Differential expression of glutamate receptors in avian neural pathways for learned vocalization.

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Learned vocalization, the substrate for human language, is a rare trait. It is found in three distantly related groups of birds-parrots, hummingbirds, and songbirds. These three groups contain cerebral vocal nuclei for learned vocalization not found in their more closely related vocal nonlearning relatives. Here, we cloned 21 receptor subunits/subtypes of all four glutamate receptor families (AMPA, kainate, NMDA, and metabotropic) and examined their expression in vocal nuclei of songbirds. We also examined expression of a subset of these receptors in vocal nuclei of hummingbirds and parrots, as well as in the brains of dove species as examples of close vocal nonlearning relatives. Among the 21 subunits/subtypes, 19 showed higher and/or lower prominent differential expression in songbird vocal nuclei relative to the surrounding brain subdivisions in which the vocal nuclei are located. This included relatively lower levels of all four AMPA subunits in lMAN, strikingly higher levels of the kainite subunit GluR5 in the robust nucleus of the arcopallium (RA), higher and lower levels respectively of the NMDA subunits NR2A and NR2B in most vocal nuclei and lower levels of the metabotropic group I subtypes (mGluR1 and -5) in most vocal nuclei and the group II subtype (mGluR2), showing a unique expression pattern of very low levels in RA and very high levels in HVC. The splice variants of AMPA subunits showed further differential expression in vocal nuclei. Some of the receptor subunits/subtypes also showed differential expression in hummingbird and parrot vocal nuclei. The magnitude of differential expression in vocal nuclei of all three vocal learners was unique compared with the smaller magnitude of differences found for nonvocal areas of vocal learners and vocal nonlearners. Our results suggest that evolution of vocal learning was accompanied by differential expression of a conserved gene family for synaptic transmission and plasticity in vocal nuclei. They also suggest that neural activity and signal transduction in vocal nuclei of vocal learners will be different relative to the surrounding brain areas.





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Wada, Kazuhiro, Hironobu Sakaguchi, Erich D Jarvis and Masatoshi Hagiwara (2004). Differential expression of glutamate receptors in avian neural pathways for learned vocalization. J Comp Neurol, 476(1). pp. 44–64. 10.1002/cne.20201 Retrieved from https://hdl.handle.net/10161/11229.

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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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