Familiarity gates socially transmitted aggression via the medial amygdala

Aggressive behavior can be acquired through observation, providing adaptive advantages but also posing significant social risks. In humans, individuals repeatedly exposed to aggression are more likely to engage in violent behavior later in life. Yet, the environmental factors and neural mechanisms underlying observationally acquired aggression remain unclear. Here, we propose that social familiarity with an aggressor is critical for activating neural circuits in observers that primes aggression. To investigate this, we established a novel behavioral paradigm termed “socially transmitted aggression (STA),” in which witness mice observed either familiar or unfamiliar demonstrators attacking intruder mice. Remarkably, male, but not female, witnesses displayed increased aggression only after observing familiar demonstrators, with no effect from unfamiliar ones. Given that excitatory neurons in the posterior ventral segment of the medial amygdala (MeApv) have been implicated in aggression priming, we hypothesized these neurons might be involved in STA as well. Supporting this hypothesis, fiber photometry revealed selective activation of excitatory MeApv neurons during familiar, but not unfamiliar, demonstrator attacks. Chemogenetically and optogenetically inhibiting these neurons suppressed STA, while activating them during unfamiliar demonstrator attacks promoted aggression. These results establish social familiarity as essential for the observational transmission of aggression and identify excitatory MeApv neurons as critical mediators of this phenomenon, offering potential avenues for clinical intervention. Significance statement Observational learning of aggression contributes significantly to antisocial behavior, yet the neural circuits and social factors underlying this phenomenon remain poorly understood. This study reveals that familiarity with an aggressor is essential for socially transmitted aggression in mice, mediated by activation of excitatory neurons in the posterior-ventral medial amygdala (MeApv). Using fiber photometry, chemogenetics, and optogenetics, we demonstrate that MeApv neuronal activity is necessary and sufficient for the expression of learned aggression. These findings uncover a neural circuit mechanism linking social identity with aggressive behavior, highlighting a potential therapeutic target for reducing pathological aggression and violence transmitted within familiar social groups.