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Hardwired to attack: Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors

View ORCID ProfileJulieta E. Lischinsky, View ORCID ProfileLuping Yin, Chenxi Shi, View ORCID ProfileNandkishore Prakash, Jared Burke, Govind Shekaran, Maria Grba, View ORCID ProfileJoshua G. Corbin, View ORCID ProfileDayu Lin
doi: https://doi.org/10.1101/2023.03.16.532692
Julieta E. Lischinsky
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
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  • ORCID record for Julieta E. Lischinsky
  • For correspondence: julieta.lischinsky@nyulangone.org dayu.lin@nyulangone.org
Luping Yin
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
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Chenxi Shi
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
2Hunter College, New York, NY, USA
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Nandkishore Prakash
3Center for Neuroscience Research, Children’s National Hospital, Washington, DC, United States
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Jared Burke
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
4Center for Neural Science, New York University, New York, NY, USA
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Govind Shekaran
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
4Center for Neural Science, New York University, New York, NY, USA
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Maria Grba
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
4Center for Neural Science, New York University, New York, NY, USA
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Joshua G. Corbin
3Center for Neuroscience Research, Children’s National Hospital, Washington, DC, United States
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  • ORCID record for Joshua G. Corbin
Dayu Lin
1Neuroscience Institute, New York University School of Medicine, New York, NY, USA
4Center for Neural Science, New York University, New York, NY, USA
5Department of Psychiatry, New York University School of Medicine, New York, NY, USA
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  • ORCID record for Dayu Lin
  • For correspondence: julieta.lischinsky@nyulangone.org dayu.lin@nyulangone.org
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Abstract

Social behaviors are innate and supported by dedicated neural circuits, but it remains unclear whether these circuits are developmentally hardwired or established through social experience. Here, we revealed distinct response patterns and functions in social behavior of medial amygdala (MeA) cells originating from two embryonically parcellated developmental lineages. MeA cells in male mice that express the transcription factor Foxp2 (MeAFoxp2) are specialized for processing male conspecific cues even before puberty and are essential for adult inter-male aggression. In contrast, MeA cells derived from the Dbx1-lineage (MeADbx1) respond broadly to social cues and are non-essential for male aggression. Furthermore, MeAFoxp2 and MeADbx1 cells show differential anatomical and functional connectivity. Altogether, our results support a developmentally hardwired aggression circuit at the level of the MeA and we propose a lineage-based circuit organization by which a cell’s embryonic transcription factor profile determines its social information representation and behavior relevance during adulthood.

Highlights

  • MeAFoxp2 cells in male mice show highly specific responses to male conspecific cues and during attack while MeADbx1 cells are broadly tuned to social cues.

  • The male-specific response of MeAFoxp2 cells is present in naïve adult males and adult social experience refines the response by increasing its trial-to-trial reliability and temporal precision.

  • MeAFoxp2 cells show biased response to males even before puberty.

  • Activation of MeAFoxp2, but not MeADbx1, cells promote inter-male aggression in naïve male mice.

  • Inactivation of MeAFoxp2, but not MeADbx1, cells suppresses inter-male aggression.

  • MeAFoxp2 and MeADbx1 cells show differential connectivity at both the input and output levels.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 17, 2023.
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Hardwired to attack: Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors
Julieta E. Lischinsky, Luping Yin, Chenxi Shi, Nandkishore Prakash, Jared Burke, Govind Shekaran, Maria Grba, Joshua G. Corbin, Dayu Lin
bioRxiv 2023.03.16.532692; doi: https://doi.org/10.1101/2023.03.16.532692
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Hardwired to attack: Transcriptionally defined amygdala subpopulations play distinct roles in innate social behaviors
Julieta E. Lischinsky, Luping Yin, Chenxi Shi, Nandkishore Prakash, Jared Burke, Govind Shekaran, Maria Grba, Joshua G. Corbin, Dayu Lin
bioRxiv 2023.03.16.532692; doi: https://doi.org/10.1101/2023.03.16.532692

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