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  • Review Article
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Neural mechanisms of birdsong memory

Nature Reviews Neuroscience volume 7, pages 347–357 (2006)Cite this article

Key Points

  • Song learning in songbirds has strong similarities with speech acquisition in human infants. Songbirds need to learn their songs from an adult conspecific. This occurs in two phases: a memorization phase, early in life, during which the young bird forms a neural representation (a 'template') of the song of a tutor; and a sensorimotor phase, during which the bird's own vocal output is matched to the stored template.

  • A network of interconnected brain nuclei, known as the 'song system', is involved in the perception, learning and production of song. Within the song system, the caudal pathway is important for song production. The rostral pathway is involved in song perception and in vocal sensorimotor learning. Initial claims that there are correlations between functional (for example, seasonal or sex) song differences and differences in song system morphology have not been supported by recent findings.

  • Two regions outside the song system show neuronal activation (measured as increased expression of immediate early genes) when zebra finches are exposed to song. In one of these regions, the caudomedial nidopallium (NCM), neuronal activation on exposure to the tutor song is significantly correlated with the strength of song learning. An electrophysiological study showed that a familiarity index, based on neuronal habituation rates in the NCM, was significantly greater in tutored males than in untutored males, and significantly positively correlated with the strength of song learning.

  • Zebra finch females do not sing, but nevertheless can learn the characteristics of their father's song and form a preference for it over novel songs. When female zebra finches that were reared with their fathers were re-exposed to their fathers' song, they showed significantly greater neuronal activation in the caudomedial mesopallium (CMM), but not in the NCM or hippocampus, compared with when they were exposed to novel song.

  • Neuronal activation in the NCM and CMM is not an artefact of isolation rearing, and is not related to attentional mechanisms.

  • The NCM and the CMM might be parallel stores that contain the neural substrate for tutor (or father's) song memory, or the 'template'. The NCM might be more directly functionally linked to the premotor nuclei in the song system. The CMM overlaps with the intermediate and medial mesopallium (IMM) that contains the neural substrate for imprinting memory in domestic chicks. The NCM and CMM may be homologous with subdivisions of the mammalian auditory association cortex, which in humans are associated with auditory learning in relation to speech acquisition.

  • Further multidisciplinary research is needed to determine whether the NCM and CMM contain the neural substrates of song memory, or whether this information is stored elsewhere in the brain. The neuroanatomical connectivity and functional relationship between these two brain regions and the song system needs to be investigated, in order for us to better understand the overall process of bird song learning. Such analyses may, ultimately, have heuristic value for the study of speech aquisition in humans.

Abstract

The process through which young male songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorization followed by a period during which the individual develops its own vocalizations. The avian 'song system', a network of brain nuclei, is the probable neural substrate for the second phase of sensorimotor learning. By contrast, the neural representation of song memory acquired in the first phase is localized outside the song system, in different regions of the avian equivalent of the human auditory association cortex.

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Figure 1: Birdsong develops through different stages.
Figure 2: The brains of songbirds and non-songbirds differ.
Figure 3: The songbird brain.
Figure 4: Brain activation in response to song.
Figure 5: Seasonal changes in physiology and vocal repertoire of wild canaries on Madeira.

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Acknowledgements

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

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Authors and Affiliations

  1. Department of Biology and Helmholtz Institute, Behavioural Biology, Padualaan 8, Utrecht University, The Netherlands

    Johan J. Bolhuis

  2. Max Planck Institute for Ornithology, Seewiesen, Germany

    Manfred Gahr

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Glossary

Song system

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

Neuroecology

The study of the neural mechanisms of behaviour and cognition, using functional or evolutionary considerations. In a neuroecological analysis of memory, functional differences are related to neuromorphological differences.

Subsong

The first songs produced by young songbirds. These songs are relatively simple and may not resemble the song of the tutor. Subsong may still change and will eventually become crystallized song, which in many songbird species is the definitive song for that particular individual.

Immediate early genes

(IEGs). Genes that can respond rapidly (within minutes) to stimulation of a cell such as a neuron. The protein products of such genes return to the cell nucleus where they affect the transcription of other, 'late response' genes. Expression of these genes (such as c-fos or ZENK) or their protein products (Fos and Zenk, respectively) signifies that the cell is activated. Therefore, IEG expression is used as a marker for neuronal activation. The genes can be stained by means of an in situ hybridization procedure, whereas the protein products can be made visible through immunocytochemistry.

Template

A metaphor for the central representation of song. Conventionally, it has been suggested that songbirds are born with a crude template that has species-specific characteristics. Auditory experience with the song of an adult conspecific male will then mould the template into a more precise representation of the tutor song.

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Bolhuis, J., Gahr, M. Neural mechanisms of birdsong memory. Nat Rev Neurosci 7, 347–357 (2006). https://doi.org/10.1038/nrn1904

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