W. Tecumseh Fitch

Morphology and development of the human vocal tract: A study using magnetic resonance imaging

Magnetic resonance imaging was used to quantify the vocal tract morphology of 129 normal humans, aged 2-25 years. Morphometric data, including midsagittal vocal tract length, shape, and proportions, were collected using computer graphic techniques. There was a significant positive correlation between vocal tract length and body size (either height or weight). The data also reveal clear differences in male and female vocal tract morphology, including changes in overall vocal tract length and the relative proportions of the oral and pharyngeal cavity. These sex differences are not evident in children, but arise at puberty, suggesting that they are part of the vocal remodeling process that occurs during puberty in males. These findings have implications for speech recognition, speech forensics, and the evolution of the human speech production system, and provide a normative standard for future studies of human vocal tract morphology and development.

The evolution of speech: a comparative review.

The evolution of speech can be studied independently of the evolution of language, with the advantage that most aspects of speech acoustics, physiology and neural control are shared with animals, and thus open to empirical investigation. At least two changes were necessary prerequisites for modern human speech abilities: (1) modification of vocal tract morphology, and (2) development of vocal imitative ability. Despite an extensive literature, attempts to pinpoint the timing of these changes using fossil data have proven inconclusive. However, recent comparative data from nonhuman primates have shed light on the ancestral use of formants (a crucial cue in human speech) to identify individuals and gauge body size. Second, comparative analysis of the diverse vertebrates that have evolved vocal imitation (humans, cetaceans, seals and birds) provides several distinct, testable hypotheses about the adaptive function of vocal mimicry. These developments suggest that, for understanding the evolution of speech, comparative analysis of living species provides a viable alternative to fossil data. However, the neural basis for vocal mimicry and for mimesis in general remains unknown.

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.

Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production

Abstract Recent work on human vocal production demonstrates that certain irregular phenomena seen in human pathological voices and baby crying result from nonlinearities in the vocal production system. Equivalent phenomena are quite common in nonhuman mammal vocal repertoires. In particular, bifurcations and chaos are ubiquitous aspects of the normal adult repertoire in many primate species. Here we argue that these phenomena result from properties inherent in the peripheral production mechanism, which allows individuals to generate highly complex and unpredictable vocalizations without requiring equivalently complex neural control mechanisms. We provide examples from the vocal repertoire of rhesus macaques, Macaca mulatta , and other species illustrating the different classes of nonlinear phenomena, and review the concepts from nonlinear dynamics that explicate these calls. Finally, we discuss the evolutionary significance of nonlinear vocal phenomena. We suggest that nonlinear phenomena may subserve individual recognition and the estimation of size or fluctuating asymmetry from vocalizations. Furthermore, neurally ‘cheap’ unpredictability may serve the valuable adaptive function of making chaotic calls difficult to predict and ignore. While noting that nonlinear phenomena are in some cases probably nonadaptive by-products of the physics of the sound-generating mechanism, we suggest that these functional hypotheses provide at least a partial explanation for the ubiquity of nonlinear calls in nonhuman vocal repertoires.

Red deer stags use formants as assessment cues during intrasexual agonistic interactions

While vocal tract resonances or formants are key acoustic parameters that define differences between phonemes in human speech, little is known about their function in animal communication. Here, we used playback experiments to present red deer stags with re-synthesized vocalizations in which formant frequencies were systematically altered to simulate callers of different body sizes. In response to stimuli where lower formants indicated callers with longer vocal tracts, stags were more attentive, replied with more roars and extended their vocal tracts further in these replies. Our results indicate that mammals other than humans use formants in vital vocal exchanges and can adjust their own formant frequencies in relation to those that they hear.

The phonetic potential of nonhuman vocal tracts: comparative cineradiographic observations of vocalizing animals.

For more than a century it has been noted that the adult human vocal tract differs from that of other mammals, in that the resting position of the larynx is much lower in humans. While animals habitually breathe with the larynx inserted into the nasal cavity, adult humans are unable to do this. This anatomical difference has been cited as an important factor limiting the vocal potential of nonhuman animals, because the low larynx of humans allows a wider range of vocal tract shapes and thus formant patterns than is available to other species. However, it is not clear that the static anatomy of dead animals provides an accurate guide to the phonetic potential of the living animals vocal tract. Here I present X-ray video observations of four mammal species (dogs Canis familiaris, goats Capra hircus, pigs Sus scrofa and cotton-top tamarins Sagunius oedipus). In all four species, the larynx was lowered from the nasopharynx, and the velum was closed, during loud calls. In dogs this temporary lowering was particularly pronounced. Although preliminary, these results suggest that the nonhuman vocal tract is more flexible than previously supposed, and that static postmortem anatomy provides an incomplete guide to the phonetic potential of nonhuman animals. The implications of these findings for theories of speech evolution are discussed.

The "domestication syndrome" in mammals: a unified explanation based on neural crest cell behavior and genetics.

Charles Darwin, while trying to devise a general theory of heredity from the observations of animal and plant breeders, discovered that domesticated mammals possess a distinctive and unusual suite of heritable traits not seen in their wild progenitors. Some of these traits also appear in domesticated birds and fish. The origin of Darwin’s “domestication syndrome” has remained a conundrum for more than 140 years. Most explanations focus on particular traits, while neglecting others, or on the possible selective factors involved in domestication rather than the underlying developmental and genetic causes of these traits. Here, we propose that the domestication syndrome results predominantly from mild neural crest cell deficits during embryonic development. Most of the modified traits, both morphological and physiological, can be readily explained as direct consequences of such deficiencies, while other traits are explicable as indirect consequences. We first show how the hypothesis can account for the multiple, apparently unrelated traits of the syndrome and then explore its genetic dimensions and predictions, reviewing the available genetic evidence. The article concludes with a brief discussion of some genetic and developmental questions raised by the idea, along with specific predictions and experimental tests.

Artificial grammar learning meets formal language theory: an overview.

Formal language theory (FLT), part of the broader mathematical theory of computation, provides a systematic terminology and set of conventions for describing rules and the structures they generate, along with a rich body of discoveries and theorems concerning generative rule systems. Despite its name, FLT is not limited to human language, but is equally applicable to computer programs, music, visual patterns, animal vocalizations, RNA structure and even dance. In the last decade, this theory has been profitably used to frame hypotheses and to design brain imaging and animal-learning experiments, mostly using the ‘artificial grammar-learning’ paradigm. We offer a brief, non-technical introduction to FLT and then a more detailed analysis of empirical research based on this theory. We suggest that progress has been hampered by a pervasive conflation of distinct issues, including hierarchy, dependency, complexity and recursion. We offer clarifications of several relevant hypotheses and the experimental designs necessary to test them. We finally review the recent brain imaging literature, using formal languages, identifying areas of convergence and outstanding debates. We conclude that FLT has much to offer scientists who are interested in rigorous empirical investigations of human cognition from a neuroscientific and comparative perspective.

Birds have primate-like numbers of neurons in the forebrain

Significance Birds are remarkably intelligent, although their brains are small. Corvids and some parrots are capable of cognitive feats comparable to those of great apes. How do birds achieve impressive cognitive prowess with walnut-sized brains? We investigated the cellular composition of the brains of 28 avian species, uncovering a straightforward solution to the puzzle: brains of songbirds and parrots contain very large numbers of neurons, at neuronal densities considerably exceeding those found in mammals. Because these “extra” neurons are predominantly located in the forebrain, large parrots and corvids have the same or greater forebrain neuron counts as monkeys with much larger brains. Avian brains thus have the potential to provide much higher “cognitive power” per unit mass than do mammalian brains. Some birds achieve primate-like levels of cognition, even though their brains tend to be much smaller in absolute size. This poses a fundamental problem in comparative and computational neuroscience, because small brains are expected to have a lower information-processing capacity. Using the isotropic fractionator to determine numbers of neurons in specific brain regions, here we show that the brains of parrots and songbirds contain on average twice as many neurons as primate brains of the same mass, indicating that avian brains have higher neuron packing densities than mammalian brains. Additionally, corvids and parrots have much higher proportions of brain neurons located in the pallial telencephalon compared with primates or other mammals and birds. Thus, large-brained parrots and corvids have forebrain neuron counts equal to or greater than primates with much larger brains. We suggest that the large numbers of neurons concentrated in high densities in the telencephalon substantially contribute to the neural basis of avian intelligence.

Finding the beat: a neural perspective across humans and non-human primates

Humans possess an ability to perceive and synchronize movements to the beat in music (‘beat perception and synchronization’), and recent neuroscientific data have offered new insights into this beat-finding capacity at multiple neural levels. Here, we review and compare behavioural and neural data on temporal and sequential processing during beat perception and entrainment tasks in macaques (including direct neural recording and local field potential (LFP)) and humans (including fMRI, EEG and MEG). These abilities rest upon a distributed set of circuits that include the motor cortico-basal-ganglia–thalamo-cortical (mCBGT) circuit, where the supplementary motor cortex (SMA) and the putamen are critical cortical and subcortical nodes, respectively. In addition, a cortical loop between motor and auditory areas, connected through delta and beta oscillatory activity, is deeply involved in these behaviours, with motor regions providing the predictive timing needed for the perception of, and entrainment to, musical rhythms. The neural discharge rate and the LFP oscillatory activity in the gamma- and beta-bands in the putamen and SMA of monkeys are tuned to the duration of intervals produced during a beat synchronization–continuation task (SCT). Hence, the tempo during beat synchronization is represented by different interval-tuned cells that are activated depending on the produced interval. In addition, cells in these areas are tuned to the serial-order elements of the SCT. Thus, the underpinnings of beat synchronization are intrinsically linked to the dynamics of cell populations tuned for duration and serial order throughout the mCBGT. We suggest that a cross-species comparison of behaviours and the neural circuits supporting them sets the stage for a new generation of neurally grounded computational models for beat perception and synchronization.