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

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.

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Published Version (Please cite this version)

10.1371/journal.pone.0042173

Publication Info

Horita, Haruhito, Masahiko Kobayashi, Wan-Chun Liu, Kotaro Oka, Erich D Jarvis and Kazuhiro Wada (2012). Specialized motor-driven dusp1 expression in the song systems of multiple lineages of vocal learning birds. PLoS One, 7(8). p. e42173. 10.1371/journal.pone.0042173 Retrieved from https://hdl.handle.net/10161/9311.

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Jarvis

Erich David Jarvis

Adjunct Professor in the Deptartment of Neurobiology

Dr. Jarvis' laboratory studies the neurobiology of vocal communication. Emphasis is placed on the molecular pathways involved in the perception and production of learned vocalizations. They use an integrative approach that combines behavioral, anatomical, electrophysiological and molecular biological techniques. The main animal model used is songbirds, one of the few vertebrate groups that evolved the ability to learn vocalizations. The generality of the discoveries is tested in other vocal learning orders, such as parrots and hummingbirds, as well as non-vocal learners, such as pigeons and non-human primates. Some of the questions require performing behavior/molecular biology experiments in freely ranging animals, such as hummingbirds in tropical forest of Brazil. Recent results show that in songbirds, parrots and hummingbirds, perception and production of song are accompanied by anatomically distinct patterns of gene expression. All three groups were found to exhibit vocally-activated gene expression in exactly 7 forebrain nuclei that are very similar to each other. These structures for vocal learning and production are thought to have evolved independently within the past 70 million years, since they are absent from interrelated non-vocal learning orders. One structure, Area X of the basal ganglia's striatum in songbirds, shows large differential gene activation depending on the social context in which the bird sings. These differences may reflect a semantic content of song, perhaps similar to human language.

The overall goal of the research is to advance knowledge of the neural mechanisms for vocal learning and basic mechanisms of brain function. These goals are further achieved by combined collaborative efforts with the laboratories of Drs. Mooney and Nowicki at Duke University, who study respectively behavior and electrophysiological aspects of songbird vocal communication.


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