The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior
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PROVIDER: PRJNA823733 | ENA |
REPOSITORIES: ENA
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Project description:Social behaviors are essential for survival and reproduction and vary strongly among individuals, species, and heritable brain diseases. The molecular and cellular bases of this variation are poorly resolved, and discovering them is necessary to understand how neural circuit and behavioral functions—and dysfunctions—vary in social contexts. Here we integrate single nucleus RNA-sequencing (snRNA-seq) with comparative genomics and automated behavior analysis to investigate the neurobiology of castle-building, a recently-evolved social, spatial, goal-directed, and repetitive construction behavior in Lake Malawi cichlid fishes. We simultaneously control for and analyze two biological variables correlated with castle-building behavior: quivering, a courtship “dance” behavior, and relative gonadal mass. We find signatures of building-, quivering-, and gonadal-associated neuronal excitation, gene expression, and neurogenesis in distinct cell populations. Converging lines of evidence support the involvement of estrogen, TrkB, and CCK signaling systems, and specific pallial excitatory neuronal subpopulations, in castle-building behavior. We show additional evidence that castle-building has evolved in part through genomic divergence in a gene module that is selectively expressed in stem-like quiescent radial glial cells (RGCs) lining the ventricular zone of the pallium. This RGC subpopulation exhibits signatures of a building-associated departure from quiescence, which in turn is associated with neuronal rebalancing in the putative fish homologue of the hippocampus. Our work supports an unexpected role for glia and neurogenesis in the evolution of social behavior, and more broadly shows how snRNA-seq can be used to systematically profile the cellular bases of previously unstudied social behaviors in new species systems.
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Project description:Social behaviors are essential for survival and reproduction and vary strongly among individuals, species, and heritable brain diseases. The molecular and cellular bases of this variation are poorly resolved, and discovering them is necessary to understand how neural circuit and behavioral functions—and dysfunctions—vary in social contexts. Here we integrate single nucleus RNA-sequencing (snRNA-seq) with comparative genomics and automated behavior analysis to investigate the neurobiology of castle-building, a recently-evolved social, spatial, goal-directed, and repetitive construction behavior in Lake Malawi cichlid fishes. We simultaneously control for and analyze two biological variables correlated with castle-building behavior: quivering, a courtship “dance” behavior, and relative gonadal mass. We find signatures of building-, quivering-, and gonadal-associated neuronal excitation, gene expression, and neurogenesis in distinct cell populations. Converging lines of evidence support the involvement of estrogen, TrkB, and CCK signaling systems, and specific pallial excitatory neuronal subpopulations, in castle-building behavior. We show additional evidence that castle-building has evolved in part through genomic divergence in a gene module that is selectively expressed in stem-like quiescent radial glial cells (RGCs) lining the ventricular zone of the pallium. This RGC subpopulation exhibits signatures of a building-associated departure from quiescence, which in turn is associated with neuronal rebalancing in the putative fish homologue of the hippocampus. Our work supports an unexpected role for glia and neurogenesis in the evolution of social behavior, and more broadly shows how snRNA-seq can be used to systematically profile the cellular bases of previously unstudied social behaviors in new species systems.
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Project description:In humans, mutations in the transcription factor encoding gene, FOXP2, are associated with language and Autism Spectrum (ASD) Disorders, the latter characterized by deficits in social interactions. However, little is known regarding the function of Foxp2 in male or female social behavior. Our previous studies in mice revealed high expression of Foxp2 within the medial subnucleus of the amygdala (MeA), a limbic brain region highly implicated in innate social behaviors such as mating, aggression, and parental care. Here, using a comprehensive panel of behavioral tests in male and female Foxp2+/- heterozygous mice, we investigated the role Foxp2 plays in MeA-linked innate social behaviors. We reveal significant deficits in olfactory processing, social interaction, mating, aggressive and parental behaviors. Interestingly, some of these deficits displayed in a sex-specific manner. To examine the consequences of Foxp2 loss of function specifically in the MeA, we conducted a proteomic analysis of microdissected MeA tissue and found sex differences in a host of proteins implicated in neuronal communication, connectivity and dopamine signaling. Consistent with this, we discovered that MeA Foxp2-lineage cells were responsive to dopamine with differences between males and females. Thus, our findings reveal a central and sex-specific role for Foxp2 in social behavior and MeA function.
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