide long-term, consistent stimuli sufficient to influence orofacial morphogenesis. In these studies the sensory inputs were tactile. The question remained: Would other forms of sensory perception also influence morphogenesis? Therefore, an experiment was planned to test the effects of other sensations upon the tonus in the jaw-suspension system. Two hypotheses were developed: (1) A change in relative tonus in the muscle groups suspending the jaws (D and E) alters the distance between the jaws (A and B, Fig. 1). (2) A break in the contact between the tongue and the dentition affects the shape of the tongue as well as the dentition.

The experiment was based on the following propositions:

Hypothesis 1
Premise A. The distance between the jaws (A and B) depends on the relative tonus in the muscle groups (D and E). Premise B. A change from nasal to oral respiration is contingent, upon a decrease of the tonus in D and an increase of the tonus in E. Conclusion: A change from nasal to oral respiration affects the distance between the jaws. This conclusion can be tested.  Rejection of the hypothesis would suggest that other functions exert a dominant influence on the muscle tonus, and the role of mastication and deglutition should be examined.

Hypothesis 2
Premise A. The morphologic harmony of tongue and dentition depends on the sense of contact between tongue and teeth. Premise B. The maintenance of an oral airway disrupts the contact between the tongue and the dentition. Conclusion: The maintenance of an oral airway interferes with the morphologic harmony between tongue and dentition. This conclusion is subject to test. Rejection of this hypothesis would suggest alternatively that tongue contact with the dentition during mastication and deglutition is more significant than previously assumed. These hypotheses have been examined in the following experiments.

Discussion
The oral cavity and the pharynx in the rhesus monkey differ from those of the human being in that the soft palate is relatively longer and the oropharyngeal port is relatively smaller in the monkey. For the animal to open the passage for mouth breathing, the posterior part of the tongue must be depressed and positioned forward along with the mandible. In man the mandible and the tongue are simply lowered. It has been assumed that, because of the anatomy of its pharynx, a monkey could not resort to mouth breathing when the nasal airways were obstructed and would therefore be in danger of asphyxiation if it had a severe cold or other nasal blockage.

In this study, when the nasal airways were gradually obstructed and finally blocked by silicone plugs, all experimental monkeys were transformed into partial and, later, complete mouth breathers. Occasionally, air passed on the posteriorly and air pressure in the nostrils forced the tissues away from the plugs.

However, this inconsistent nasal exhalation was considered insignificant in the experiment. It is significant that the structure of the oropharyngeal port depends on its function; an oral airway can develop and can be maintained in a 2-1/2 to 3-year-old normal monkey after the respiratory system gains control of the structure. Face height increased more in the mouth-breathing monkeys than in the control animals. This indicated that oral respiration was, indeed, associated with a consistent lowering of the mandible, which allowed an additional extrusion of the teeth. On the basis of this experiment, the first hypothesis cannot be rejected. Therefore, it can be assumed that any consistent sensor; input which affects the relative tonus in the muscle groups suspending the mandible influences the extrusion of the teeth and the establishment of face height. The magnitude of increase in the distance between the jaws attributable to changes in oral sensation was sufficient to warrant its consideration as a factor in the etiology of dental malocclusion.

The term consistent has been employed to describe the influential tactile stimuli in the first experiment as well as the sensory input elicited by enforced oral respiration in the second experiment. The frequency of the sensory input and the rate of recurrence of a series of sensory inputs necessary to elicit a morphogenic muscle behavior have not been established. These experiments recorded only the length of time for the new structure to become manifest. Oral sensation is essential in mastication and deglutition, and it is an important component of speech. Presumably, these functions influence muscle development and posture. However, still remaining to be tested is the effect of these factors on jaw morphogenesis and the development of dental occlusion.

Certain pilot studies have been focused on the sense of occlusal contact, which presumably functions in the sensory-motor feedback mechanism controlling jaw relation, These experiments demonstrated that the teeth moved away and escaped the experimentally introduced occlusal stimuli before any significant morphologic response outside of the immediate periodontal system could be registered. Future experiments will be designed to include the response characteristics of the periodontal system. In a normal monkey, as in a human being with good and stable dental occlusion, adaptation between tongue and dentition may be considered complete. The second hypothesis held that a break in the contact between the tongue and the dentition affects the position of the tongue as well as the positioning of the teeth. In the experimental animals the normal relationship between the tongue and the dentition was altered during respiration, but not necessarily during mastication, deglutition, and between breaths. It was expected, therefore, that
developing changes in the dentition would be relatively limited and would demonstrate a tendency to crowding of the teeth and changes in dental arch form. It was anticipated that the tongue would respond with only minor changes in shape: although it would assume a different position in order to allow air to pass between the tongue and the palate. If changes in tongue position and particularly in dentition did not occur, the hypothesis would be rejected. Mouth breathing would then be considered harmless and not capable of significant disruption of the sensory-motor systems modeling the oral structures.

However, the experimental procedures did result in changes in the dentition and in changes in tongue position. Therefore, the hypothesis could not be rejected on the basis of the experiments.
After a few months of the experiment the initial tongue posture changes were replaced by alterations in shape. The narrowing and flattening of the tongue in the area of the oropharyngenl port and at the tongue tip followed the forward positioning of the mandible which was initially necessary in order to permit breathing.

The influence of the sensory-motor system serving respiration could be distinguished from the systems underlying mastication and sound production, inasmuch as the former still functioned under general anesthesia (pentobarbital sodium, 0.5 cc. per kilogram). The findings indicate that tongue-surface sensation and proprioception transmitted and integrated with the respiratory system cause the tongue to withdraw from certain contact areas. The response was expressed in a forward protrusion and pointing of the tongue, which eventually affected it morphologically. Under normal conditions, when the sense of contact between tongue and teeth results in conformity, the tactile stimuli probably elicit a thrust toward the site of stimulus. Reflex circuits which may be activated in these functions have been described,7-10 but future experiments should test their significance in morphogenesis. McNamaral has recently described neurologic and morphologic changes in response to chronic mandibular protrusion.

The dental malocclusions in the experimental animals were strikingly uniform. It is difficult to associate the uniformity among the malocclusions with the variability among the tongues. It appears probable that the teeth were uniformly affected by a more dominating influence from the lips after the tongue withdrew from the dentition. It is also possible that chewing and deglutition may have exerted an inhibiting effect on the developing malocclusions.

However, these experiments demonstrated that the response pattern depended on the dominant sensory feedback system and that at least two response patterns could be distinguished. The first was characterized by the morphologic adaptation and probably was based on a reflex thrust against the site of the stimulus. This response serves to align the teeth between the tongue and the outer muscle matrix, and it may produce malocclusion if either the tongue or the jaws are deviant, as in cleft palate or macroglossia.12, I3

The second response pattern was characterized by the withdrawal of the tongue from the site of the stimulus. This response may result in severe skeletal and dental irregularities because the tongue will continue to withdraw and offer little resistance to the teeth being forced lingually by the lip and cheek musculature. The process will progress as long as the teeth are subjected to labial pressure. The changing tongue position will eventually affect the shape and position of the mandible.

Certain observations in these experiments are of clinical significance. The responses to a change in the sensory-motor systems suspending the mandible and controlling tongue position succeed each other in a particular sequence, which can be described as a “response chain.” The serial reaction may continue for a year or more, until adaptation to the stimulus is complete. In the experiment with the acrylic palatal inserts, the initial response was a lowering of the tongue and mandible to avoid the stimulus. The second response involved adaptational tongue changes, which allowed it to return to its original position.

Third, the indentation in the tongue diminished as skeletal changes allowed a more permanent lowering of the mandible. This was followed by a fourth response-the manifestation of dental malocclusion. The direct effect of the original stimulus was reduced as the chain of responses proceeded. A key stimulus which elicits a response chain resulting in a dental malocclusion constitutes an etiologic factor. If possible, a therapeutic measure should focus on an etiologic factor and elicit a “response chain” which produces a normal occlusion.

The observation that the shape of the tongue and its impact on the dental arches are closely related to its behavior during respiration should be consider in orthodontic treatment planning.
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