Convergent differential regulation of parvalbumin in the brains of vocal learners.

Spoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associa...

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Main Authors: Erina Hara, Miriam V Rivas, James M Ward, Kazuo Okanoya, Erich D Jarvis
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3253077?pdf=render
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author Erina Hara
Miriam V Rivas
James M Ward
Kazuo Okanoya
Erich D Jarvis
author_facet Erina Hara
Miriam V Rivas
James M Ward
Kazuo Okanoya
Erich D Jarvis
author_sort Erina Hara
collection DOAJ
description Spoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65-300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.
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spelling doaj.art-311d42692c6946e48b121aeba0770a422022-12-22T01:19:44ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0171e2945710.1371/journal.pone.0029457Convergent differential regulation of parvalbumin in the brains of vocal learners.Erina HaraMiriam V RivasJames M WardKazuo OkanoyaErich D JarvisSpoken language and learned song are complex communication behaviors found in only a few species, including humans and three groups of distantly related birds--songbirds, parrots, and hummingbirds. Despite their large phylogenetic distances, these vocal learners show convergent behaviors and associated brain pathways for vocal communication. However, it is not clear whether this behavioral and anatomical convergence is associated with molecular convergence. Here we used oligo microarrays to screen for genes differentially regulated in brain nuclei necessary for producing learned vocalizations relative to adjacent brain areas that control other behaviors in avian vocal learners versus vocal non-learners. A top candidate gene in our screen was a calcium-binding protein, parvalbumin (PV). In situ hybridization verification revealed that PV was expressed significantly higher throughout the song motor pathway, including brainstem vocal motor neurons relative to the surrounding brain regions of all distantly related avian vocal learners. This differential expression was specific to PV and vocal learners, as it was not found in avian vocal non-learners nor for control genes in learners and non-learners. Similar to the vocal learning birds, higher PV up-regulation was found in the brainstem tongue motor neurons used for speech production in humans relative to a non-human primate, macaques. These results suggest repeated convergent evolution of differential PV up-regulation in the brains of vocal learners separated by more than 65-300 million years from a common ancestor and that the specialized behaviors of learned song and speech may require extra calcium buffering and signaling.http://europepmc.org/articles/PMC3253077?pdf=render
spellingShingle Erina Hara
Miriam V Rivas
James M Ward
Kazuo Okanoya
Erich D Jarvis
Convergent differential regulation of parvalbumin in the brains of vocal learners.
PLoS ONE
title Convergent differential regulation of parvalbumin in the brains of vocal learners.
title_full Convergent differential regulation of parvalbumin in the brains of vocal learners.
title_fullStr Convergent differential regulation of parvalbumin in the brains of vocal learners.
title_full_unstemmed Convergent differential regulation of parvalbumin in the brains of vocal learners.
title_short Convergent differential regulation of parvalbumin in the brains of vocal learners.
title_sort convergent differential regulation of parvalbumin in the brains of vocal learners
url http://europepmc.org/articles/PMC3253077?pdf=render
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