Ontogeny of postnatal hyoid and larynx descent in humans
Introduction
Although there have been several studies (summarized below) of hyoid position relative to the vertebral column, the mandible, and the cranial base, there is little understanding of how spatial relations between these regions change during ontogeny. In addition, we believe, there have been no longitudinal quantitative studies of overall growth of the vocal tract during ontogeny.
Data on the ontogeny of hyo-laryngeal descent are needed for testing hypotheses about functional constraints on both speech and deglutition. The low position of the human larynx relative to the hard palate, in combination with flexure of the cranial base and a short face, sets up a uniquely structured supralaryngeal vocal tract that functions as a dynamic “two-tube” with equally long horizontal (SVTH, from the posterior pharyngeal wall to the lips) and vertical (SVTV, from the vocal folds to the velum) portions (Fig. 1). According to the quantal theory of speech (Fant, 1960, Stevens, 1972, Baer et al., 1991, Lieberman et al., 1992), it is especially advantageous for the ratio of SVTV to SVTH to be 1.0. This ratio, in combination with the tongue's ability to modify independently the cross-sectional areas of SVTV and SVTH by approx. tenfold, enables humans to produce a wide range of acoustically differentiable sounds regardless of vocal-tract length (Lieberman, 1984, Beckman et al., 1995). Hyo-laryngeal descent is also important for deglutition. During swallowing, the coordination of supra- and infrahyoid muscles is partly a function of the spatial relations between the hyoid, epiglottis, mandible and mouth (Miller, 1982, Bosma, 1992, Palmer et al., 1992, Palmer et al., 1997, Gay et al., 1994). However, hyo-laryngeal descent may be disadvantageous in humans because the low position of their hyoid causes the epiglottis to lose the ability to form a seal with the soft palate, increasing the risk of aspirating food, and of developing dysphagia from poor intermuscular coordination during deglutition (Dodds, 1989, Bosma, 1992, Palmer et al., 1992, Laitman and Reidenberg, 1997).
Accurate ontogenetic data on the size and shape of the pharynx are needed to test hypotheses about the dual roles of hyo-laryngeal descent in deglutition and vocalization. How and when the hyoid and larynx move inferiorly relative to the palate and jaw during ontogeny is poorly known, in part because the position of the hyoid and larynx relative to other structures can only be measured accurately in living individuals in comparable positions (e.g. upright, during quiet respiration and with closed jaws). During most of postnatal growth, the hyo-laryngeal complex descends relative to the face and cranial base but not relative to the vertebral column. At 23–25 weeks in utero, the fetal hyoid and larynx are high relative to the cervical vertebrae, with the larynx extending from the basioccipital to the level of C3 or C4 (Bosma, 1986, Magriples and Laitman, 1987). In the neonate, the hyoid lies opposite the junction between C2 and C3, just inferior to the mandible, and the larynx extends from approx. C3 to C4 (King, 1952, Laitman and Crelin, 1976, Senecail, 1979, Bosma, 1986).
The hyoid gradually descends relative to the skull until adulthood. By 2 years of age, the hyoid and larynx have attained their adult position relative to the cervical vertebrae, with the superior margin of the hyoid body opposite the junction between C3 and C4 (Carlsöö and Leijon, 1960, Roche and Barkla, 1965, Westhorpe, 1987). Some additional descent of the larynx occurs at puberty, resulting in a slight degree of sexual dimorphism, which is most probably a function of dimorphism in body size (Fitch and Giedd, 1999).
Numerous studies have found the position of the hyoid to be fairly conservative among adults relative to the vertebral column and skull. During quiet respiration, the greater horn of the hyoid body typically lies opposite the body of C3 or between the C3–C4 junction, with no significant differences in position between adult males and females (Bibby and Preston, 1981), and with either no or only slight differences in position among adults with various types of malocclusion or variations in craniofacial shape (Kumar et al., 1995, Athanasiou et al., 1991, Tallgren and Solow, 1987, Haralabakis et al., 1993). The resting position of the hyoid is usually normal in dysphagic individuals (Curtis, 1989), but failure to elevate the hyo-laryngeal complex properly during swallowing is a common cause of dysphagia, and may be associated with inadequate opening of the upper oesophageal sphincter as well as impaired protection of the airway during swallowing (Dodds et al., 1990).
Data are also needed on the ontogeny of hyo-laryngeal descent relative to the cranial base and mouth in order to document growth of the SVT, defined here as the portion of the pharynx which extends from the vocal folds to the front of the oral cavity. As noted above, the unique two-tube SVT in humans (Fig. 1) is characterized by equally long horizontal (SVTH) and vertical (SVTV) portions. Numerous factors, including the position and shape of the tongue, cheeks, lips, and mandible, influence the cross-sectional shapes of SVTV and SVTH, but to the best of our knowledge no longitudinal studies have directly measured SVT growth in humans. In a recent study, Fitch and Giedd (1999) used sagittal magnetic resonance images from 130 individuals aged 2.8 years and older to assess SVT growth, divided into several regions. They found significant increases in length in all portions of the SVT throughout childhood and puberty, but only the velar and pharyngeal portions of the SVT grew significantly during puberty and adulthood (14–25 years). Fitch and Giedd, however, used images produced with the individual in a supine position, and the sample was split into just three broad age categories (prepubertal, peripubertal and postpubertal).
Our primary objective was to examine the ontogeny of hyoid and laryngeal descent and the growth of the vocal tract. A second objective was to test the hypothesis that spatial constraints related to deglutition impose greater restrictions on the rate and degree of hyo-laryngeal descent than those related to vocalization. Successful deglutition requires precise coordination of tongue, hyoid, epiglottis and oesophageal sphincter movements (Miller, 1982, Bosma, 1992, Thexton and Crompton, 1989). During a typical swallow, the suprahyoid muscles elevate and protrude the hyo-laryngeal complex, opening the upper oesophageal sphincter and pulling the larynx away from the path of the descending bolus. At the same time, the laryngeal sphincter constricts and the epiglottis flexes. As with other types of highly patterned reflexive actions, coordination of these movements is a function of the relative onset and duration of many muscle contractions and spatial relations between the mandible, tongue, hyoid, epiglottis and oesophageal sphincter. This study does not address patterns of muscle activity (see Miller, 1982, Hiiemae and Crompton, 1985, Palmer et al., 1992), but instead examines vertical distances between the larynx, hyoid, mandible and cranial base. As swallowing is primarily an involuntary, highly patterned reflex activity, muscular coordination among the components of the pharynx would be expected to remain stable during ontogeny if the mandible, hyoid and larynx grow inferiorly at similar rates, thus maintaining consistent vertical spatial positions relative to each other. In contrast, if hyo-laryngeal descent is unconstrained by changes in suprahyoid muscle coordination related to deglutition, then there is no special reason for the hyoid, larynx and mandible to descend relative to the cranium at similar rates. Instead, the rate of hyo-laryngeal descent might be expected to equal that of anteroposterior facial growth to maintain the adaptive 1:1 ratio of SVTH to SVTV that characterizes the adult human vocal tract.
Section snippets
Sample
Our sample was of 15 males and 13 females (Fig. 2) selected from the Denver Growth Study conducted by the Child Research Council, University of Colorado School of Medicine (McCammon, 1970). Those chosen were Caucasian Americans radiographed between 1931 and 1966 at a distance of 7.5 feet in lateral and frontal view at the age of 1, 3 and 9 months, and thereafter every 12 months until adulthood (Maresh and Washburn, 1938, Maresh, 1948). From the age of 1 year 9 months, the participants had been
Ontogeny
Fig. 3 and Fig. 4 plot ontogenetic trajectories of the vertical and horizontal components of the pharynx, respectively. Gonion, the hyoid and the larynx all descended gradually relative to the palatal plane and to each other throughout the postnatal growth period in a typical facial growth trajectory (Fig. 3). The most rapid changes occurred between 9 months and 2.75 years of age. By postnatal month 1, resting hyoid position averaged 1 cm below the mandibular margin with no significant changes
Discussion
We demonstrate that growth in the vertical and horizontal portions of the pharynx occurs at different rates before 14 years of age. In particular, the relative vertical growth between the vocal folds, the hyoid, the base of the mandible and the hard palate maintains constant proportions between these regions, whereas the ratio of vertical to horizontal dimensions changes considerably. The SVT has two phases of growth in terms of proportionality: in phase I, before about 6–8 years of age, SVTH
Acknowledgements
We thank S. Leigh for statistical advice, and A.W. Crompton and P. Lieberman for stimulating discussions. This research was supported in part by funding from the Center for the Advanced Study of Human Paleobiology, George Washington University (to DEL), a National Science Foundation Graduate Fellowship (to RCM), and research grant #DC02123 from the NIH/National Institute on Deafness and Other Communication Disorders (to JBP).
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