Vocal tract anatomy and the neural bases of talking

Being able to talk entails having both a species-specific tongue and neural mechanisms that can acquire and execute the motor acts that generate human speech. Darwinian modification of anatomy initially adapted for swallowing yielded the human tongue and supralaryngeal vocal tract (SVT). These speciesspecific adaptations extend the range of vowel formant frequencies to include the quantal vowels [i], [u] and [a]. The biological cost is an increased risk of choking. Speech is possible absent these sounds, as is the case for young children, but it is not as robust a means of communication. The tongues and SVTs of human newborn infants cannot produce quantal vowels, contrary to the claims of L-J Boe and his colleagues which are based on their VLAM modeling technique. VLAM modeling distorts newborn tongues and SVTs to conform to those of adult humans. Similar distortions invalidate VLAM modeling of the vocal anatomy of young children and reconstructions of fossil hominins. Although other mammals are able to lower their larynges, their tongues cannot form the shapes necessary to produce quantal vowels. The neural bases by which the complex motor control patterns necessary to produce speech are learned and executed involve cortical–basal ganglia neural circuits similar to those present in other primates. In humans, the FOXP2 transcriptional factor enhanced motor control, associative learning and other aspects of cognition by increasing synaptic plasticity and dendritic connectivity in the basal ganglia and other components of these circuits. Other transcriptional factors that differentiate humans from chimpanzees appear to enhance neuronal transmission. Cortical-to-cortical circuits undoubtedly play a role in human language, much as they do in other aspects of behavior. However, the direct, cortical-to-laryngeal neural circuits that Deacon and Fitch believe account for human speech do not exist. Constraints on neck length in fossil hominins permit new assessments of their SVTs, and an insight on when human neural capacities for speech production evolved. Fully human SVTs are not apparent until 50,000 years ago in the Upper Paleolithic European populations but must have been present much earlier in Africa. The neural capacity for speech motor control also must have present in early human African populations. & 2012 Elsevier Ltd. All rights reserved. 1. The evolutionary framework It is clear that being able to talk is a ‘‘derived’’ property of the hominin lineage that led to Homo sapiens. Being able to talk differentiates us from chimpanzees, our closest living relative, and other species. Dogs, for example, can learn to respond to two hundred or more spoken words (Kaminski, Call, & Fischer, 2004), but they cannot talk. The question is whether these species cannot talk because they lack the requisite anatomy, or whether they lack neural structures that could regulate speech production. The thesis presented here is that though speech is possible using non-human primate anatomy, human anatomy and brains both evolved to yield a more robust communications system. Moreover, that the evolution of human speech anatomy provides an insight on when the neural capability for speech motor control was present. Both the anatomy and the neural mechanisms ll rights reserved. involved in speech motor control were shaped by Darwinian processes. The opportunistic, ‘‘proximate logic’’ (Mayr, 1982) of evolution is apparent in modifications of the primate tongue and neck and neural circuits that occur in non-human primates. As we shall see, humans do not appear to have unique neural circuits that regulate speech production. Transcriptional genes, including the FOXP2 transcriptional factor, instead appear to have enhanced the ability of neural circuits that exist in other primates to both learn and execute the internally guided motor acts that are necessary to produce human speech. 2. Did the human tongue and SVT evolve to enhance speech communication? One line of enquiry, which dates back to Johannes Muller’s (1848) treatise, The physiology of the sense, voice and muscular motion with the mental faculties, has explored the anatomy and P. Lieberman / Journal of Phonetics 40 (2012) 608–622 609 physiology of speech production. The human supralaryngeal vocal tract (SVT), the airway above the larynx, generates the formant frequency patterns that play a major role in conveying words. Quantitative studies show that the length and shape of the SVT, more precisely, the cross-sectional area along its length, determines formant frequencies (e.g., Chiba & Kajiyama, 1941; Fant, 1970). The role of the human tongue, which can play a major role in determining the shape of the SVT as a person talks, has been noted in studies spanning 150 years (e.g., Bell, 1865; De Boer, 2010; Nearey, 1978; Stevens, 1972). Charles Darwin in the first edition of On the origin of species, raised the question of whether the human tongue might been modified in the course of evolution to facilitate speech production. Darwin noted, ‘‘The strange fact that every particle of food and drink which we swallow has to pass over the orifice of the trachea, with some risk of falling into the lungs y’’(Darwin, 1859, 1964, p. 191). In the 20th century Victor Negus’s studies of comparative anatomy pointed out the species-specific nature of the human tongue. Negus also showed that the tongues and SVTs of human newborn infants were similar in many ways to those of nonhuman primates. Negus attributed the lower position of the larynx in adult humans to the restructuring of the human skull which shortened the length of the oral cavity that, in turn, changed the shape of the human tongue and caused it to descend into the pharynx. The adult larynx thus descended because it ‘‘is closely apposed to the tongue’’ (Negus, 1949, pp. 25–26). Negus concluded that the human tongue had developed for ‘‘y purposes of speech.’’ (1949, p. 198). The findings of computer-modeling studies that calculated the range of formant frequencies that could be produced by adult human and non-human SVTs supported Negus’s hypothesis (Lieberman, Klatt, & Wilson, 1969; Lieberman et al., 1972). The 1969 study used a computer-implemented vocal tract modeling technique which calculated the formant frequency patterns of the vowels that a rhesus macaque could produce. The range of tongue shapes that a monkey could produce was estimated by taking into account constraints on tongue deformation (since confirmed by Takemoto, 2001, 2008) and moving its tongue towards the positions used by adult human speakers to yield the ‘‘point’’ vowels [i], [u] and [a] that delimit the range of vowels generally used in human languages (Greenberg, 1963; Maddieson, 1984). The computer model showed that the monkey’s vowel space did not include these point vowels. Subsequent computer modeling studies (Lieberman et al., 1972) revealed similar limits on the phonetic capabilities of chimpanzees and human newborn infants whose SVTs are similar to those of nonhuman primates (Crelin, 1969; Negus, 1949). Lieberman and Crelin (1971) concluded that the vocal tract of La Chapelle-aux-Saints Neanderthal was similar to that of a large human newborn. The cineradiographic data on newborn infant cry of Truby, Bosma, and Lind (1965) and an adult human, Perkell (1969) guided the jaw, tongue, lip and laryngeal maneuvers used to derive the range of possible Neanderthal SVT configurations modeled. As Lieberman and Crelin (1971, p. 211) noted, ‘‘When we were in doubt as, for example, with respect to the range of variation in the area of the larynx, we used data derived from adult Man that would enhance the phonetic ability of the Neanderthal vocal tract (Fant, 1960). Moreover, the larynx of the SVT modeled was placed in the lowest position evident in the ‘‘forceful’’ cries in which the newborn larynx descended’’ (Truby et al., 1965, pp. 75 and 77). The dynamic SVT movements in the Truby et al. (1965) and Perkell’s (1969) cineradiographic studies were used to derive the range of SVT shapes modeled in the subsequent Lieberman et al. (1972) study. Critiques, such as Fitch (2010, p. 317) that characterize these computer modeling studies as ‘‘futile,’’ because they attempted, ‘‘to reconstruct the details of articulatory movements from muscle angles in dead or anaesthetized animals’’ are not in accord with the facts. Negus’s views on the reshaping of the adult human SVT turned out to be partially correct. At birth most of the tongue is positioned in the mouth, and its shape is flat, as is the case for other mammals. In newborn human infants, the proportion of the tongue in the oral ‘‘horizontal’’ (SVTh) part of the infant oral cavity relative to the part of the tongue in the ‘‘vertical’’ pharynx (SVTv)—SVTh/SVTv was 1.5, when the larynx was lowered in the ‘‘forceful’’ cries pictured in Truby et al. (1965, pp. 75—78). The human tongue does not attain its adult 1:1 SVTh/SVTv proportions and almost circular posterior mid-sagittal shape until age 6– 8 years. Daniel Lieberman and his colleagues tracked the descent and reshaping of the human tongue using cepalometric radiographs of 15 males and 13 females systematically taken between the ages of one month and 14 years. The developmental process by which the species-specific human vocal tract is formed is complex and takes 6–8 years, sometimes as long as age 10 years (Lieberman & McCarthy, 1999; Lieberman, McCarthy, Hiiemae, & Palmer, 2001). The length of the oral cavity is first constrained and shortened in humans via a number of mechanisms including absence of a rostrum and ventral rotation of the ethmomaxillary complex, which moves the hard palate back on the base of the skull (Lieberman, 2011). The shape and position of the tongue then gradually change. The newborn tongue is flat and is positioned almost entirely in the oral cavity. It achieves its posterior rounded contour as it descends down into the pharynx, carrying the larynx do