Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds

Haruhito Horita, Masahiko Kobayashi, Wan chun Liu, Kotaro Oka, Erich D. Jarvis, Kazuhiro Wada

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Mechanisms for the evolution of convergent behavioral traits are largely unknown. Vocal learning is one such trait that evolved multiple times and is necessary in humans for the acquisition of spoken language. Among birds, vocal learning is evolved in songbirds, parrots, and hummingbirds. Each time similar forebrain song nuclei specialized for vocal learning and production have evolved. This finding led to the hypothesis that the behavioral and neuroanatomical convergences for vocal learning could be associated with molecular convergence. We previously found that the neural activity-induced gene dual specificity phosphatase 1 (dusp1) was up-regulated in non-vocal circuits, specifically in sensory-input neurons of the thalamus and telencephalon; however, dusp1 was not up-regulated in higher order sensory neurons or motor circuits. Here we show that song motor nuclei are an exception to this pattern. The song nuclei of species from all known vocal learning avian lineages showed motor-driven up-regulation of dusp1 expression induced by singing. There was no detectable motor-driven dusp1 expression throughout the rest of the forebrain after non-vocal motor performance. This pattern contrasts with expression of the commonly studied activity-induced gene egr1, which shows motor-driven expression in song nuclei induced by singing, but also motor-driven expression in adjacent brain regions after non-vocal motor behaviors. In the vocal non-learning avian species, we found no detectable vocalizing-driven dusp1 expression in the forebrain. These findings suggest that independent evolutions of neural systems for vocal learning were accompanied by selection for specialized motor-driven expression of the dusp1 gene in those circuits. This specialized expression of dusp1 could potentially lead to differential regulation of dusp1-modulated molecular cascades in vocal learning circuits.

Original languageEnglish
Article numbere42173
JournalPLoS One
Volume7
Issue number8
DOIs
Publication statusPublished - 2012 Aug 2

Fingerprint

Dual Specificity Phosphatase 1
Birds
Music
animal communication
learning
Learning
birds
Prosencephalon
Singing
brain
Sensory Receptor Cells
Networks (circuits)
Genes
Neurons
Parrots
Telencephalon
language development
Songbirds
hummingbirds
thalamus

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds. / Horita, Haruhito; Kobayashi, Masahiko; Liu, Wan chun; Oka, Kotaro; Jarvis, Erich D.; Wada, Kazuhiro.

In: PLoS One, Vol. 7, No. 8, e42173, 02.08.2012.

Research output: Contribution to journalArticle

Horita, Haruhito ; Kobayashi, Masahiko ; Liu, Wan chun ; Oka, Kotaro ; Jarvis, Erich D. ; Wada, Kazuhiro. / Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds. In: PLoS One. 2012 ; Vol. 7, No. 8.
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