Animal Communication Teach Research Articles

What can animal communication teach us about human language?

Language has been considered by many to be uniquely human. Numerous theories for how it evolved have been proposed but rarely tested. The articles in this theme issue consider the extent to which aspects of language, such as vocal learning, phonology, syntax, semantics, intentionality, cognition and neurobiological adaptations, are shared with other animals. By adopting a comparative approach, insights into the mechanisms and origins of human language can be gained. While points of agreement exist among the authors, conflicting viewpoints are expressed on several issues, such as the presence of proto-syntax in animal communication, the neural basis of the Merge operation, and the neurogenetic changes necessary for vocal learning. Future comparative research in animal communication has the potential to teach us even more about the evolution, neurobiology and cognitive basis of human language. This article is part of the theme issue 'What can animal communication teach us about human language?'

Birdsong as a window into language origins and evolutionary neuroscience.

Humans and songbirds share the key trait of vocal learning, manifested in speech and song, respectively. Striking analogies between these behaviours include that both are acquired during developmental critical periods when the brain's ability for vocal learning peaks. Both behaviours show similarities in the overall architecture of their underlying brain areas, characterized by cortico-striato-thalamic loops and direct projections from cortical neurons onto brainstem motor neurons that control the vocal organs. These neural analogies extend to the molecular level, with certain song control regions sharing convergent transcriptional profiles with speech-related regions in the human brain. This evolutionary convergence offers an unprecedented opportunity to decipher the shared neurogenetic underpinnings of vocal learning. A key strength of the songbird model is that it allows for the delineation of activity-dependent transcriptional changes in the brain that are driven by learned vocal behaviour. To capitalize on this advantage, we used previously published datasets from our laboratory that correlate gene co-expression networks to features of learned vocalization within and after critical period closure to probe the functional relevance of genes implicated in language. We interrogate specific genes and cellular processes through converging lines of evidence: human-specific evolutionary changes, intelligence-related phenotypes and relevance to vocal learning gene co-expression in songbirds. This article is part of the theme issue 'What can animal communication teach us about human language?'

Scratching beneath the surface: intentionality in great ape signal production.

Despite important similarities having been found between human and animal communication systems, surprisingly little research effort has focussed on whether the cognitive mechanisms underpinning these behaviours are also similar. In particular, it is highly debated whether signal production is the result of reflexive processes, or can be characterized as intentional. Here, we critically evaluate the criteria that are used to identify signals produced with different degrees of intentionality, and discuss recent attempts to apply these criteria to the vocal, gestural and multimodal communicative signals of great apes and more distantly related species. Finally, we outline the necessary research tools, such as physiologically validated measures of arousal, and empirical evidence that we believe would propel this debate forward and help unravel the evolutionary origins of human intentional communication. This article is part of the theme issue 'What can animal communication teach us about human language?'

Animal cognition and the evolution of human language: why we cannot focus solely on communication.

Studies of animal communication are often assumed to provide the ‘royal road’ to understanding the evolution of human language. After all, language is the pre-eminent system of human communication: doesn't it make sense to search for its precursors in animal communication systems? From this viewpoint, if some characteristic feature of human language is lacking in systems of animal communication, it represents a crucial gap in evolution, and evidence for an evolutionary discontinuity. Here I argue that we should reverse this logic: because a defining feature of human language is its ability to flexibly represent and recombine concepts, precursors for many important components of language should be sought in animal cognition rather than animal communication. Animal communication systems typically only permit expression of a small subset of the concepts that can be represented and manipulated by that species. Thus, if a particular concept is not expressed in a species' communication system this is not evidence that it lacks that concept. I conclude that if we focus exclusively on communicative signals, we sell the comparative analysis of language evolution short. Therefore, animal cognition provides a crucial (and often neglected) source of evidence regarding the biology and evolution of human language.This article is part of the theme issue ‘What can animal communication teach us about human language?’

The neurobiology of innate, volitional and learned vocalizations in mammals and birds.

Vocalization is an ancient vertebrate trait essential to many forms of communication, ranging from courtship calls to free verse. Vocalizations may be entirely innate and evoked by sexual cues or emotional state, as with many types of calls made in primates, rodents and birds; volitional, as with innate calls that, following extensive training, can be evoked by arbitrary sensory cues in non-human primates and corvid songbirds; or learned, acoustically flexible and complex, as with human speech and the courtship songs of oscine songbirds. This review compares and contrasts the neural mechanisms underlying innate, volitional and learned vocalizations, with an emphasis on functional studies in primates, rodents and songbirds. This comparison reveals both highly conserved and convergent mechanisms of vocal production in these different groups, despite their often vast phylogenetic separation. This similarity of central mechanisms for different forms of vocal production presents experimentalists with useful avenues for gaining detailed mechanistic insight into how vocalizations are employed for social and sexual signalling, and how they can be modified through experience to yield new vocal repertoires customized to the individual's social group. This article is part of the theme issue 'What can animal communication teach us about human language?'

A taxonomy for vocal learning.

Humans and songbirds learn to sing or speak by listening to acoustic models, forming auditory templates, and then learning to produce vocalizations that match the templates. These taxa have evolved specialized telencephalic pathways to accomplish this complex form of vocal learning, which has been reported for very few other taxa. By contrast, the acoustic structure of most animal vocalizations is produced by species-specific vocal motor programmes in the brainstem that do not require auditory feedback. However, many mammals and birds can learn to fine-tune the acoustic features of inherited vocal motor patterns based upon listening to conspecifics or noise. These limited forms of vocal learning range from rapid alteration based on real-time auditory feedback to long-term changes of vocal repertoire and they may involve different mechanisms than complex vocal learning. Limited vocal learning can involve the brainstem, mid-brain and/or telencephalic networks. Understanding complex vocal learning, which underpins human speech, requires careful analysis of which species are capable of which forms of vocal learning. Selecting multiple animal models for comparing the neural pathways that generate these different forms of learning will provide a richer view of the evolution of complex vocal learning and the neural mechanisms that make it possible.This article is part of the theme issue ‘What can animal communication teach us about human language?’

Towards a new taxonomy of primate vocal production learning.

The extent to which vocal learning can be found in nonhuman primates is key to reconstructing the evolution of speech. Regarding the adjustment of vocal output in relation to auditory experience (vocal production learning in the narrow sense), effects on the ontogenetic trajectory of vocal development as well as adjustment to group-specific call features have been found. Yet, a comparison of the vocalizations of different primate genera revealed striking similarities in the structure of calls and repertoires in different species of the same genus, indicating that the structure of nonhuman primate vocalizations is highly conserved. Thus, modifications in relation to experience only appear to be possible within relatively tight species-specific constraints. By contrast, comprehension learning may be extremely rapid and open-ended. In conjunction, these findings corroborate the idea of an ancestral independence of vocal production and auditory comprehension learning. To overcome the futile debate about whether or not vocal production learning can be found in nonhuman primates, we suggest putting the focus on the different mechanisms that may mediate the adjustment of vocal output in response to experience; these mechanisms may include auditory facilitation and learning from success. This article is part of the theme issue 'What can animal communication teach us about human language?'

Some cautions regarding the phonological continuity hypothesis.

We consider the Phonological Continuity Hypothesis (PCH) of Fitch (2018) in light of a broader range of formal systems. A consideration of the learning and generalization of simple patterns such as AAB from Marcus (Marcus 2000 Curr. Dir. 9, 145-147(doi:10.1111/1467-8721.00080)) shows that finite-state automata defined in the standard way fail to generalize in a compatible fashion. However, pushdown automata with finite-memory limits do show compatible generalization capabilities. The third class of formal systems-tree automata-provide yet another possibility for the processing of words within sentences. We conclude that there are additional possible formal differences between sound patterns and sentence patterns, which will make testing the PCH even more difficult. This article is part of the theme issue 'What can animal communication teach us about human language?'

The syntax-semantics interface in animal vocal communication.

Syntax (rules for combining words or elements) and semantics (meaning of expressions) are two pivotal features of human language, and interaction between them allows us to generate a limitless number of meaningful expressions. While both features were traditionally thought to be unique to human language, research over the past four decades has revealed intriguing parallels in animal communication systems. Many birds and mammals produce specific calls with distinct meanings, and some species combine multiple meaningful calls into syntactically ordered sequences. However, it remains largely unclear whether, like phrases or sentences in human language, the meaning of these call sequences depends on both the meanings of the component calls and their syntactic order. Here, leveraging recently demonstrated examples of meaningful call combinations, we introduce a framework for exploring the interaction between syntax and semantics (i.e. the syntax-semantic interface) in animal vocal sequences. We outline methods to test the cognitive mechanisms underlying the production and perception of animal vocal sequences and suggest potential evolutionary scenarios for syntactic communication. We hope that this review will stimulate phenomenological studies on animal vocal sequences as well as experimental studies on the cognitive processes, which promise to provide further insights into the evolution of language. This article is part of the theme issue 'What can animal communication teach us about human language?'

Syntax and compositionality in animal communication.

Syntax has been found in animal communication but only humans appear to have generative, hierarchically structured syntax. How did syntax evolve? I discuss three theories of evolutionary transition from animal to human syntax: computational capacity, structural flexibility and event perception. The computation hypothesis is supported by artificial grammar experiments consistently showing that only humans can learn linear stimulus sequences with an underlying hierarchical structure, a possible by-product of computationally powerful large brains. The structural flexibility hypothesis is supported by evidence of meaning-bearing combinatorial and permutational signal sequences in animals, with sometimes compositional features, but no evidence for generativity or hierarchical structure. Again, animals may be constrained by computational limits in short-term memory but possibly also by limits in articulatory control and social cognition. The event categorization hypothesis, finally, posits that humans are cognitively predisposed to analyse natural events by assigning agency and assessing how agents impact on patients, a propensity that is reflected by the basic syntactic units in all languages. Whether animals perceive natural events in the same way is largely unknown, although event perception may provide the cognitive grounding for syntax evolution. This article is part of the theme issue 'What can animal communication teach us about human language?'

Exploring the cerebral substrate of voice perception in primate brains.

One can consider human language to be the Swiss army knife of the vast domain of animal communication. There is now growing evidence suggesting that this technology may have emerged from already operational material instead of being a sudden innovation. Sharing ideas and thoughts with conspecifics via language constitutes an amazing ability, but what value would it hold if our conspecifics were not first detected and recognized? Conspecific voice (CV) perception is fundamental to communication and widely shared across the animal kingdom. Two questions that arise then are: is this apparently shared ability reflected in common cerebral substrate? And, how has this substrate evolved? The paper addresses these questions by examining studies on the cerebral basis of CV perception in humans' closest relatives, non-human primates. Neuroimaging studies, in particular, suggest the existence of a ‘voice patch system’, a network of interconnected cortical areas that can provide a common template for the cerebral processing of CV in primates.This article is part of the theme issue ‘What can animal communication teach us about human language?’

Behaviour, biology and evolution of vocal learning in bats.

The comparative approach can provide insight into the evolution of human speech, language and social communication by studying relevant traits in animal systems. Bats are emerging as a model system with great potential to shed light on these processes given their learned vocalizations, close social interactions, and mammalian brains and physiology. A recent framework outlined the multiple levels of investigation needed to understand vocal learning across a broad range of non-human species, including cetaceans, pinnipeds, elephants, birds and bats. Here, we apply this framework to the current state-of-the-art in bat research. This encompasses our understanding of the abilities bats have displayed for vocal learning, what is known about the timing and social structure needed for such learning, and current knowledge about the prevalence of the trait across the order. It also addresses the biology (vocal tract morphology, neurobiology and genetics) and evolution of this trait. We conclude by highlighting some key questions that should be answered to advance our understanding of the biological encoding and evolution of speech and spoken communication. This article is part of the theme issue 'What can animal communication teach us about human language?'

Hierarchy processing in human neurobiology: how specific is it?

Although human and non-human animals share a number of perceptual and cognitive abilities, they differ in their ability to process hierarchically structured sequences. This becomes most evident in the human capacity to process natural language characterized by structural hierarchies. This capacity is neuroanatomically grounded in the posterior part of left Broca's area (Brodmann area (BA) 44), located in the inferior frontal gyrus, and its dorsal white matter fibre connection to the temporal cortex. Within this neural network, BA 44 itself subserves hierarchy building and the strength of its connection to the temporal cortex correlates with the processing of syntactically complex sentences. Whether these brain structures are also relevant for other human cognitive abilities is a current debate. Here, this question will be evaluated with respect to those human cognitive abilities that are assumed to require hierarchy building, such as music, mathematics and Theory of Mind. Rather than supporting a domain-general view, the data indicate domain-selective neural networks as the neurobiological basis for processing hierarchy in different cognitive domains. Recent cross-species white matter comparisons suggest that particular connections within the networks may make the crucial difference in the brain structure of human and non-human primates, thereby enabling cognitive functions specific to humans. This article is part of the theme issue 'What can animal communication teach us about human language?'

Sound sequences in birdsong: how much do birds really care?

The complex and melodic nature of many birds' songs has raised interest in potential parallels between avian vocal sequences and human speech. The similarities between birdsong and speech in production and learning are well established, but surprisingly little is known about how birds perceive song sequences. One popular laboratory songbird, the zebra finch (Taeniopygia guttata), has recently attracted attention as an avian model for human speech, in part because the male learns to produce the individual elements in its song motif in a fixed sequence. But psychoacoustic evidence shows that adult zebra finches are relatively insensitive to the sequential features of song syllables. Instead, zebra finches and other birds seem to be exquisitely sensitive to the acoustic details of individual syllables to a degree that is beyond human hearing capacity. Based on these findings, we present a finite-state model of zebra finch perception of song syllable sequences and discuss the rich informational capacity of their vocal system. Furthermore, we highlight the abilities of budgerigars (Melopsittacus undulatus), a parrot species, to hear sequential features better than zebra finches and suggest that neurophysiological investigations comparing these species could prove fruitful for uncovering neural mechanisms for auditory sequence perception in human speech. This article is part of the theme issue 'What can animal communication teach us about human language?'

Becoming human: human infants link language and cognition, but what about the other great apes?

Human language has no parallel elsewhere in the animal kingdom. It is unique not only for its structural complexity but also for its inextricable interface with core cognitive capacities such as object representation, object categorization and abstract rule learning. Here, we (i) review recent evidence documenting how (and how early) language interacts with these core cognitive capacities in the mind of the human infant, and (ii) consider whether this link exists in non-human great apes-our closest genealogical cousins. Research with human infants demonstrates that well before they begin to speak, infants have already forged a link between language and core cognitive capacities. Evident by just three months of age, this language-cognition link unfolds in a rich developmental cascade, with each advance providing the foundation for subsequent, more precise and more powerful links. This link supports our species' capacity to represent and convey abstract concepts and to communicate beyond the immediate here and now. By contrast, although the communication systems of great apes are sophisticated in their own right, there is no conclusive evidence that apes establish reference, convey information declaratively or pass down communicative devices via cultural transmission. Thus, the evidence currently available reinforces the uniqueness of human language and the power of its interface to cognition. This article is part of the theme issue 'What can animal communication teach us about human language?'