Voice processing in human and non-human primates

Humans share with non-human primates a number of voice perception abilities of crucial importance in social interactions, such as the ability to identify a conspecific individual from its vocalizations. Speech perception is likely to have evolved in our ancestors on the basis of pre-existing neural mechanisms involved in extracting behaviourally relevant information from conspecific vocalizations (CVs). Studying the neural bases of voice perception in primates thus not only has the potential to shed light on cerebral mechanisms that may be--unlike those involved in speech perception--directly homologous between species, but also has direct implications for our understanding of how speech appeared in humans. In this comparative review, we focus on behavioural and neurobiological evidence relative to two issues central to voice perception in human and non-human primates: (i) are CVs 'special', i.e. are they analysed using dedicated cerebral mechanisms not used for other sound categories, and (ii) to what extent and using what neural mechanisms do primates identify conspecific individuals from their vocalizations?     

Primate vocal communication: a useful tool for understanding human speech and language evolution?

Language is a uniquely human trait, and questions of how and why it evolved have been intriguing scientists for years. Nonhuman primates (primates) are our closest living relatives, and their behavior can be used to estimate the capacities of our extinct ancestors. As humans and many primate species rely on vocalizations as their primary mode of communication, the vocal behavior of primates has been an obvious target for studies investigating the evolutionary roots of human speech and language. By studying the similarities and differences between human and primate vocalizations, comparative research has the potential to clarify the evolutionary processes that shaped human speech and language. This review examines some of the seminal and recent studies that contribute to our knowledge regarding the link between primate calls and human language and speech. We focus on three main aspects of primate vocal behavior: functional reference, call combinations, and vocal learning. Studies in these areas indicate that despite important differences, primate vocal communication exhibits some key features characterizing human language. They also indicate, however, that some critical aspects of speech, such as vocal plasticity, are not shared with our primate cousins. We conclude that comparative research on primate vocal behavior is a very promising tool for deepening our understanding of the evolution of human speech and language, but much is still to be done as many aspects of monkey and ape vocalizations remain largely unexplored.     

Early specialization for voice and emotion processing in the infant brain

Human voices play a fundamental role in social communication, and areas of the adult "social brain" show specialization for processing voices and their emotional content (superior temporal sulcus, inferior prefrontal cortex, premotor cortical regions, amygdala, and insula). However, it is unclear when this specialization develops. Functional magnetic resonance (fMRI) studies suggest that the infant temporal cortex does not differentiate speech from music or backward speech, but a prior study with functional near-infrared spectroscopy revealed preferential activation for human voices in 7-month-olds, in a more posterior location of the temporal cortex than in adults. However, the brain networks involved in processing nonspeech human vocalizations in early development are still unknown. To address this issue, in the present fMRI study, 3- to 7-month-olds were presented with adult nonspeech vocalizations (emotionally neutral, emotionally positive, and emotionally negative) and nonvocal environmental sounds. Infants displayed significant differential activation in the anterior portion of the temporal cortex, similarly to adults. Moreover, sad vocalizations modulated the activity of brain regions involved in processing affective stimuli such as the orbitofrontal cortex and insula. These results suggest remarkably early functional specialization for processing human voice and negative emotions.     

On the pursuit of the brain network for proto-syntactic learning in non-human primates: conceptual issues and neurobiological hypotheses

Songbirds have become impressive neurobiological models for aspects of human verbal communication because they learn to sequence their song elements, analogous, in some ways, to how humans learn to produce spoken sequences with syntactic structure. However, mammals such as non-human primates are considered to be at best limited-vocal learners and not able to sequence their vocalizations, although some of these animals can learn certain 'artificial grammar' sequences. Thus, conceptual issues have slowed the progress in exploring potential neurobiological homologues to language-related processes in species that are taxonomically closely related to humans. We consider some of the conceptual issues impeding a pursuit of, as we define them, 'proto-syntactic' capabilities and their neuronal substrates in non-human animals. We also discuss ways to better bridge comparative behavioural and neurobiological data between humans and other animals. Finally, we propose guiding neurobiological hypotheses with which we aim to facilitate the future testing of the level of correspondence between the human brain network for syntactic-learning and related neurobiological networks present in other primates. Insights from the study of non-human primates and other mammals are likely to complement those being obtained in birds to further our knowledge of the human language-related network at the cellular level.     

Deconstructing language by comparative gene expression: from neurobiology to microarray

Language is a defining characteristic of our species that has emerged quite recently on an evolutionary timescale. Understanding the neurobiological substrates and genetic underpinnings of language constitutes a basic challenge for both neuroscience and genetics. The functional localization of language in the brain has been progressively refined over the last century through studies of aphasics and more recently through neuroimaging. Concurrently, structural specializations in these brain regions have been identified by virtue of their lateralization in humans and also through comparisons with homologous brain regions in non-human primate species. Comparative genomics has revealed the genome of our closest living relative, the chimpanzee, to be astonishingly similar to our own. To explore the role that changes in the regulation of gene expression have had in recent human evolution, several groups have used microarrays to compare expression levels for thousands of genes in the brain between humans and chimpanzees. By applying this approach to the increasingly refined peri-sylvian network of brain regions involved in language, it may be possible to discern functionally significant changes in gene expression that are universal among humans but unique to our species, thus casting light on the molecular basis of language in the brain.     

Deconstructing language by comparative gene expression: from neurobiology to microarray

Language is a defining characteristic of our species that has emerged quite recently on an evolutionary timescale. Understanding the neurobiological substrates and genetic underpinnings of language constitutes a basic challenge for both neuroscience and genetics. The functional localization of language in the brain has been progressively refined over the last century through studies of aphasics and more recently through neuroimaging. Concurrently, structural specializations in these brain regions have been identified by virtue of their lateralization in humans and also through comparisons with homologous brain regions in non-human primate species. Comparative genomics has revealed the genome of our closest living relative, the chimpanzee, to be astonishingly similar to our own. To explore the role that changes in the regulation of gene expression have had in recent human evolution, several groups have used microarrays to compare expression levels for thousands of genes in the brain between humans and chimpanzees. By applying this approach to the increasingly refined peri-sylvian network of brain regions involved in language, it may be possible to discern functionally significant changes in gene expression that are universal among humans but unique to our species, thus casting light on the molecular basis of language in the brain.     

Bird speech perception and vocal production: a comparison with humans

Research into speech perception by nonhuman animals can be crucially informative in assessing whether specific perceptual phenomena in humans have evolved to decode speech, or reflect more general traits. Birds share with humans not only the capacity to use complex vocalizations for communication but also many characteristics of its underlying developmental and mechanistic processes; thus, birds are a particularly interesting group for comparative study. This review first discusses commonalities between birds and humans in perception of speech sounds. Several psychoacoustic studies have shown striking parallels in seemingly speech-specific perceptual phenomena, such as categorical perception of voice-onset-time variation, categorization of consonants that lack phonetic invariance, and compensation for coarticulation. Such findings are often regarded as evidence for the idea that the objects of human speech perception are auditory or acoustic events rather than articulations. Next, I highlight recent research on the production side of avian communication that has revealed the existence of vocal tract filtering and articulation in bird species-specific vocalization, which has traditionally been considered a hallmark of human speech production. Together, findings in birds show that many of characteristics of human speech perception are not uniquely human but also that a comparative approach to the question of what are the objects of perception--articulatory or auditory events--requires careful consideration of species-specific vocal production mechanisms.     

Monkeys and humans share a common computation for face/voice integration

Speech production involves the movement of the mouth and other regions of the face resulting in visual motion cues. These visual cues enhance intelligibility and detection of auditory speech. As such, face-to-face speech is fundamentally a multisensory phenomenon. If speech is fundamentally multisensory, it should be reflected in the evolution of vocal communication: similar behavioral effects should be observed in other primates. Old World monkeys share with humans vocal production biomechanics and communicate face-to-face with vocalizations. It is unknown, however, if they, too, combine faces and voices to enhance their perception of vocalizations. We show that they do: monkeys combine faces and voices in noisy environments to enhance their detection of vocalizations. Their behavior parallels that of humans performing an identical task. We explored what common computational mechanism(s) could explain the pattern of results we observed across species. Standard explanations or models such as the principle of inverse effectiveness and a "race" model failed to account for their behavior patterns. Conversely, a "superposition model", positing the linear summation of activity patterns in response to visual and auditory components of vocalizations, served as a straightforward but powerful explanatory mechanism for the observed behaviors in both species. As such, it represents a putative homologous mechanism for integrating faces and voices across primates.     

Language, Handedness, and Primate Brains: Did the Australopithecines Sign?

Evidence from comparative primate neuroanatomy, archaeology, and studies of vocalization systems of nonhuman primates suggests that human vocal language has a long evolutionary history and that there is continuity between our early primate ancestors' call systems and human speech. Old World monkeys exhibit cerebral asymmetries similar to those that appear related to human language. If arboreal monkeylike ancestors of humans were also characterized by cerebral asymmetry, then the fundamental asymmetry that forms the neurological substrate for human language may have been established through selection for simple "discrete" call systems in an arboreal habitat and would have occurred much longer ago than previously thought. The eventual shift from an arboreal to a terrestrial habitat was accompanied by increased complexity ("gradation") of vocal communication systems. The archaeological record of tools suggests that communication systems became still more complex under the selective pressures that led to bipedalism and that language had been selected for by the time that bipedalism was achieved. Contrary to the gestural hypothesis, right-handedness (which could not have preceded freeing of the hands) succeeded speech and may have been due to selective pressures for increased complexity of communication, causing a Field Effect upon the brain. [australopithecine, cerebral asymmetry, language, primate brains, right-handedness]     

Children's development of self-regulation in speech production

Species-specific vocalizations fall into two broad categories: those that emerge during maturation, independent of experience, and those that depend on early life interactions with conspecifics. Human language and the communication systems of a small number of other species, including songbirds, fall into this latter class of vocal learning. Self-monitoring has been assumed to play an important role in the vocal learning of speech and studies demonstrate that perception of your own voice is crucial for both the development and lifelong maintenance of vocalizations in humans and songbirds. Experimental modifications of auditory feedback can also change vocalizations in both humans and songbirds. However, with the exception of large manipulations of timing, no study to date has ever directly examined the use of auditory feedback in speech production under the age of 4. Here we use a real-time formant perturbation task to compare the response of toddlers, children, and adults to altered feedback. Children and adults reacted to this manipulation by changing their vowels in a direction opposite to the perturbation. Surprisingly, toddlers' speech didn't change in response to altered feedback, suggesting that long-held assumptions regarding the role of self-perception in articulatory development need to be reconsidered.     

Neural overlap in processing music and speech

Neural overlap in processing music and speech, as measured by the co-activation of brain regions in neuroimaging studies, may suggest that parts of the neural circuitries established for language may have been recycled during evolution for musicality, or vice versa that musicality served as a springboard for language emergence. Such a perspective has important implications for several topics of general interest besides evolutionary origins. For instance, neural overlap is an important premise for the possibility of music training to influence language acquisition and literacy. However, neural overlap in processing music and speech does not entail sharing neural circuitries. Neural separability between music and speech may occur in overlapping brain regions. In this paper, we review the evidence and outline the issues faced in interpreting such neural data, and argue that converging evidence from several methodologies is needed before neural overlap is taken as evidence of sharing.     

非人灵长类声音通讯的研究进展

声音通讯是非人灵长类研究一个重要的研究领域,有助于了解非人灵长类的社会行为、个体关系、行为进化和社会演化等,甚至对探究人类语言起源和进化等方面也具有十分重要的意义。本文通过对非人灵长类声音通讯的研究内容、影响因素和研究方法等进行了梳理,探讨非人灵长类声音通讯研究的前景和展望,旨在进一步推动国内非人灵长类声音通讯研究的深入,同时为相关研究提供借鉴和参考。     

The Functional Connectome of Speech Control

In the past few years, several studies have been directed to understanding the complexity of functional interactions between different brain regions during various human behaviors. Among these, neuroimaging research installed the notion that speech and language require an orchestration of brain regions for comprehension, planning, and integration of a heard sound with a spoken word. However, these studies have been largely limited to mapping the neural correlates of separate speech elements and examining distinct cortical or subcortical circuits involved in different aspects of speech control. As a result, the complexity of the brain network machinery controlling speech and language remained largely unknown. Using graph theoretical analysis of functional MRI (fMRI) data in healthy subjects, we quantified the large-scale speech network topology by constructing functional brain networks of increasing hierarchy from the resting state to motor output of meaningless syllables to complex production of real-life speech as well as compared to non-speech-related sequential finger tapping and pure tone discrimination networks. We identified a segregated network of highly connected local neural communities (hubs) in the primary sensorimotor and parietal regions, which formed a commonly shared core hub network across the examined conditions, with the left area 4p playing an important role in speech network organization. These sensorimotor core hubs exhibited features of flexible hubs based on their participation in several functional domains across different networks and ability to adaptively switch long-range functional connectivity depending on task content, resulting in a distinct community structure of each examined network. Specifically, compared to other tasks, speech production was characterized by the formation of six distinct neural communities with specialized recruitment of the prefrontal cortex, insula, putamen, and thalamus, which collectively forged the formation of the functional speech connectome. In addition, the observed capacity of the primary sensorimotor cortex to exhibit operational heterogeneity challenged the established concept of unimodality of this region.     

Auditory processing--speech, space and auditory objects

There have been recent developments in our understanding of the auditory neuroscience of non-human primates that, to a certain extent, can be integrated with findings from human functional neuroimaging studies. This framework can be used to consider the cortical basis of complex sound processing in humans, including implications for speech perception, spatial auditory processing and auditory scene segregation.     

Responses to Vocalizations and Auditory Controls in the Human Newborn Brain

In the adult brain, speech can recruit a brain network that is overlapping with, but not identical to, that involved in perceiving non-linguistic vocalizations. Using the same stimuli that had been presented to human 4-month-olds and adults, as well as adult macaques, we sought to shed light on the cortical networks engaged when human newborns process diverse vocalization types. Near infrared spectroscopy was used to register the response of 40 newborns'' perisylvian regions when stimulated with speech, human and macaque emotional vocalizations, as well as auditory controls where the formant structure was destroyed but the long-term spectrum was retained. Left fronto-temporal and parietal regions were significantly activated in the comparison of stimulation versus rest, with unclear selectivity in cortical activation. These results for the newborn brain are qualitatively and quantitatively compared with previous work on newborns, older human infants, adult humans, and adult macaques reported in previous work.     

Functional imaging of the auditory processing applied to speech sounds

In this paper, we describe domain-general auditory processes that we believe are prerequisite to the linguistic analysis of speech. We discuss biological evidence for these processes and how they might relate to processes that are specific to human speech and language. We begin with a brief review of (i) the anatomy of the auditory system and (ii) the essential properties of speech sounds. Section 4 describes the general auditory mechanisms that we believe are applied to all communication sounds, and how functional neuroimaging is being used to map the brain networks associated with domain-general auditory processing. Section 5 discusses recent neuroimaging studies that explore where such general processes give way to those that are specific to human speech and language.     

Communicative signaling activates 'Broca's' homolog in chimpanzees

Broca's area, a cerebral cortical area located in the inferior frontal gyrus (IFG) of the human brain, has been identified as one of several critical regions associated with the motor planning and execution of language. Anatomically, Broca's area is most often larger in the left hemisphere, and functional imaging studies in humans indicate significant left-lateralized patterns of activation during language-related tasks. If, and to what extent, nonhuman primates, particularly chimpanzees, possess a homologous region that is involved in the production of their own communicative signals remains unknown. Here, we show that portions of the IFG as well as other cortical and subcortical regions in chimpanzees are active during the production of communicative signals. These findings are the first to provide direct evidence of the neuroanatomical structures associated with the production of communicative behaviors in chimpanzees. Significant activation in the left IFG in conjunction with other cortical and subcortical brain areas during the production of communicative signals in chimpanzees suggests that the neurological substrates underlying language production in the human brain may have been present in the common ancestor of humans and chimpanzees.     

Vervet monkeys and humans show brain asymmetries for processing conspecific vocalizations, but with opposite patterns of laterality

A robust finding in the human neurosciences is the observation of a left hemisphere specialization for processing spoken language. Previous studies suggest that this auditory specialization and brain asymmetry derive from a primate ancestor. Most of these studies focus on the genus Macaca and all demonstrate a left hemisphere bias. Due to the narrow taxonomic scope, however, we lack a sense of the distribution of this asymmetry among primates. Further, although the left hemisphere bias appears mediated by conspecific calls, other possibilities exist including familiarity, emotional relevance and more general acoustic properties of the signal. To broaden the taxonomic scope and test the specificity of the apparent hemisphere bias, we conducted an experiment on vervets (Cercopithecus aethiops)-a different genus of old world monkeys and implemented the relevant acoustic controls. Using the same head orienting procedure tested with macaques, results show a strong left ear/right hemisphere bias for conspecific vocalizations (both familiar and unfamiliar), but no asymmetry for other primate vocalizations or non-biological sounds. These results suggest that although auditory asymmetries for processing species-specific vocalizations are a common feature of the primate brain, the direction of this asymmetry may be relatively plastic. This finding raises significant questions for how ontogenetic and evolutionary forces have impacted on primate brain evolution.     

When the hands speak.

In the present review we will summarize evidence that the control of spoken language shares the same system involved in the control of arm gestures. Studies of primate premotor cortex discovered the existence of the so-called mirror system as well as of a system of double commands to hand and mouth. These systems may have evolved initially in the context of ingestion, and later formed a platform for combined manual and vocal communication. In humans, manual gestures are integrated with speech production, when they accompany speech. Lip kinematics and parameters of voice spectra during speech production are influenced by executing or observing transitive actions (i.e. guided by an object). Manual actions also play an important role in language acquisition in children, from the babbling stage onwards. Behavioural data reported here even show a reciprocal influence between words and symbolic gestures and studies employing neuroimaging and repetitive transcranial magnetic stimulation (rTMS) techniques suggest that the system governing both speech and gesture is located in Broca's area.     

Convergent differential regulation of parvalbumin in the brains of vocal learners

Spoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65-300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.