Functional Identification of Specialized Basal Ganglia Circuits that Regulate Vocal Motor Sequences
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ABSTRACT:
PROVIDER: PRJNA561195 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR10007864_1.fastq.gz | Fastqsanger.gz | |||
| SRR10007864_2.fastq.gz | Fastqsanger.gz | |||
| SRR10007865_1.fastq.gz | Fastqsanger.gz | |||
| SRR10007865_2.fastq.gz | Fastqsanger.gz |
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Project description:Production of learned vocalizations requires precise selection and accurate sequencing of appropriate vocal-motor actions. The basal ganglia are essential for the selection and sequencing of motor actions, but the cellular specializations and circuit mechanisms governing accurate sequencing of vocalizations are unknown. Here, we use single-nucleus RNA sequencing and genetic manipulations to map basal ganglia cell types and circuits involved in the production of songbird vocal sequences. We identify cell-type specializations in direct-like and indirect-like basal ganglia pathways, including evolutionary expansion of striatal and arkypallidal cell-types that could facilitate vocal sequencing. We also reversibly reduced the expression of FoxP2 with a viral knockdown. For birds in which FoxP2 was knocked down, striatal neurons exhibited decreased expression of Drd1 and showed an increased ratio of Drd2/Drd1 expression. These findings identify key evolutionary specializations and circuits essential for selection and sequencing of vocal-motor actions necessary for vocal communication.
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Project description:The identification of molecular specializations in cortical circuitry supporting complex behaviors, such as learned vocalizations, requires understanding the neuroanatomical context from which these circuits arise. In songbirds, the robust nucleus of the arcopallium (RA) provides the sole descending projection for fine motor control of vocalizations. Using single nuclei transcriptomics and spatial gene expression mapping in zebra finches, we were able to define cell types and molecular specializations that distinguish RA from adjacent regions involved in non-vocal motor and sensory processing. We describe an RA-specific vocal projection neuron, differential composition of inhibitory neuron subtypes, and unique glial specializations. We show how several cell-specific molecular features arise in a sex-dependent manner during development. Based on the molecular data, we were also able to electrophysiologically probe, for the first time, predicted GABAergic subtypes within RA. To facilitate future utilization of the data, we have developed interactive apps that allow integration of cell level molecular data with developmental and spatial distribution data from our gene expression brain atlas (ZEBrA). With this resource, users can explore molecular specializations of vocal-motor neurons and support cells that likely reflect adaptations key to the physiology and evolution of vocal control circuits.
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Project description:Similarities between speech and birdsong make songbirds advantageous for investigating the neurogenetics of learned vocal communication; a complex phenotype likely supported by ensembles of interacting genes in cortico-basal ganglia pathways of both species. To date, only FoxP2 has been identified as critical to both speech and birdsong. We performed weighted gene co-expression network analysis on microarray data from singing zebra finches to discover gene ensembles regulated during vocal behavior. We found ~2,000 singing- regulated genes comprising 3 co-expression groups unique to area X, the basal ganglia subregion dedicated to learned vocal-motor behavior. These contained known targets of human FOXP2 and potential avian targets. We validated novel biological pathways for vocalization. Our findings show that higher-order gene co-expression patterns, rather than expression levels, molecularly distinguish area X from the ventral striato-pallidum during singing. The previously unknown structure of singing-driven networks enables prioritization of molecular interactors that likely bear on human motor disorders, especially those affecting speech. Gene expression was measured in 2 basal ganglia sub-regions (area X & ventral striato-pallidum (VSP)) of 27 adult male zebra finches that sang different amounts of song over a 2hr period in the morning. 18 birds were allowed to sing freely, 9 birds were discouraged from singing by the presence of an investigator and those that sang fewer than 10 song motifs were considered “non-singers”.
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Project description:Young songbirds produce vocal "babbling," and the variability of their songs is thought to underlie a process of trial-and-error vocal learning. It is known that this exploratory variability requires the "cortical" component of a basal ganglia (BG) thalamocortical loop, but less understood is the role of the BG and thalamic components in this behavior. We found that large bilateral lesions to the songbird BG homolog Area X had little or no effect on song variability during vocal babbling. In contrast, lesions to the BG-recipient thalamic nucleus DLM (medial portion of the dorsolateral thalamus) largely abolished normal vocal babbling in young birds and caused a dramatic increase in song stereotypy. These findings support the idea that the motor thalamus plays a key role in the expression of exploratory juvenile behaviors during learning.
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Project description:We used microarrays to characterize transcriptome profiles of rat vocal fold tissue following surgical injury (vs. naive tissue); rat vocal fold fibroblasts harvested from scar tissue at the 60 d time point (vs. naive fibroblasts); rat vocal fold scar fibroblasts treated with siRNA against the collagen chaperone protein rat gp46 (vs. scramble siRNA). Adult Fischer 344 rat vocal fold tissue was harvested at 3, 14, and 60 days following surgical injury (control = age-matched naive tissue); rat vocal fold scar fibroblasts were obtained via explant culture of tissue obtained 60 days following surgical injury and harvested at 80% confluence during passage 1 (control = age-matched naive rat vocal fold fibroblasts); rat vocal fold scar fibroblasts were treated for 1 h with 50 nM liposome-delivered siRNA against rat gp46 when 80% confluent at passage 1, cultured for an additional 24 h in fresh media, then harvested (control = rat vocal fold scar fibroblasts treated with 50 nM liposome-delivered scramble siRNA).
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Project description:Similarities between speech and birdsong make songbirds advantageous for investigating the neurogenetics of learned vocal communication; a complex phenotype likely supported by ensembles of interacting genes in cortico-basal ganglia pathways of both species. To date, only FoxP2 has been identified as critical to both speech and birdsong. We performed weighted gene co-expression network analysis on microarray data from singing zebra finches to discover gene ensembles regulated during vocal behavior. We found ~2,000 singing- regulated genes comprising 3 co-expression groups unique to area X, the basal ganglia subregion dedicated to learned vocal-motor behavior. These contained known targets of human FOXP2 and potential avian targets. We validated novel biological pathways for vocalization. Our findings show that higher-order gene co-expression patterns, rather than expression levels, molecularly distinguish area X from the ventral striato-pallidum during singing. The previously unknown structure of singing-driven networks enables prioritization of molecular interactors that likely bear on human motor disorders, especially those affecting speech.
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