Remodeling of Dendritic Spines in the Avian Vocal Motor Cortex Following Deafening Depends on the Basal Ganglia Circuit

Zhou, Xinna; Fu, Xin; Lin, Chun Nan; Zhou, Xiaojuan; Liu, Jin; Wang, Li; Zhang, Xinwen; Zuo, Mingzhang; Fan, Xiaoyue; Li, Dapeng; Sun, Yingyu

doi:10.1093/cercor/bhw130

Cited by 4 publications

(21 citation statements)

References 76 publications

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“…Using confocal microscopy and 3D electron microscopy, we demonstrated the sensitivity of dendritic spine length and spine synapse number to auditory deprivation. Together with previous data on the effect of Area X lesions on deafening-induced vocal changes (Kojima et al 2013;Zhou et al 2017), we suggest that these striatal changes might contribute to adult vocal plasticity.…”

Section: Discussionsupporting

confidence: 85%

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Deafening‐induced rapid changes to spine synaptic connectivity in the adult avian vocal basal ganglia

et al. 2021

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The basal ganglia have been implicated in auditory-dependent vocal learning and plasticity in human and songbirds, but the underlying neural phenotype remains to be clarified. Here, using confocal imaging and three-dimensional electron microscopy, we investigated striatal structural plasticity in response to hearing loss in Area X, the avian vocal basal ganglia, in adult male zebra finch (Taeniopygia guttata). We observed a rapid elongation of dendritic spines, by approximately 13%, by day 3 after deafening, and a considerable increase in spine synapse density, by approximately 61%, by day 14 after deafening, compared with the controls with an intact cochlea. These findings reveal structural sensitivity of Area X to auditory deprivation and suggest that this striatal plasticity might contribute to deafening-induced changes to learned vocal behavior.

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Section: Discussionsupporting

confidence: 85%

“…Dendritic spines were analyzed blindly as described by Zhou et al . (2017), using NeuronStudio software (Rodriguez et al . 2008).…”

Section: Methodsmentioning

confidence: 99%

Deafening‐induced rapid changes to spine synaptic connectivity in the adult avian vocal basal ganglia

et al. 2021

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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, 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

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et al. 2022

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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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Postnatal Ablation of Synaptic Retinoic Acid Signaling Impairs Cortical Information Processing and Sensory Discrimination in Mice

et al. 2018

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Retinoic acid (RA) and its receptors (RARs) are well established essential transcriptional regulators during embryonic development. Recent findings in cultured neurons identified an independent and critical post-transcriptional role of RA and RARα in the homeostatic regulation of excitatory and inhibitory synaptic transmission in mature neurons. However, the functional relevance of synaptic RA signaling has not been established. Here, using somatosensory cortex as a model system and the RARα conditional knock-out mouse as a tool, we applied multiple genetic manipulations to delete RARα postnatally in specific populations of cortical neurons, and asked whether synaptic RA signaling observed in cultured neurons is involved in cortical information processing Indeed, conditional ablation of RARα in mice via a CaMKIIα-Cre or a layer 5-Cre driver line or via somatosensory cortex-specific viral expression of Cre-recombinase impaired whisker-dependent texture discrimination, suggesting a critical requirement of RARα expression in L5 pyramidal neurons of somatosensory cortex for normal tactile sensory processing. Transcranial two-photon imaging revealed a significant increase in dendritic spine elimination on apical dendrites of somatosensory cortical layer 5 pyramidal neurons in these mice. Interestingly, the enhancement of spine elimination is whisker experience-dependent as whisker trimming rescued the spine elimination phenotype. Additionally, experiencing an enriched environment improved texture discrimination in RARα-deficient mice and reduced excessive spine pruning. Thus, RA signaling is essential for normal experience-dependent cortical circuit remodeling and sensory processing. The importance of synaptic RA signaling has been demonstrated in studies. However, whether RA signaling mediated by RARα contributes to neural circuit functions remains largely unknown. In this study, using a RARα conditional knock-out mouse, we performed multiple regional/cell-type-specific manipulation of RARα expression in the postnatal brain, and show that RARα signaling contributes to normal whisker-dependent texture discrimination as well as regulating spine dynamics of apical dendrites from layer (L5) pyramidal neurons in S1. Deletion of RARα in excitatory neurons in the forebrain induces elevated spine elimination and impaired sensory discrimination. Our study provides novel insights into the role of RARα signaling in cortical processing and experience-dependent spine maturation.

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Remodeling of Dendritic Spines in the Avian Vocal Motor Cortex Following Deafening Depends on the Basal Ganglia Circuit

Cited by 4 publications

References 76 publications

Deafening‐induced rapid changes to spine synaptic connectivity in the adult avian vocal basal ganglia

Deafening‐induced rapid changes to spine synaptic connectivity in the adult avian vocal basal ganglia

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

Postnatal Ablation of Synaptic Retinoic Acid Signaling Impairs Cortical Information Processing and Sensory Discrimination in Mice

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