Developmental changes in the shape of the supralaryngeal vocal tract in chimpanzees

The hyoid bone and larynx in human neonates are positioned as high as in other mammals. However, during postnatal life, they descend relative to the hard palate more rapidly compared with the horizontal growth of the oral cavity. This process is completed through the descent of the laryngeal skeleton relative to the hyoid, and through the descent of the hyoid relative to the cranial base. Thus, the human supralaryngeal vocal tract (SVT) develops to form a two-tube configuration with equally long horizontal and vertical parts. Longitudinal studies on living chimpanzee infants show that the descent of the larynx is more rapid than the horizontal growth of the oral cavity. This is primarily attributed to the descent of their larynges relative to the hyoid bone, but this is not accompanied by the descent of the hyoid. The present study, using embalmed specimens of chimpanzees, also shows that the horizontal and vertical parts of the SVT grow in chimpanzees similarly to humans during infancy. However, in chimpanzees, the horizontal part of the SVT grows greatly, whereas the vertical part of the SVT grows only slightly during the juvenile period. As a result, the chimpanzee larynx does not descend rapidly relative to the oral elongation during that period. Such differences may be related to the structural and morphological development of the facial skeleton and mandible, which affects prognathism and hyoid descent. These results support the hypothesis that the descent of the larynx evolved in at least two steps during hominoid evolution.     

Development of the supralaryngeal vocal tract in Japanese macaques: implications for the evolution of the descent of the larynx

The configuration of the supralaryngeal vocal tract depends on the nonuniform growth of the oral and pharyngeal portion. The human pharynx develops to form a unique configuration, with the epiglottis losing contact with the velum. This configuration develops from the great descent of the larynx relative to the palate, which is accomplished through both the descent of the laryngeal skeleton relative to the hyoid and the descent of the hyoid relative to the palate. Chimpanzees show both processes of laryngeal descent, as in humans, but the evolutionary path before the divergence of the human and chimpanzee lineages is unclear. The development of laryngeal descent in six living Japanese macaque monkeys, Macaca fuscata, was examined monthly during the first three years of life using magnetic resonance imaging, to delineate the present or absence of these two processes and their contributions to the development of the pharyngeal topology. The macaque shows descent of the hyoid relative to the palate, but lacks the descent of the laryngeal skeleton relative to the hyoid and that of the EG from the VL. We argue that the former descent is simply a morphological consequence of mandibular growth and that the latter pair of descents arose in a common ancestor of extant hominoids. Thus, the evolutionary path of the great descent of the larynx is likely to be explained by a model comprising multiple and mosaic evolutionary pathways, wherein these developmental phenomena may have contributed secondarily to the faculty of speech in the human lineage.     

The descended larynx is not uniquely human

Morphological modifications of vocal anatomy are widespread among vertebrates, and the investigation of the physiological mechanisms and adaptive functions of such variants is an important focus of research into the evolution of communication. The "descended larynx" of adult humans has traditionally been considered unique to our species, representing an adaptation for articulate speech, and debate concerning the position of the larynx in extinct hominids assumes that a lowered larynx is diagnostic of speech and language. Here, we use bioacoustic analyses of vocalizing animals, together with anatomical analyses of functional morphology, to document descended larynges in red and fallow deer. The resting position of the larynx in males of these species is similar to that in humans, and, during roaring, red-deer stags lower the larynx even further, to the sternum. These findings indicate that laryngeal descent is not uniquely human and has evolved at least twice in independent lineages. We suggest that laryngeal descent serves to elongate the vocal tract, allowing callers to exaggerate their perceived body size by decreasing vocal-tract resonant frequencies. Vocal-tract elongation is common in birds and is probably present in additional mammals. Size exaggeration provides a non-linguistic alternative hypothesis for the descent of the larynx in human evolution.     

Comparative morphology of the hyo-laryngeal complex in anthropoids: two steps in the evolution of the descent of the larynx

The descent of the larynx is a key phenomenon not only in postnatal development, but also in the evolution of human speech. The positional change of the larynx is affected by the descent of the hyoid bone in relation to the mandible and cranial base, and that of the laryngeal framework in relation to the hyoid bone. The phylogeny of the spatial configuration of the hyo-laryngeal complex is one of the most important sources of information for elucidating the evolution of laryngeal descent. In the present study, the anatomy of the complex was examined in various species of anthropoids to compare the configuration, the shape of the basihyal and thyroid cartilage, and the length of the lateral thyrohyoid ligaments. Non-human hominoids share most features with humans, while cercopithecoids and ceboids have anatomical features that sharply contrast to humans, except for the form of the thyroid cartilage in ceboids. The laryngeal framework in hominoids is well separated from and assured of mobility independent of the hyoid. In cercopithecoids and ceboids, it is, by contrast, locked into and tied tightly with the hyoid so that the hyo-laryngeal complex acts as a functional unit. This spatial configuration is considered to be significantly related to the mechanism that prevents aspiration, including epiglottic movement and vestibular closure. Non-human hominoids are inferred to share the mechanism with human adults, not with cercopithecoids and ceboids, although their larynx is located as high as the latter. Consequently, it is hypothesized that the descent of the larynx evolved in two steps. The first step would have been descent of the thyroid in relation to the hyoid for the evolution of the mechanism preventing aspiration, which occurred in the common ancestor of hominoids. The second step, descent of the hyoid within the neck, occurred during hominid evolution for human speech. Electronic Publication     

The postnatal ontogeny of the sexually dimorphic vocal apparatus in goitred gazelles (Gazella subgutturosa)

This study quantitatively documents the progressive development of sexual dimorphism of the vocal organs along the ontogeny of the goitred gazelle (Gazella subgutturosa). The major, male‐specific secondary sexual features, of vocal anatomy in goitred gazelle are an enlarged larynx and a marked laryngeal descent. These features appear to have evolved by sexual selection and may serve as a model for similar events in male humans. Sexual dimorphism of larynx size and larynx position in adult goitred gazelles is more pronounced than in humans, whereas the vocal anatomy of neonate goitred gazelles does not differ between sexes. This study examines the vocal anatomy of 19 (11 male, 8 female) goitred gazelle specimens across three age‐classes, that is, neonates, subadults and mature adults. The postnatal ontogenetic development of the vocal organs up to their respective end states takes considerably longer in males than in females. Both sexes share the same features of vocal morphology but differences emerge in the course of ontogeny, ultimately resulting in the pronounced sexual dimorphism of the vocal apparatus in adults. The main differences comprise larynx size, vocal fold length, vocal tract length, and mobility of the larynx. The resilience of the thyrohyoid ligament and the pharynx, including the soft palate, and the length changes during contraction and relaxation of the extrinsic laryngeal muscles play a decisive role in the mobility of the larynx in both sexes but to substantially different degrees in adult females and males. Goitred gazelles are born with an undescended larynx and, therefore, larynx descent has to develop in the course of ontogeny. This might result from a trade‐off between natural selection and sexual selection requiring a temporal separation of different laryngeal functions at birth and shortly after from those later in life. J. Morphol. 277:826–844, 2016. © 2016 Wiley Periodicals, Inc.     

Approche paléontologique de l’évolution du langage : un état des lieux

One of the most influential paleoanthropological approaches to the question of language origins has been the attempt to reconstruct the supralaryngeal vocal tract (SVT) in fossil humans. In particular, the low placement of the larynx was considered to be a uniquely human feature and was interpreted as a specific adaptation to produce human speech. Nevertheless, based on the anatomy of the basicranium and the hyoid bone, various researchers reached different conclusions regarding the placement of the larynx in human fossils, especially in Neandertals. Further, the recent finding of a low placement of the larynx in chimpanzees, calls into question the basic premise on which much of this research has been based. To overcome this, we have proposed and developed a new line of research into the question of speech capabilities in fossil specimens which is focused not on the ability to produce the sounds of spoken language, but on the capacity to perceive them. The modern human auditory pattern is unique among primates in showing a relatively heightened sensitivity to the midrange frequencies between 2-4 kHz, a frequency range which coincides with that of spoken language. Our analysis shows that the preserved skeletal anatomy of the outer and middle ear in the Middle Pleistocene hominids from the site of the Sima de los Huesos is compatible with human-like auditory capacities, and is clearly different from chimpanzees in the midrange frequencies. These results strongly suggest that the anatomical structures which support the modern hum and pattern of intraspecific communication were already present in these human ancestors. Further, the presence of a common condition in both the modern human and Neandertal evolutionary lineages suggests this represents an ancient adaptation within the genus Homo.     

A reappraisal of the anatomical basis for speech in Middle Palaeolithic hominids

The recovery of a fossil hominid skeleton with a complete hyoid bone from Mousterian deposits in Kebara Cave, Israel, provides new evidence pertaining to the evolution of speech. Previous studies of speech in the Middle Palaeolithic (most notably those on Neandertals) have focused on the basicranium as an indicator of speech capabilities. This work critiques the use of the basicranium and instead presents the anatomical relations of the hyoid and adjacent structures in living humans as a basis for understanding the form of the vocal tract. The size and morphology of the hyoid from Kebara and its relations to other anatomical components are almost identical to those in modern humans, suggesting that Middle Palaeolithic populations were anatomically capable of fully modern speech.     

The anatomy of vocal divergence in North American Elk and European red deer

Loud and frequent vocalizations play an important role in courtship behavior in Cervus species. European red deer (Cervus elaphus) produce low‐pitched calls, whereas North American elk (Cervus canadensis) produce high‐pitched calls, which is remarkable for one of the biggest land mammals. Both species engage their vocal organs in elaborate maneuvers but the precise mechanism is unknown. Vocal organs were compared by macroscopic and microscopic dissection. The larynx is sexually dimorphic in red deer but not in elk. The laryngeal lumen is more constricted in elk, and narrows further during ontogeny. Several elements of the hyoid skeleton and two of four vocal tract segments are longer in red deer than in elk allowing greater vocal tract expansion and elongation. We conclude that elk submit the larynx and vocal tract to much higher tension than red deer, whereby, enormously stressed vocal folds of reduced effective length create a high resistance glottal source. The narrow, high impedance laryngeal vestibulum matches glottal and vocal tract impedance allowing maximum power transfer. In red deer longer and relaxed vocal folds create a less resistant glottal source and a wider vestibulum matches the low glottal impedance to the vocal tract, thereby also ensuring maximum power transfer. J. Morphol., 2013. © 2012 Wiley Periodicals, Inc.     

Dominant frequency of loud mew calls of felids (Mammalia: Carnivora) decreases during ontogenetic growth

• 1 A negative correlation between body weight and frequency characteristics of a species' vocalizations exists in mammals, due to the acoustics of vocal sound production (‘source‐filter theory’; source = larynx; filter = supralaryngeal vocal tract) and the strong positive correlation between body weight and vocal tract length.
• 2 A negative correlation is hypothesized to exist between increasing body weight and frequency characteristics of calls during ontogeny as well.
• 3 This hypothesis is tested for mean dominant frequency (maximum spectral energy peak) of intense mew calls in juveniles of five species of the Felidae: lion Panthera leo, jaguar Panthera onca, leopard Panthera pardus, tiger Panthera tigris and puma Puma concolor.
• 4 In the five felid species in which the hyoid is incompletely ossified (genera Panthera and Uncia), the larynx undergoes a considerable ontogenetic descent, resulting in a proportionally longer vocal tract in adult individuals than in all other species of the family, which have a fully ossified hyoid without a descent.
• 5 In all five species studied here, mean dominant frequency decreases as body weight increases during growth. In the four Panthera species (with laryngeal descent) dominant frequency is determined by the vocal tract (the filter), and dominant frequency is largely similar at similar weights, indicating a similar correlation between the ontogenetic increase in body weight (and vocal tract length) and the decrease in mean dominant frequency. In the puma (without laryngeal descent) dominant frequency is determined by the larynx (the source), it is considerably higher than in the Panthera species, and the course of its ontogenetic decrease differs considerably from that in Panthera.
• 6 The data do not support a uniform scaling relationship between body weight and mean dominant frequency of intense mew calls in the Felidae during ontogenetic growth.

     

Some aspects of dimorphism and human speech

The production of human speech involves thre supralaryngeal airway filtering the acoustic energy generated by either laryngeal or noise sources. Both the supralaryngeal vocal tract and the larynx are subject to sexual dimorphism in anatomically modernHomo sapiens, yielding acoustic signals that can convey a speaker’s sex. Formant frequencies can be lower because the adult male supralaryngeal vocal tract is often longer. The fundamental frequency of phonation also can be lower because of the enlargement of the thyroid cartilage of the larynx and concomitant increases in the length and mass of the vocal cords. Secondary, learned supralaryngeal vocal tract maneuvers can also lower or raise formant frequencies. These acoustic effects yield male-female «microphonetic» dialects that are ultimately related to the average dimorphism found in the adult population. The dimorphism anatomy of the supralaryngeal vocal tract and larynx of fossil hominoids can be inferred from their skulls.     

Short Faces,Big Tongues: Developmental Origin of the Human Chin

During the course of human evolution, the retraction of the face underneath the braincase, and closer to the cervical column, has reduced the horizontal dimension of the vocal tract. By contrast, the relative size of the tongue has not been reduced, implying a rearrangement of the space at the back of the vocal tract to allow breathing and swallowing. This may have left a morphological signature such as a chin (mental prominence) that can potentially be interpreted in Homo. Long considered an autopomorphic trait of Homo sapiens, various extinct hominins show different forms of mental prominence. These features may be the evolutionary by-product of equivalent developmental constraints correlated with an enlarged tongue. In order to investigate developmental mechanisms related to this hypothesis, we compare modern 34 human infants against 8 chimpanzee fetuses, whom development of the mandibular symphysis passes through similar stages. The study sets out to test that the shared ontogenetic shape changes of the symphysis observed in both species are driven by the same factor – the space restriction at the back of the vocal tract and the associated arrangement of the tongue and hyoid bone. We apply geometric morphometric methods to extensive three-dimensional anatomical landmarks and semilandmarks configuration, capturing the geometry of the cervico-craniofacial complex including the hyoid bone, tongue muscle and the mandible. We demonstrate that in both species, the forward displacement of the mental region derives from the arrangement of the tongue and hyoid bone, in order to cope with the relative horizontal narrowing of the oral cavity. Because humans and chimpanzees share this pattern of developmental integration, the different forms of mental prominence seen in some extinct hominids likely originate from equivalent ontogenetic constraints. Variations in this process could account for similar morphologies.     

The anatomy, physiology, acoustics and perception of speech: essential elements in analysis of the evolution of human speech

Inferences on the evolution of human speech based on anatomical data must take into account its physiology, acoustics and perception. Human speech is generated by the supralaryngeal vocal tract (SVT) acting as an acoustic filter on noise sources generated by turbulent airflow and quasi-periodic phonation generated by the activity of the larynx. The formant frequencies, which are major determinants of phonetic quality, are the frequencies at which relative energy maxima will pass through the SVT filter. Neither the articulatory gestures of the tongue nor their acoustic consequences can be fractionated into oral and pharyngeal cavity components. Moreover, the acoustic cues that specify individual consonants and vowels are “encoded”, i.e., melded together. Formant frequency encoding makes human speech a vehicle for rapid vocal communication. Non-human primates lack the anatomy that enables modern humans to produce sounds that enhance this process, as well as the neural mechanisms necessary for the voluntary control of speech articulation. The specific claims of Duchin (1990) are discussed.     

Two atavistic characteristics of the laryngeal skeleton

In the analysis of laryngeal anomalies in 30 selected phoniatric patients by CT examination, 2 atavisms of the laryngeal skeleton were found. The ventral enclosure of the thyroid cartilage by the hyoid bone presents an inhibition malformation of the laryngeal skeleton with essential reduced vocal ability. The posterior junction between the cornu majus ossis hyoidei and the cornu superius cartilaginis thyroideae is marked by the direct contact of these cornua lacking the ligamentum thyrohyoideum laterale. Both anomalies are characterized by the persistence of the close relation between the hyoid bone and the thyroid cartilage, which normally exists phylogenetically as well as ontogenetically. That could be shown by anatomical sections performed on 4 human newborns in the horizontal plane.     

Functional reconstruction of the supralaryngeal vocal tract of fossil human

The purpose of the study was to reconstruct the supralaryngeal vocal tract of the archaic human from Petralona in Greece and to assess its vocal abilities. The reconstruction of the position of the hyoid bone of the Palaeolithic hominid from Petralona has been done by using the relation between the flexion of the basicranium and the inclination of the processus styloideus. The results indicate the lower position of the larynx in the fossil hominid. This conclusion was confirmed by an assessment of the position of the hyoid bones by extrapolating from a sample of 45 x-rays scans of recent adult human males.     

Vocal production mechanisms in a non-human primate: morphological data and a model

Human beings are thought to be unique amongst the primates in their capacity to produce rapid changes in the shape of their vocal tracts during speech production. Acoustically, vocal tracts act as resonance chambers, whose geometry determines the position and bandwidth of the formants. Formants provide the acoustic basis for vowels, which enable speakers to refer to external events and to produce other kinds of meaningful communication. Formant-based referential communication is also present in non-human primates, most prominently in Diana monkey alarm calls. Previous work has suggested that the acoustic structure of these calls is the product of a non-uniform vocal tract capable of some degree of articulation. In this study we test this hypothesis by providing morphological measurements of the vocal tract of three adult Diana monkeys, using both radiography and dissection. We use these data to generate a vocal tract computational model capable of simulating the formant structures produced by wild individuals. The model performed best when it combined a non-uniform vocal tract consisting of three different tubes with a number of articulatory manoeuvres. We discuss the implications of these findings for evolutionary theories of human and non-human vocal production.     

Human hyoid bones from the middle Pleistocene site of the Sima de los Huesos (Sierra de Atapuerca, Spain)

This study describes and compares two hyoid bones from the middle Pleistocene site of the Sima de los Huesos in the Sierra de Atapuerca (Spain). The Atapuerca SH hyoids are humanlike in both their morphology and dimensions, and they clearly differ from the hyoid bones of chimpanzees and Australopithecus afarensis. Their comparison with the Neandertal specimens Kebara 2 and SDR-034 makes it possible to begin to approach the question of temporal variation and sexual dimorphism in this bone in fossil humans. The results presented here show that the degree of metric and anatomical variation in the fossil sample was similar in magnitude and kind to living humans. Modern hyoid morphology was present by at least 530 kya and appears to represent a shared derived feature of the modern human and Neandertal evolutionary lineages inherited from their last common ancestor.     

Mobile larynx in Mongolian gazelle: Retraction of the larynx during rutting barks in male Mongolian gazelle (Procapra gutturosa Pallas, 1777)

This study provides the first evidence of pronounced temporary laryngeal descent in a bovid species. An elaborate acoustic display is prominent in male courtship behavior of polygynous Mongolian gazelle. During rut, rounding up of females is accompanied by continuous head‐up barking by dominant males. Throughout the rut their evolutionarily enlarged larynx descends to a low mid‐neck resting position. In the course of each bark the larynx is additionally retracted toward the sternum by 30% of the resting vocal tract length. A geometric model of active larynx movements was constructed by combining results of video documentation, dissection, skeletonization, and behavioral observation. The considerable distance between resting position and maximal laryngeal descent suggests a backward tilting of the hyoid apparatus and an extension of the thyrohyoid connection during the retraction phase. Return to the resting position is effected by strap muscles and by the elastic recoil of the pharynx and the thyrohyoid connection. An intrapharyngeal inflation of the peculiar palatinal pharyngeal pouch of adult males is inferred from a short‐time expansion of the ventral neck region rostral to the laryngeal prominence. The neck of adult dominant males is accentuated by long gray guard hairs during the rut. The passive swinging of the heavy larynx of adult males during locomotion gives the impression of a handicap imposed on rutting males. Apparently, this disadvantage becomes outweighed by the profits for reproductive success. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

The ontogeny of cranial base angulation in humans and chimpanzees and its implications for reconstructing pharyngeal dimensions

This paper examines differences in the processes by which the cranial base flexes in humans and extends in chimpanzees. In addition, we test the extent to which one can use comparisons of cranial base angles in humans and non-human primates to predict vocal tract dimensions. Four internal cranial base angles and one external cranial base angle were measured in a longitudinal sample of Homo sapiens and a cross-sectional sample of Pan troglodytes. These data show that the processes of cranial base angulation differ substantially in these species. While the human cranial base flexes postnatally in a rapid growth trajectory that is complete by two years, the cranial base in P. troglodytes extends postnatally in a more prolonged skeletal growth trajectory. These comparisons also demonstrate that the rate of cranial base angulation is comparable for different measures, but that angles which incorporate different anterior cranial base measurements correlate poorly. We also examined ontogenetic relationships between internal and external cranial base angles and vocal tract growth in humans to test the hypothesis that cranial base angulation influences pharyngeal dimensions and can, therefore, be used to estimate vocal tract proportions in fossil hominids. Our results indicate that internal and external cranial base angles are independent of the horizontal and vertical dimensions of the vocal tract. Instead, a combination of mandibular and palatal landmarks can be used to predict dimensions of the vocal tract in H. sapiens. The developmental contrasts in cranial base angulation between humans and non-human primates may have important implications for testing hypotheses about the relationship between cranial base flexion and other craniofacial dimensions in hominid evolution.     

Vocal-auditory functions in the chimpanzee: Vowel perception

The perception of vowels was studied in chimpanzees and humans, using a reaction time task in which reaction times for discrimination of vowels were taken as an index of similarity between vowels. Vowels used were five synthetic and natural Japanese vowels and eight natural French vowels. The chimpanzees required long reaction times for discrimination of synthetic [i] from [u] and [e] from [o], that is, they need long latencies for discrimination between vowels based on differences in frequency of the second formant. A similar tendency was observed for discrimination of natural [i] from [u]. The human subject required long reaction times for discrimination between vowels along the first formant axis. These differences can be explained by differences in auditory sensitivity between the two species and the motor theory of speech perception. A vowel, which is pronounced by different speakers, has different acoustic properties. However, humans can perceive these speech sounds as the same vowel. The phenomenon of perceptual constancy in speech perception was studied in chimpanzees using natural vowels and a synthetic [o]- [a] continuum. The chimpanzees ignored the difference in the sex of the speakers and showed a capacity for vocal tract normalization.     

Speech motor control

The development of new measurement techniques and improved models of the larynx and the vocal tract have significantly advanced our understanding of speech motor control. Recently, several groups have been using electromagnetic transduction techniques to record tongue movements. The laryngeal vibrations have been modeled and studied using techniques from non-linear dynamics. Computational models of supraglottal movements have been proposed and tested. A connectionist model that synthesizes the results obtained from observing the effects of variations in rate, stress, and phonetic context on speech kinematics has recently been proposed.