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Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior.

ABSTRACT: Social behaviors are mediated by the activity of highly complex neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used Drosophila melanogaster to explore the molecular signature of neurons expressing receptor for neuropeptide F (NPF), the fly homolog of neuropeptide Y (NPY). By comparing the transcription profile of NPFR neurons to those of nine other populations of neurons, we discovered that NPFR neurons exhibit a unique transcriptome, enriched with receptors for various neuropeptides and neuromodulators, as well as with genes known to regulate behavioral processes, such as learning and memory. By manipulating RNA editing and protein ubiquitination programs specifically in NPFR neurons, we demonstrate that the proper expression of their unique transcriptome and proteome is required to suppress male courtship and certain features of social group interaction. Our results highlight the importance of transcriptome and proteome diversity in the regulation of complex behaviors and pave the path for future dissection of the spatiotemporal regulation of genes within highly complex tissues, such as the brain.

SUBMITTER: Ryvkin J

PROVIDER: S-EPMC8044454 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior.

Ryvkin Julia J Bentzur Assa A Shmueli Anat A Tannenbaum Miriam M Shallom Omri O Dokarker Shiran S Benichou Jennifer I C JIC Levi Mali M Shohat-Ophir Galit G

Frontiers in behavioral neuroscience 20210331

Social behaviors are mediated by the activity of highly complex neuronal networks, the function of which is shaped by their transcriptomic and proteomic content. Contemporary advances in neurogenetics, genomics, and tools for automated behavior analysis make it possible to functionally connect the transcriptome profile of candidate neurons to their role in regulating behavior. In this study we used <i>Drosophila melanogaster</i> to explore the molecular signature of neurons expressing receptor f ...[more]

PMID: 33867948

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Project description:Variation in the mutual responsiveness of social partners to each other can be reflected in behavioral suites that covary with neural activity in ways that track the salience or valence of interactions. Juvenile social isolation alters social behavior and neural activity during social interaction, but whether and how it alters the covariation between behavior and neural activity has not been as well explored. To address this issue, four classes of experimental subjects: isolated males, socially housed males, isolated females, and socially housed females, were paired with an opposite-sex social partner that had been socially housed. Social behaviors and c-Fos expression in the serotonergic dorsal raphe nucleus (DRN) were then measured in subjects following the social interactions. Relative to social housing, postweaning isolation led to a decrease in the density of neurons double-labeled for tryptophan hydroxylase and c-Fos in the dorsomedial subdivision of the DRN, regardless of sex. Vocal and non-vocal behaviors were also affected by isolation. In interactions with isolated males, both ultrasonic vocalization (USVs) and broadband vocalizations (squeaks) increased in conjunction with greater male investigation of females. Neural and behavioral measures also correlated with each other. In the isolated male group, the density of double-labeled neurons in the dorsomedial DRN was negatively correlated with USV production and positively correlated with a principal component of non-vocal behavior corresponding to greater defensive kicking by females and less investigation and mounting behavior. This correlation was reversed in direction for socially housed males, and for isolated males versus isolated females. These findings confirm that the dynamics of social interactions are reflected in c-Fos activation in the dorsomedial DRN, and suggest an altered responsiveness of serotonergic neurons to social interaction following social isolation in males, in parallel with an altered male response to female cues.

Dataset Information

Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior.

Publications

Transcriptome Analysis of NPFR Neurons Reveals a Connection Between Proteome Diversity and Social Behavior.

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