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Birdsong "transcriptomics": neurochemical specializations of the oscine song system.

Lovell PV, Clayton DF, Replogle KL, Mello CV - PLoS ONE (2008)

Bottom Line: Using high-throughput functional genomics we have identified approximately 200 novel molecular markers of adult zebra finch HVC, a key node of the song system.These markers clearly differentiate HVC from the general pallial region to which HVC belongs, and thus represent molecular specializations of this song nucleus.Our study represents one of the most comprehensive molecular genetic characterizations of a brain nucleus involved in a complex learned behavior in a vertebrate.

View Article: PubMed Central - PubMed

Affiliation: Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon, United States of America.

ABSTRACT

Background: Vocal learning is a rare and complex behavioral trait that serves as a basis for the acquisition of human spoken language. In songbirds, vocal learning and production depend on a set of specialized brain nuclei known as the song system.

Methodology/principal findings: Using high-throughput functional genomics we have identified approximately 200 novel molecular markers of adult zebra finch HVC, a key node of the song system. These markers clearly differentiate HVC from the general pallial region to which HVC belongs, and thus represent molecular specializations of this song nucleus. Bioinformatics analysis reveals that several major neuronal cell functions and specific biochemical pathways are the targets of transcriptional regulation in HVC, including: 1) cell-cell and cell-substrate interactions (e.g., cadherin/catenin-mediated adherens junctions, collagen-mediated focal adhesions, and semaphorin-neuropilin/plexin axon guidance pathways); 2) cell excitability (e.g., potassium channel subfamilies, cholinergic and serotonergic receptors, neuropeptides and neuropeptide receptors); 3) signal transduction (e.g., calcium regulatory proteins, regulators of G-protein-related signaling); 4) cell proliferation/death, migration and differentiation (e.g., TGF-beta/BMP and p53 pathways); and 5) regulation of gene expression (candidate retinoid and steroid targets, modulators of chromatin/nucleolar organization). The overall direction of regulation suggest that processes related to cell stability are enhanced, whereas proliferation, growth and plasticity are largely suppressed in adult HVC, consistent with the observation that song in this songbird species is mostly stable in adulthood.

Conclusions/significance: Our study represents one of the most comprehensive molecular genetic characterizations of a brain nucleus involved in a complex learned behavior in a vertebrate. The data indicate numerous targets for pharmacological and genetic manipulations of the song system, and provide novel insights into mechanisms that might play a role in the regulation of song behavior and/or vocal learning.

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(A) Schematic of a male zebra finch brain showing the approximate locations of HVC and underlying auditory shelf, as well as other major nuclei of the song system and major pallial and subpallial brain divisions. HVC provides major input into: a direct motor pathway (black nuclei), and an anterior forebrain pathway (white nuclei). Laser capture microdissection (LCM) was used to conservatively sample HVC and the underlying auditory shelf (LCM sites denoted by dotted ovals). (B and C) Under brightfield (B, white arrows) HVC could be identified by a characteristic bump on the surface of the brain and the presence of large cells and cell clusters; under dark-field (C) mylenated fibers are seen close to the ventral boundary of HVC. LCM dissections were confirmed by examination of the section after LCM (D), as well as of tissue adhered to the capture cap (E). Abbreviations: A, anterior; P, Posterior; D, Dorsal; V, Ventral; DLM, medial dorsolateral thalamic nucleus; LMAN, lateral magnocellular nucleus of the anterior nidopallium; nXIIts, tracheo-syringeal portion of the hypoglossal nerve nucleus; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; X, striatal area X; Arco., arcopallium; Nido., nidopallum; Meso., mesopallium; Hyper., hyperpallium.
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pone-0003440-g001: (A) Schematic of a male zebra finch brain showing the approximate locations of HVC and underlying auditory shelf, as well as other major nuclei of the song system and major pallial and subpallial brain divisions. HVC provides major input into: a direct motor pathway (black nuclei), and an anterior forebrain pathway (white nuclei). Laser capture microdissection (LCM) was used to conservatively sample HVC and the underlying auditory shelf (LCM sites denoted by dotted ovals). (B and C) Under brightfield (B, white arrows) HVC could be identified by a characteristic bump on the surface of the brain and the presence of large cells and cell clusters; under dark-field (C) mylenated fibers are seen close to the ventral boundary of HVC. LCM dissections were confirmed by examination of the section after LCM (D), as well as of tissue adhered to the capture cap (E). Abbreviations: A, anterior; P, Posterior; D, Dorsal; V, Ventral; DLM, medial dorsolateral thalamic nucleus; LMAN, lateral magnocellular nucleus of the anterior nidopallium; nXIIts, tracheo-syringeal portion of the hypoglossal nerve nucleus; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; X, striatal area X; Arco., arcopallium; Nido., nidopallum; Meso., mesopallium; Hyper., hyperpallium.

Mentions: In songbirds, the caudo-dorsal portion of the nidopallium (a part of the avian pallium that is thought to share a common origin with mammalian cortical regions) encompasses both HVC, a specialized nucleus of the song system that is unique to songbirds, and the Shelf, a component of the central auditory system that is present in all birds (Fig. 1A) [15]. Our basic hypothesis is that HVC constitutes a differentiated nucleus within the caudo-dorsal nidopallium that is specialized for vocal-motor control and vocal learning, while the Shelf is part of a more primordial avian brain circuitry involved in auditory processing.


Birdsong "transcriptomics": neurochemical specializations of the oscine song system.

Lovell PV, Clayton DF, Replogle KL, Mello CV - PLoS ONE (2008)

(A) Schematic of a male zebra finch brain showing the approximate locations of HVC and underlying auditory shelf, as well as other major nuclei of the song system and major pallial and subpallial brain divisions. HVC provides major input into: a direct motor pathway (black nuclei), and an anterior forebrain pathway (white nuclei). Laser capture microdissection (LCM) was used to conservatively sample HVC and the underlying auditory shelf (LCM sites denoted by dotted ovals). (B and C) Under brightfield (B, white arrows) HVC could be identified by a characteristic bump on the surface of the brain and the presence of large cells and cell clusters; under dark-field (C) mylenated fibers are seen close to the ventral boundary of HVC. LCM dissections were confirmed by examination of the section after LCM (D), as well as of tissue adhered to the capture cap (E). Abbreviations: A, anterior; P, Posterior; D, Dorsal; V, Ventral; DLM, medial dorsolateral thalamic nucleus; LMAN, lateral magnocellular nucleus of the anterior nidopallium; nXIIts, tracheo-syringeal portion of the hypoglossal nerve nucleus; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; X, striatal area X; Arco., arcopallium; Nido., nidopallum; Meso., mesopallium; Hyper., hyperpallium.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2563692&req=5

pone-0003440-g001: (A) Schematic of a male zebra finch brain showing the approximate locations of HVC and underlying auditory shelf, as well as other major nuclei of the song system and major pallial and subpallial brain divisions. HVC provides major input into: a direct motor pathway (black nuclei), and an anterior forebrain pathway (white nuclei). Laser capture microdissection (LCM) was used to conservatively sample HVC and the underlying auditory shelf (LCM sites denoted by dotted ovals). (B and C) Under brightfield (B, white arrows) HVC could be identified by a characteristic bump on the surface of the brain and the presence of large cells and cell clusters; under dark-field (C) mylenated fibers are seen close to the ventral boundary of HVC. LCM dissections were confirmed by examination of the section after LCM (D), as well as of tissue adhered to the capture cap (E). Abbreviations: A, anterior; P, Posterior; D, Dorsal; V, Ventral; DLM, medial dorsolateral thalamic nucleus; LMAN, lateral magnocellular nucleus of the anterior nidopallium; nXIIts, tracheo-syringeal portion of the hypoglossal nerve nucleus; RA, robust nucleus of the arcopallium; RAm, nucleus retroambigualis; X, striatal area X; Arco., arcopallium; Nido., nidopallum; Meso., mesopallium; Hyper., hyperpallium.
Mentions: In songbirds, the caudo-dorsal portion of the nidopallium (a part of the avian pallium that is thought to share a common origin with mammalian cortical regions) encompasses both HVC, a specialized nucleus of the song system that is unique to songbirds, and the Shelf, a component of the central auditory system that is present in all birds (Fig. 1A) [15]. Our basic hypothesis is that HVC constitutes a differentiated nucleus within the caudo-dorsal nidopallium that is specialized for vocal-motor control and vocal learning, while the Shelf is part of a more primordial avian brain circuitry involved in auditory processing.

Bottom Line: Using high-throughput functional genomics we have identified approximately 200 novel molecular markers of adult zebra finch HVC, a key node of the song system.These markers clearly differentiate HVC from the general pallial region to which HVC belongs, and thus represent molecular specializations of this song nucleus.Our study represents one of the most comprehensive molecular genetic characterizations of a brain nucleus involved in a complex learned behavior in a vertebrate.

View Article: PubMed Central - PubMed

Affiliation: Neurological Sciences Institute, Oregon Health and Science University, Beaverton, Oregon, United States of America.

ABSTRACT

Background: Vocal learning is a rare and complex behavioral trait that serves as a basis for the acquisition of human spoken language. In songbirds, vocal learning and production depend on a set of specialized brain nuclei known as the song system.

Methodology/principal findings: Using high-throughput functional genomics we have identified approximately 200 novel molecular markers of adult zebra finch HVC, a key node of the song system. These markers clearly differentiate HVC from the general pallial region to which HVC belongs, and thus represent molecular specializations of this song nucleus. Bioinformatics analysis reveals that several major neuronal cell functions and specific biochemical pathways are the targets of transcriptional regulation in HVC, including: 1) cell-cell and cell-substrate interactions (e.g., cadherin/catenin-mediated adherens junctions, collagen-mediated focal adhesions, and semaphorin-neuropilin/plexin axon guidance pathways); 2) cell excitability (e.g., potassium channel subfamilies, cholinergic and serotonergic receptors, neuropeptides and neuropeptide receptors); 3) signal transduction (e.g., calcium regulatory proteins, regulators of G-protein-related signaling); 4) cell proliferation/death, migration and differentiation (e.g., TGF-beta/BMP and p53 pathways); and 5) regulation of gene expression (candidate retinoid and steroid targets, modulators of chromatin/nucleolar organization). The overall direction of regulation suggest that processes related to cell stability are enhanced, whereas proliferation, growth and plasticity are largely suppressed in adult HVC, consistent with the observation that song in this songbird species is mostly stable in adulthood.

Conclusions/significance: Our study represents one of the most comprehensive molecular genetic characterizations of a brain nucleus involved in a complex learned behavior in a vertebrate. The data indicate numerous targets for pharmacological and genetic manipulations of the song system, and provide novel insights into mechanisms that might play a role in the regulation of song behavior and/or vocal learning.

Show MeSH
Related in: MedlinePlus