The slings and arrows of comparative linguistics.

In this Formal Comment the authors respond to objections to their previous Essay, reiterating that comparative linguistics is not an easy undertaking.

Meaningful syntactic structure in songbird vocalizations?

The faculty of language is thought to be uniquely human. Recently, it has been claimed that songbirds are able to associate meaning with sound, comparable to the way that humans do. In human language, the meaning of expressions (semantics) is dependent on a mind-internal hierarchical structure (syntax). Meaning is associated with structure through the principle of compositionality, whereby the meaning of a complex expression is a function of the meaning of its constituent parts and the mode of composition. We argue that while recent experimental findings on songbird call sequences offer exciting novel insights into animal communication, despite claims to the contrary, they are quite unlike what we find in human language. There are indeed remarkable behavioral and neural parallels in auditory-vocal imitation learning between songbirds and human infants that are absent in our closest evolutionary relatives, the great apes. But so far, there is no convincing evidence of syntax-determined meaning in nonhuman animals.

Language: UG or not to be, that is the question.

Language is not the same as speech or communication; rather, it is a computational cognitive system. It has appeared very recently, consistent with a minimalist view of language's hierarchical syntactic structure.

How could language have evolved?

The evolution of the faculty of language largely remains an enigma. In this essay, we ask why. Language's evolutionary analysis is complicated because it has no equivalent in any nonhuman species. There is also no consensus regarding the essential nature of the language "phenotype." According to the "Strong Minimalist Thesis," the key distinguishing feature of language (and what evolutionary theory must explain) is hierarchical syntactic structure. The faculty of language is likely to have emerged quite recently in evolutionary terms, some 70,000-100,000 years ago, and does not seem to have undergone modification since then, though individual languages do of course change over time, operating within this basic framework. The recent emergence of language and its stability are both consistent with the Strong Minimalist Thesis, which has at its core a single repeatable operation that takes exactly two syntactic elements a and b and assembles them to form the set {a, b}.

Twitter evolution: converging mechanisms in birdsong and human speech.

Vocal imitation in human infants and in some orders of birds relies on auditory-guided motor learning during a sensitive period of development. It proceeds from 'babbling' (in humans) and 'subsong' (in birds) through distinct phases towards the full-fledged communication system. Language development and birdsong learning have parallels at the behavioural, neural and genetic levels. Different orders of birds have evolved networks of brain regions for song learning and production that have a surprisingly similar gross anatomy, with analogies to human cortical regions and basal ganglia. Comparisons between different songbird species and humans point towards both general and species-specific principles of vocal learning and have identified common neural and molecular substrates, including the forkhead box P2 (FOXP2) gene.

Human-like brain hemispheric dominance in birdsong learning.

Unlike nonhuman primates, songbirds learn to vocalize very much like human infants acquire spoken language. In humans, Broca's area in the frontal lobe and Wernicke's area in the temporal lobe are crucially involved in speech production and perception, respectively. Songbirds have analogous brain regions that show a similar neural dissociation between vocal production and auditory perception and memory. In both humans and songbirds, there is evidence for lateralization of neural responsiveness in these brain regions. Human infants already show left-sided dominance in their brain activation when exposed to speech. Moreover, a memory-specific left-sided dominance in Wernicke's area for speech perception has been demonstrated in 2.5-mo-old babies. It is possible that auditory-vocal learning is associated with hemispheric dominance and that this association arose in songbirds and humans through convergent evolution. Therefore, we investigated whether there is similar song memory-related lateralization in the songbird brain. We exposed male zebra finches to tutor or unfamiliar song. We found left-sided dominance of neuronal activation in a Broca-like brain region (HVC, a letter-based name) of juvenile and adult zebra finch males, independent of the song stimulus presented. In addition, juvenile males showed left-sided dominance for tutor song but not for unfamiliar song in a Wernicke-like brain region (the caudomedial nidopallium). Thus, left-sided dominance in the caudomedial nidopallium was specific for the song-learning phase and was memory-related. These findings demonstrate a remarkable neural parallel between birdsong and human spoken language, and they have important consequences for our understanding of the evolution of auditory-vocal learning and its neural mechanisms.

Darwin in mind: new opportunities for evolutionary psychology.

Evolutionary Psychology (EP) views the human mind as organized into many modules, each underpinned by psychological adaptations designed to solve problems faced by our Pleistocene ancestors. We argue that the key tenets of the established EP paradigm require modification in the light of recent findings from a number of disciplines, including human genetics, evolutionary biology, cognitive neuroscience, developmental psychology, and paleoecology. For instance, many human genes have been subject to recent selective sweeps; humans play an active, constructive role in co-directing their own development and evolution; and experimental evidence often favours a general process, rather than a modular account, of cognition. A redefined EP could use the theoretical insights of modern evolutionary biology as a rich source of hypotheses concerning the human mind, and could exploit novel methods from a variety of adjacent research fields.

Comparative analyses of speech and language converge on birds.

Unlike nonhuman primates, thousands of bird species have articulatory capabilities that equal or surpass those of humans, and they develop their vocalizations through vocal imitation in a way that is very similar to how human infants learn to speak. An understanding of how speech mechanisms have evolved is therefore unlikely to yield key insights into how the human brain is special.

From songs to synapses: molecular mechanisms of birdsong memory. Molecular mechanisms of auditory learning in songbirds involve immediate early genes, including zenk and arc, the ERK/MAPK pathway and synapsins.

There are remarkable behavioral, neural, and genetic similarities between the way songbirds learn to sing and human infants learn to speak. Furthermore, the brain regions involved in birdsong learning, perception, and production have been identified and characterized in detail. In particular, the caudal medial nidopallium (the avian analog of the mammalian auditory-association cortex) has been found to contain the neural substrate of auditory memory, paving the way for analyses of the underlying molecular mechanisms. Recently, the zebra finch genome was sequenced, and annotated cDNA databases representing over 15,000 unique brain-expressed genes are available, enabling high-throughput gene expression analyses. Here we review the involvement of immediate early genes (e.g. zenk and arc), their downstream targets (e.g. synapsins), and their regulatory signaling pathways (e.g. MAPK/ERK) in songbird memory. We propose that in-depth investigations of zenk- and ERK-dependent cascades will help to further unravel the molecular basis of auditory memory.

Language and learning: the cognitive revolution at 60-odd.

Around the middle of the last century, the prevailing psychological paradigm of behaviourism was challenged by what is now known as the cognitive revolution. Behaviourists viewed learning as changes in patterns of behaviour through reinforcement. By contrast, advocates of the cognitive approach argued that such behavioural changes were outward manifestations of computational operations on mental representations. Here we consider the current state of the cognitive revolution, focusing on the two most contentious issues in the debate: language and learning. The cognitive approach has proved to be extremely fruitful in both fields. Although contemporary learning theory has almost completely embraced the cognitive approach, the study of language has witnessed a clear empiricist trend to revert back to a kind of neo-behaviourism. Many contemporary authors contend that language is a means of communication that is learned solely through the observation of external events, and culturally transmitted to successive generations. Here, we argue that learning and language can only be properly understood from a cognitive perspective, where the mind is conceived of as a biologically underpinned computational system. As is the case in learning theory, there is abundant evidence showing that language is subserved by an autonomous cognitive system in the mind. We conclude that the cognitive revolution has fundamentally changed our understanding of the mind.

Vocal learning in songbirds: the role of syllable order in song recognition.

Songbird vocal learning has interesting behavioural and neural parallels with speech acquisition in human infants. Zebra finch males sing one unique song that they imitate from conspecific males, and both sexes learn to recognize their father's song. Although males copy the stereotyped syllable sequence of their father's song, the role of sequential information in recognition remains unclear. Here, we investigated father's song recognition after changing the serial order of syllables (switching the middle syllables, first and last syllables, or playing all syllables in inverse order). Behavioural approach and call responses of adult male and female zebra finches to their father's versus unfamiliar songs in playback tests demonstrated significant recognition of father's song with all syllable-order manipulations. We then measured behavioural responses to normal versus inversed-order father's song. In line with our first results, the subjects did not differentiate between the two. Interestingly, when males' strength of song learning was taken into account, we found a significant correlation between song imitation scores and the approach responses to the father's song. These findings suggest that syllable sequence is not essential for recognition of father's song in zebra finches, but that it does affect responsiveness of males in proportion to the strength of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Memory-specific correlated neuronal activity in higher-order auditory regions of a parrot.

Male budgerigars (Melopsittacus undulatus) are open-ended learners that can learn to produce new vocalisations as adults. We investigated neuronal activation in male budgerigars using the expression of the protein products of the immediate early genes zenk and c-fos in response to exposure to conspecific contact calls (CCs: that of the mate or an unfamiliar female) in three subregions (CMM, dNCM and vNCM) of the caudomedial pallium, a higher order auditory region. Significant positive correlations of Zenk expression were found between these subregions after exposure to mate CCs. In contrast, exposure to CCs of unfamiliar females produced no such correlations. These results suggest the presence of a CC-specific association among the subregions involved in auditory memory. The caudomedial pallium of the male budgerigar may have functional subdivisions that cooperate in the neuronal representation of auditory memory.

Birdsong memory: a neural dissociation between song recognition and production.

Songbirds learn their song from an adult conspecific tutor when they are young, much like the acquisition of speech in human infants. When an adult zebra finch is re-exposed to its tutor's song, there is increased neuronal activation in the caudomedial nidopallium (NCM), the songbird equivalent of the auditory association cortex. This neuronal activation is related to the fidelity of song imitation, suggesting that the NCM may contain the neural representation of song memory. We found that bilateral neurotoxic lesions to the NCM of adult male zebra finches impaired tutor-song recognition but did not affect the males' song production or their ability to discriminate calls. These findings demonstrate that the NCM performs an essential role in the representation of tutor-song memory. In addition, our results show that tutor-song memory and a motor program for the bird's own song have separate neural representations in the songbird brain. Thus, in both humans and songbirds, the cognitive systems of vocal production and auditory recognition memory are subserved by distinct brain regions.

Memory in the making: localized brain activation related to song learning in young songbirds.

Songbird males learn to sing their songs from an adult 'tutor' early in life, much like human infants learn to speak. Similar to humans, in the songbird brain there are separate neural substrates for vocal production and for auditory memory. In adult songbirds, the caudal pallium, the avian equivalent of the auditory association cortex, has been proposed to contain the neural substrate of tutor song memory, while the song system is involved in song production as well as sensorimotor learning. If this hypothesis is correct, there should be neuronal activation in the caudal pallium, and not in the song system, while the young bird is hearing the tutor song. We found increased song-induced molecular neuronal activation, measured as the expression of an immediate early gene, in the caudal pallium of juvenile zebra finch males that were in the process of learning to sing their songs. No such activation was found in the song system. Molecular neuronal activation was significantly greater in response to tutor song than to novel song or silence in the medial part of the caudomedial nidopallium (NCM). In the caudomedial mesopallium, there was significantly greater molecular neuronal activation in response to tutor song than to silence. In addition, in the NCM there was a significant positive correlation between spontaneous molecular neuronal activation and the strength of song learning during sleep. These results suggest that the caudal pallium contains the neural substrate for tutor song memory, which is activated during sleep when the young bird is in the process of learning its song. The findings provide insight into the formation of auditory memories that guide vocal production learning, a process fundamental for human speech acquisition.

Brains for birds and babies: Neural parallels between birdsong and speech acquisition.

Language as a computational cognitive mechanism appears to be unique to the human species. However, there are remarkable behavioral similarities between song learning in songbirds and speech acquisition in human infants that are absent in non-human primates. Here we review important neural parallels between birdsong and speech. In both cases there are separate but continually interacting neural networks that underlie vocal production, sensorimotor learning, and auditory perception and memory. As in the case of human speech, neural activity related to birdsong learning is lateralized, and mirror neurons linking perception and performance may contribute to sensorimotor learning. In songbirds that are learning their songs, there is continual interaction between secondary auditory regions and sensorimotor regions, similar to the interaction between Wernicke's and Broca's areas in human infants acquiring speech and language. Taken together, song learning in birds and speech acquisition in humans may provide useful insights into the evolution and mechanisms of auditory-vocal learning.

The growth of language: Universal Grammar, experience, and principles of computation.

Human infants develop language remarkably rapidly and without overt instruction. We argue that the distinctive ontogenesis of child language arises from the interplay of three factors: domain-specific principles of language (Universal Grammar), external experience, and properties of non-linguistic domains of cognition including general learning mechanisms and principles of efficient computation. We review developmental evidence that children make use of hierarchically composed structures ('Merge') from the earliest stages and at all levels of linguistic organization. At the same time, longitudinal trajectories of development show sensitivity to the quantity of specific patterns in the input, which suggests the use of probabilistic processes as well as inductive learning mechanisms that are suitable for the psychological constraints on language acquisition. By considering the place of language in human biology and evolution, we propose an approach that integrates principles from Universal Grammar and constraints from other domains of cognition. We outline some initial results of this approach as well as challenges for future research.

What do animals learn in artificial grammar studies?

Artificial grammar learning is a popular paradigm to study syntactic ability in nonhuman animals. Subjects are first trained to recognize strings of tokens that are sequenced according to grammatical rules. Next, to test if recognition depends on grammaticality, subjects are presented with grammar-consistent and grammar-violating test strings, which they should discriminate between. However, simpler cues may underlie discrimination if they are available. Here, we review stimulus design in a sample of studies that use particular sounds as tokens, and that claim or suggest their results demonstrate a form of sequence rule learning. To assess the extent of acoustic similarity between training and test strings, we use four simple measures corresponding to cues that are likely salient. All stimulus sets contain biases in similarity measures such that grammatical test stimuli resemble training stimuli acoustically more than do non-grammatical test stimuli. These biases may contribute to response behaviour, reducing the strength of grammatical explanations. We conclude that acoustic confounds are a blind spot in artificial grammar learning studies in nonhuman animals.