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Twitter evolution: converging mechanisms in birdsong and human speech

Key Points

  • Unlike non-human primates, songbirds learn to vocalize very much like human infants learn to speak. In both cases, young individuals form auditory memories of the vocalizations of adults during a sensitive period, and they acquire their own vocalizations through a transitional phase that is called 'subsong' in birds and 'babbling' in infants.

  • In songbirds, a network of interconnected brain nuclei, known as the song system, is involved in the perception, learning and production of song. Parts of the song system are analogous — and possibly homologous — to human basal ganglia as well as regions in the frontal cortex that are involved in speech.

  • In songbirds, regions outside the song system, in the caudal pallium, are involved in auditory memory; activation of one of these regions, the caudiomedial nidopallium (NCM), is related to the strength of tutor song memory. These pallial regions are analogous — and possibly homologous — to a region in the human temporal lobe known as the auditory association cortex that is involved in speech processing.

  • In both humans and songbirds, the vocal 'motor regions' are also involved in auditory perception. For learning and maintenance of speech and birdsong, continual interaction between auditory and motor regions to match what is heard and what is produced is necessary.

  • Some species of songbirds including Bengalese finches (Lonchura striata domestica) have types of note-to-note transition rules that could be expressed as 'finite-state syntax', which is a simpler form of human syntax.

  • FOXP2 is the first gene specifically implicated in speech and language, and its sequences are more than 90% conserved between birds and mammals. FOXP2 is regulated developmentally and seasonally and by singing activity in songbirds, and experimentally downregulated FOXP2 levels impair song learning.

  • Further multidisciplinary research is needed to study the molecular, neural and cognitive mechanisms of birdsong, and its similarities with human speech. Such analyses may ultimately have heuristic value for the study of speech acquisition and production in humans and its underlying mechanisms.

Abstract

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.

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Figure 1: The songbird brain and the human brain.
Figure 2: Neural dissociation between birdsong recognition and production.

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Acknowledgements

We are grateful to R. C. Berwick and to three anonymous referees for their constructive comments on an earlier version of the manuscript.

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Correspondence to Johan J. Bolhuis, Kazuo Okanoya or Constance Scharff.

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Supplementary information

Supplementary information S1 (box)

Birdsong learning: variations on a theme (PDF 216 kb)

Supplementary information S2 (box)

A specialised neural circuit involved in avian 'babbling' (PDF 206 kb)

Supplementary information S3 (box)

Syntax and semantics in bird vocalisations (PDF 218 kb)

Supplementary information S4 (box)

Neural mechanisms of human syntax (PDF 213 kb)

Supplementary information S5 (box)

Syntactic organisation and recursion in birds and humans (PDF 218 kb)

Supplementary information S6 (box)

Mirror neurons in song and speech (PDF 218 kb)

Supplementary information S7 (box)

The role of sleep in song and speech (PDF 218 kb)

Related links

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FURTHER INFORMATION

Johan J. Bolhuis' homepage

Kazuo Okanoya's homepage

Constance Scharff's homepage

NCBI Zebra Finch Genome Resources website

Glossary

FOXP2

A transcription factor of the large forkhead box (Fox) family, originally discovered in Drosophila. FOX genes have important roles in the development of many tissues and diseases.

Seasonal breeder

An animal (for example, a songbird species) that breeds only during a specific period of the year.

Opportunistic breeder

An animal (for example, a songbird species) that can breed year-round.

Action-based learning

Also known as selective learning. A song learning style that selects the final sound repertoire after an initial overproduction of song elements, based on auditory or visual feedback from conspecifics.

Instruction-based learning

Also known as sensorimotor learning. A song learning style principally exemplified by the zebra finch, in which vocal 'babbling' is gradually modified through auditory guided sensorimotor learning. Both 'instruction-based' and 'action-based' learning can occur in the same species to various degrees.

Syntax

In a narrow sense, syntax refers to a set of rules that governs the arrangements of words to produce a sentence. In a broader sense, syntax refers to a set of rules to hierarchically and sequentially arrange elements to produce a string.

Song system

A network of forebrain nuclei that is involved in the perception, acquisition and production of song.

Working memory

A form of memory in which information is stored for a limited period during which it can be used; in humans the classic example is remembering a telephone number that is then dialled and immediately forgotten.

Homologous

Homologous traits (or brain regions) are thought to have evolved from a common ancestor.

Analogous

Analogous traits (or brain regions) have a similar function, but are thought to have evolved independently in distantly related species.

Template

A term used to denote the central representation of birdsong. It is thought that songbirds are born with a crude template that has species-specific characteristics. Auditory experience, first with the song of an adult conspecific male and later with the individual's own vocal output, then moulds the template into a more precise representation of the tutor song.

Semantics

In a narrow sense, semantics refers to the study of meaning in language. In a broader sense, semantics refers to information content of a signal.

Amniotes

The collective name for mammals, reptiles and birds that are characterized by four limbs, a spinal column and embryos that develop within a fluid-filled cavity that is enclosed by membranes ('amnion').

Transgenesis

The introduction of an exogenous gene — a transgene — into an organism which results in expression of the new gene and its transmission into the next generation.

Non-vocal learner

A bird species that does not learn its vocalizations.

Recursion

A term used by linguists to refer to the embedding of a structure into the same type of structure — for example, embedding a sentence into another sentence.

Phonological

In a narrow sense, referring to the set of physical and psychological features of a unit of speech. In a broader sense, referring to the acoustic characteristics of a unit of sound.

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Bolhuis, J., Okanoya, K. & Scharff, C. Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11, 747–759 (2010). https://doi.org/10.1038/nrn2931

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