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Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors.

ABSTRACT: Social behaviors are innate and supported by dedicated neural circuits, but the molecular identities of these circuits and how they are established developmentally and shaped by experience remain unclear. Here we show that medial amygdala (MeA) cells originating from two embryonically parcellated developmental lineages have distinct response patterns and functions in social behavior in male mice. MeA cells expressing the transcription factor Foxp2 (MeA^Foxp2) are specialized for processing male conspecific cues and are essential for adult inter-male aggression. By contrast, MeA cells derived from the Dbx1 lineage (MeA^Dbx1) respond broadly to social cues, respond strongly during ejaculation and are not essential for male aggression. Furthermore, MeA^Foxp2 and MeA^Dbx1 cells show differential anatomical and functional connectivity. Altogether, our results suggest a developmentally hardwired aggression circuit at the MeA level and a lineage-based circuit organization by which a cell's embryonic transcription factor profile determines its social information representation and behavioral relevance during adulthood.

SUBMITTER: Lischinsky JE

PROVIDER: S-EPMC10689240 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors.

Lischinsky Julieta E JE Yin Luping L Shi Chenxi C Prakash Nandkishore N Burke Jared J Shekaran Govind G Grba Maria M Corbin Joshua G JG Lin Dayu D

Nature neuroscience 20231109 12

Social behaviors are innate and supported by dedicated neural circuits, but the molecular identities of these circuits and how they are established developmentally and shaped by experience remain unclear. Here we show that medial amygdala (MeA) cells originating from two embryonically parcellated developmental lineages have distinct response patterns and functions in social behavior in male mice. MeA cells expressing the transcription factor Foxp2 (MeA<sup>Foxp2</sup>) are specialized for proces ...[more]

PMID: 37946049

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Project description:Social play is a frequently studied behavior and it is the most characteristic form of social interaction observed in adolescent rats. Social play is necessary for adolescents to develop proper cognitive, emotional, and social competency. Deficits in social play have been observed in several neurodegenerative disorders such as autism, schizophrenia, and attention deficit hyperactivity disorder. However, the information available on neural substrates and the mechanism involved in social play is still limited. This study characterized social play by proteomic and transcriptional profiling studies. Social play was performed on male Sprague Dawley rats on postnatal day 38 and protein and gene expression in the amygdala was determined following behavioral testing. The proteomic analysis led to the identification of 170 differentially expressed proteins (p≤0.05) with 67 upregulated and 103 downregulated proteins. The transcriptomic analysis led to the identification of 188 genes (adjusted p≤0.05) with 55 upregulated and 133 downregulated genes. Based on both protein and gene expression data, DAVID analysis revealed that social play altered neurotransmitter signaling including GABAergic and glutamatergic signaling and G-protein coupled receptor (GPCR) signaling. These data suggest that the synaptic levels of GABA and glutamate increased during play. Ingenuity Pathway Analysis (IPA) confirmed these alterations. IPA also revealed that differentially expressed genes/proteins in our data had significant over representation of additional neurotransmitter signaling systems, including the opioid, serotonin, and dopamine systems, suggesting that play alters the systems involved in the regulation of reward. In addition, corticotropin-releasing hormone signaling was altered indicating that an increased level of stress occurs during play. Our data suggest that increased inhibitory GPCR signaling in these neurotransmitter pathways occurs following social play as a physiological response to regulate the induced level of reward and stress and to maintain the excitatory-inhibitory balance in the neurotransmitter systems.

Dataset Information

Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors.

Publications

Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors.

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