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Long-distance retinoid signaling in the zebra finch brain.

Roeske TC, Scharff C, Olson CR, Nshdejan A, Mello CV - PLoS ONE (2014)

Bottom Line: Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts.This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling.Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Hunter College, City University of New York, New York, New York, United States of America.

ABSTRACT
All-trans retinoic acid (ATRA), the main active metabolite of vitamin A, is a powerful signaling molecule that regulates large-scale morphogenetic processes during vertebrate embryonic development, but is also involved post-natally in regulating neural plasticity and cognition. In songbirds, it plays an important role in the maturation of learned song. The distribution of the ATRA-synthesizing enzyme, zRalDH, and of ATRA receptors (RARs) have been described, but information on the distribution of other components of the retinoid signaling pathway is still lacking. To address this gap, we have determined the expression patterns of two obligatory RAR co-receptors, the retinoid X receptors (RXR) α and γ, and of the three ATRA-degrading cytochromes CYP26A1, CYP26B1, and CYP26C1. We have also studied the distribution of zRalDH protein using immunohistochemistry, and generated a refined map of ATRA localization, using a modified reporter cell assay to examine entire brain sections. Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts. This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling. Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

No MeSH data available.


Related in: MedlinePlus

Neural substrates for singing and song learning.A and B: schematics of the song control system and relevant auditory structures. Represented are the posterior vocal-motor pathway (VMP, blue), and the anterior forebrain pathway (AFP, red). HVC is the origin of both pathways and the entry site of inputs from auditory areas (yellow) into the song system. For abbreviations, see table 1. In A, brain topography is preserved, for easier comparison with experimental brain sections. In B, indication of broad brain subdivisions (on the right) facilitates comparison with mammalian brains.
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pone-0111722-g001: Neural substrates for singing and song learning.A and B: schematics of the song control system and relevant auditory structures. Represented are the posterior vocal-motor pathway (VMP, blue), and the anterior forebrain pathway (AFP, red). HVC is the origin of both pathways and the entry site of inputs from auditory areas (yellow) into the song system. For abbreviations, see table 1. In A, brain topography is preserved, for easier comparison with experimental brain sections. In B, indication of broad brain subdivisions (on the right) facilitates comparison with mammalian brains.

Mentions: The songbird is a particularly interesting model to examine the role that retinoids play in postnatal behavioral plasticity [20], because song is a complex learned vocal behavior that depends on retinoid signaling for its normal development [21]. Furthermore, the set of discrete brain nuclei that subserve the acquisition and production of song (a.k.a. ‘the song system’) is well characterized anatomically and functionally. This system has two main subdivisions (fig. 1; reviewed by Prather [22]): 1) the posterior vocal-motor pathway (VMP), comprising the nidopallial nucleus HVC (used as proper name; for abbreviations, see table 1), the robust nucleus of the arcopallium (RA), and brainstem vocal and respiratory centers; and 2) the anterior forebrain pathway (AFP), consisting of a pallial—basal-ganglia—thalamo—pallial loop that includes striatal Area X, the medial part of the dorsolateral thalamic nucleus (DLM) and the lateral magnocellular nucleus of the anterior nidopallium (lMAN). The two pathways are connected through HVC-to-Area X and LMAN-to-RA projections. The vocal-motor pathway is essential for singing, whereas the AFP is required for song acquisition in juvenile birds and for modulating song variability and auditory-dependent plasticity in both juvenile and adult birds, as reviewed by Gale and Perkel [23]. HVC is an important node in the song system since it gives rise to both the posterior and anterior pathways, and it is also a major entry site for auditory information [22]. High-order auditory areas like the caudomedial nidopallium (NCM) and the caudal mesopallium (CM) receive input from the primary auditory telencephalic area, field L, and are involved in the perceptual processing and/or memorization of birdsong [22].


Long-distance retinoid signaling in the zebra finch brain.

Roeske TC, Scharff C, Olson CR, Nshdejan A, Mello CV - PLoS ONE (2014)

Neural substrates for singing and song learning.A and B: schematics of the song control system and relevant auditory structures. Represented are the posterior vocal-motor pathway (VMP, blue), and the anterior forebrain pathway (AFP, red). HVC is the origin of both pathways and the entry site of inputs from auditory areas (yellow) into the song system. For abbreviations, see table 1. In A, brain topography is preserved, for easier comparison with experimental brain sections. In B, indication of broad brain subdivisions (on the right) facilitates comparison with mammalian brains.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230966&req=5

pone-0111722-g001: Neural substrates for singing and song learning.A and B: schematics of the song control system and relevant auditory structures. Represented are the posterior vocal-motor pathway (VMP, blue), and the anterior forebrain pathway (AFP, red). HVC is the origin of both pathways and the entry site of inputs from auditory areas (yellow) into the song system. For abbreviations, see table 1. In A, brain topography is preserved, for easier comparison with experimental brain sections. In B, indication of broad brain subdivisions (on the right) facilitates comparison with mammalian brains.
Mentions: The songbird is a particularly interesting model to examine the role that retinoids play in postnatal behavioral plasticity [20], because song is a complex learned vocal behavior that depends on retinoid signaling for its normal development [21]. Furthermore, the set of discrete brain nuclei that subserve the acquisition and production of song (a.k.a. ‘the song system’) is well characterized anatomically and functionally. This system has two main subdivisions (fig. 1; reviewed by Prather [22]): 1) the posterior vocal-motor pathway (VMP), comprising the nidopallial nucleus HVC (used as proper name; for abbreviations, see table 1), the robust nucleus of the arcopallium (RA), and brainstem vocal and respiratory centers; and 2) the anterior forebrain pathway (AFP), consisting of a pallial—basal-ganglia—thalamo—pallial loop that includes striatal Area X, the medial part of the dorsolateral thalamic nucleus (DLM) and the lateral magnocellular nucleus of the anterior nidopallium (lMAN). The two pathways are connected through HVC-to-Area X and LMAN-to-RA projections. The vocal-motor pathway is essential for singing, whereas the AFP is required for song acquisition in juvenile birds and for modulating song variability and auditory-dependent plasticity in both juvenile and adult birds, as reviewed by Gale and Perkel [23]. HVC is an important node in the song system since it gives rise to both the posterior and anterior pathways, and it is also a major entry site for auditory information [22]. High-order auditory areas like the caudomedial nidopallium (NCM) and the caudal mesopallium (CM) receive input from the primary auditory telencephalic area, field L, and are involved in the perceptual processing and/or memorization of birdsong [22].

Bottom Line: Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts.This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling.Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

View Article: PubMed Central - PubMed

Affiliation: Department of Psychology, Hunter College, City University of New York, New York, New York, United States of America.

ABSTRACT
All-trans retinoic acid (ATRA), the main active metabolite of vitamin A, is a powerful signaling molecule that regulates large-scale morphogenetic processes during vertebrate embryonic development, but is also involved post-natally in regulating neural plasticity and cognition. In songbirds, it plays an important role in the maturation of learned song. The distribution of the ATRA-synthesizing enzyme, zRalDH, and of ATRA receptors (RARs) have been described, but information on the distribution of other components of the retinoid signaling pathway is still lacking. To address this gap, we have determined the expression patterns of two obligatory RAR co-receptors, the retinoid X receptors (RXR) α and γ, and of the three ATRA-degrading cytochromes CYP26A1, CYP26B1, and CYP26C1. We have also studied the distribution of zRalDH protein using immunohistochemistry, and generated a refined map of ATRA localization, using a modified reporter cell assay to examine entire brain sections. Our results show that (1) ATRA is more broadly distributed in the brain than previously predicted by the spatially restricted distribution of zRalDH transcripts. This could be due to long-range transport of zRalDH enzyme between different nuclei of the song system: Experimental lesions of putative zRalDH peptide source regions diminish ATRA-induced transcription in target regions. (2) Four telencephalic song nuclei express different and specific subsets of retinoid-related receptors and could be targets of retinoid regulation; in the case of the lateral magnocellular nucleus of the anterior nidopallium (lMAN), receptor expression is dynamically regulated in a circadian and age-dependent manner. (3) High-order auditory areas exhibit a complex distribution of transcripts representing ATRA synthesizing and degrading enzymes and could also be a target of retinoid signaling. Together, our survey across multiple connected song nuclei and auditory brain regions underscores the prominent role of retinoid signaling in modulating the circuitry that underlies the acquisition and production of learned vocalizations.

No MeSH data available.


Related in: MedlinePlus