Ultrastructural and electrophysiological analysis of Area X in the untutored and deafened Bengalese finch in relation to normally reared birds

Peng, Zhe; Zhang, Xuebo; Liu, Yu; Chen, Xi; Zeng, Shaoju; Zhang, Xinwen; Zuo, Mingzhang; xu, JinCao; Yu-bin, JI; Han, Zhongming

doi:10.1016/j.brainres.2013.06.031

Cited by 4 publications

(6 citation statements)

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“…Genes related to synaptic transmission were differentially expressed across multiple pallial regions, including song regions RA, HVC, and LMAN as well as the non-song region NCL. Neuron spine-associated genes were upregulated across RA, Arco., and HVC, consistent with previous reports of altered spine dynamics in the song motor pathway following deafening ( Peng et al, 2012a ; Peng et al, 2013 ; Tschida and Mooney, 2012 ; Zhou et al, 2017 ).…”

Section: Resultssupporting

confidence: 92%

“…Past work has shown that experimentally removing this feedback by deafening results in the gradual deterioration of both song spectral structure and temporal ordering of the individual elements (syllables) that comprise song ( Nordeen and Nordeen, 1992 ; Okanoya and Yamaguchi, 1997 ; Woolley and Rubel, 1997 ). Deafening also drives a range of physiological, cellular, and molecular changes in the song system, including alterations to neuronal turnover ( Scott et al, 2000 ; Wang et al, 1999 ) (but see Pytte et al, 2012 ), dendritic spine morphology ( Peng et al, 2012a ; Peng et al, 2013 ; Tschida and Mooney, 2012 ; Zhou et al, 2017 ), neuronal excitability ( Tschida and Mooney, 2012 ), and gene expression ( Watanabe et al, 2002 ).…”

Section: Resultsmentioning

confidence: 99%

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Neural circuit-wide analysis of changes to gene expression during deafening-induced birdsong destabilization

Colquitt

Green

et al. 2023

eLife

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Sensory feedback is required for the stable execution of learned motor skills, and its loss can severely disrupt motor performance. The neural mechanisms that mediate sensorimotor stability have been extensively studied at systems and physiological levels, yet relatively little is known about how disruptions to sensory input alter the molecular properties of associated motor systems. Songbird courtship song, a model for skilled behavior, is a learned and highly structured vocalization that is destabilized following deafening. Here, we sought to determine how the loss of auditory feedback modifies gene expression and its coordination across the birdsong sensorimotor circuit. To facilitate this system-wide analysis of transcriptional responses, we developed a gene expression profiling approach that enables the construction of hundreds of spatially-defined RNA-sequencing libraries. Using this method, we found that deafening preferentially alters gene expression across birdsong neural circuitry relative to surrounding areas, particularly in premotor and striatal regions. Genes with altered expression are associated with synaptic transmission, neuronal spines, and neuromodulation and show a bias toward expression in glutamatergic neurons and Pvalb/Sst-class GABAergic interneurons. We also found that connected song regions exhibit correlations in gene expression that were reduced in deafened birds relative to hearing birds, suggesting that song destabilization alters the inter-region coordination of transcriptional states. Finally, lesioning LMAN, a forebrain afferent of RA required for deafening-induced song plasticity, had the largest effect on groups of genes that were also most affected by deafening. Combined, this integrated transcriptomics analysis demonstrates that the loss of peripheral sensory input drives a distributed gene expression response throughout associated sensorimotor neural circuitry and identifies specific candidate molecular and cellular mechanisms that support the stability and plasticity of learned motor skills.

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Section: Resultssupporting

confidence: 92%

Section: Resultsmentioning

confidence: 99%

Neural circuit-wide analysis of changes to gene expression during deafening-induced birdsong destabilization

Colquitt

Green

et al. 2023

eLife

View full text Add to dashboard Cite

show abstract

“…Genes related to synaptic transmission were differentially expressed across multiple pallial regions, including song regions RA, HVC, and LMAN as well as the non-song region NCL. Neuron spine-associated genes were upregulated across RA, Arco., and HVC, consistent with previous reports of altered spine dynamics in the song motor pathway following deafening (Peng et al, 2013(Peng et al, , 2012aTschida and Mooney, 2012;Zhou et al, 2017).…”

Section: Song System-wide Transcriptional Signatures Of Song Destabil...supporting

confidence: 92%

“…For the songbird, prior studies have identified a variety of circuit, cellular, and molecular mechanisms that may contribute to deafening-induced song-destabilization (Brainard and Doupe, 2000;Kojima et al, 2013;Mandelblat-Cerf et al, 2014;Peng et al, 2013Peng et al, , 2012aPeng et al, , 2012bScott et al, 2000;Tschida and Mooney, 2012;Wang et al, 1999;Watanabe et al, 2002;Zhou et al, 2017). These prior demonstrations, which have focused on a disparate set of song control structures and specific candidate mechanisms, motivated our interest in applying a circuit-wide and unbiased approach in this system to identify molecular responses to auditory deprivationinduced motor destabilization.…”

Section: Discussionmentioning

confidence: 99%

“…Past work has shown that experimentally removing this feedback by deafening results in the gradual deterioration of both song spectral structure and temporal ordering of the individual elements (syllables) that comprise song (Nordeen and Nordeen, 1992;Okanoya and Yamaguchi, 1997;Woolley and Rubel, 1997). Deafening also drives a range of physiological, cellular, and molecular changes in the song system, including alterations to neuronal turnover (Scott et al, 2000;Wang et al, 1999) (but see (Pytte et al, 2012)), dendritic spine morphology (Peng et al, 2013(Peng et al, , 2012aTschida and Mooney, 2012;Zhou et al, 2017), neuronal excitability (Tschida and Mooney, 2012), and gene expression (Watanabe et al, 2002).…”

Section: Deafening Destabilizes Birdsong and Increases Song Variabilitymentioning

confidence: 99%

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Neural circuit-wide analysis of gene expression during deafening-induced destabilization of birdsong

Colquitt

Green

et al. 2022

Preprint

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Sensory feedback is required for stable execution of learned motor skills, and its loss can severely disrupt motor performance. The neural mechanisms that mediate sensorimotor stability have been extensively studied at systems and physiological levels, yet relatively little is known about how disruptions to sensory input alter the molecular properties of associated motor systems. Songbird courtship song, a model for skilled behavior, is a learned and highly structured vocalization that is destabilized following deafening. Here, we sought to determine how the loss of auditory feedback modifies gene expression and its coordination across the birdsong sensorimotor circuit. To facilitate this system-wide analysis of transcriptional responses, we developed a gene expression profiling approach that enables the construction of hundreds of spatially-defined RNA-sequencing libraries. Using this method, we found that deafening preferentially alters gene expression across birdsong neural circuitry relative to surrounding areas, particularly in premotor and striatal regions. Genes with altered expression are associated with synaptic transmission, neuronal spines, and neuromodulation and show a bias toward expression in glutamatergic neurons and Pvalb/Sst-class GABAergic interneurons. We also found that connected song regions exhibit correlations in gene expression that were reduced in deafened birds relative to hearing birds, suggesting that song destabilization alters the inter-region coordination of transcriptional state. Finally, lesioning LMAN, a forebrain afferent of RA required for deafening-induced song plasticity, had the largest effect on groups of genes that were also most affected by deafening. Combined, this integrated transcriptomics analysis demonstrates that the loss of peripheral sensory input drives a distributed gene expression response throughout associated sensorimotor neural circuitry and identifies specific candidate molecular and cellular mechanisms that support stability and plasticity of learned motor skills.

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Notch1 is involved in cell proliferation and neuronal differentiation in the HVC of zebra finch (Taeniopygia guttata)

Chen

Jie

et al. 2023

Behavioural Brain Research

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Ultrastructural and electrophysiological analysis of Area X in the untutored and deafened Bengalese finch in relation to normally reared birds

Cited by 4 publications

References 45 publications

Neural circuit-wide analysis of changes to gene expression during deafening-induced birdsong destabilization

Neural circuit-wide analysis of changes to gene expression during deafening-induced birdsong destabilization

Neural circuit-wide analysis of gene expression during deafening-induced destabilization of birdsong

Notch1 is involved in cell proliferation and neuronal differentiation in the HVC of zebra finch (Taeniopygia guttata)

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