Regulation of social interaction in mice by a frontostriatal circuit modulated by established hierarchical relationships

Robert N. Fetcho, Baila S. Hall, David J. Estrin, Alexander P. Walsh, Peter J. Schuette, Jesse Kaminsky, Ashna Singh, Jacob Roshgodal, Charlotte C. Bavley, Viraj Nadkarni, Susan Antigua, Thu N. Huynh, Logan Grosenick, Camille Carthy, Lauren Komer, Avishek Adhikari, Francis S. Lee, Anjali M. Rajadhyaksha () and Conor Liston ()
Additional contact information
Robert N. Fetcho: Weill Cornell Medicine
Baila S. Hall: Weill Cornell Medicine
David J. Estrin: Weill Cornell Medicine
Alexander P. Walsh: Weill Cornell Medicine
Peter J. Schuette: University of California, Los Angeles
Jesse Kaminsky: Weill Cornell Medicine
Ashna Singh: Weill Cornell Medicine
Jacob Roshgodal: Weill Cornell Medicine
Charlotte C. Bavley: Weill Cornell Medicine
Viraj Nadkarni: Weill Cornell Medicine
Susan Antigua: Weill Cornell Medicine
Thu N. Huynh: Weill Cornell Medicine
Logan Grosenick: Weill Cornell Medicine
Camille Carthy: Weill Cornell Medicine
Lauren Komer: Weill Cornell Medicine
Avishek Adhikari: University of California, Los Angeles
Francis S. Lee: Weill Cornell Medicine
Anjali M. Rajadhyaksha: Weill Cornell Medicine
Conor Liston: Weill Cornell Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract Social hierarchies exert a powerful influence on behavior, but the neurobiological mechanisms that detect and regulate hierarchical interactions are not well understood, especially at the level of neural circuits. Here, we use fiber photometry and chemogenetic tools to record and manipulate the activity of nucleus accumbens-projecting cells in the ventromedial prefrontal cortex (vmPFC-NAcSh) during tube test social competitions. We show that vmPFC-NAcSh projections signal learned hierarchical relationships, and are selectively recruited by subordinate mice when they initiate effortful social dominance behavior during encounters with a dominant competitor from an established hierarchy. After repeated bouts of social defeat stress, this circuit is preferentially activated during social interactions initiated by stress resilient individuals, and plays a necessary role in supporting social approach behavior in subordinated mice. These results define a necessary role for vmPFC-NAcSh cells in the adaptive regulation of social interaction behavior based on prior hierarchical interactions.

Date: 2023
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DOI: 10.1038/s41467-023-37460-6

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