Sex Difference in the Integration of Visual Social Stimulus and Emotional Auditory Stimulus

Project Summary Human mimicry, referred to as synchronization or the "chameleon effect," involves unconsciously imitating gestures, behaviors, facial expressions, speech patterns, and even the emotions of others. This phenomenon is pivotal in social interactions because it fosters social bonding, group cohesion, and cooperation by influencing

how others are perceived. Mimicry fosters conscious empathy, aiding individuals in understanding and empathizing with the emotions and intentions of others. Meanwhile, animals also synchronize behaviors, but there are no studies on the underlying circuit mechanisms due to the lack of laboratory paradigms. We have

developed a method to quantify the synchronization of emotional responses in mice and found that mice synchronized conditioned freezing, which required the integration of visual social stimulus and the auditory emotional cue. In both sexes, the positive synchronization required the ventral hippocampus (vHPC), its inputs

to the amygdala, and vision, suggesting that vHPC processes the partner's visual social stimuli and then feeds it into the auditory fear circuit at the amygdala level to achieve synchrony by modulating freezing. Surprisingly, vHPC inactivation caused sex-specific effects: male dyads lost the positive synchrony, but the females switched

from positive to "negative synchronization" and actively avoided aligning their freezing bouts. It suggests fundamental sex differences in the socio-emotional integrator. We will test a hypothesis that a female-specific superior colliculus-mediated alternative visual stream to the auditory fear circuit drives negative fear synchrony,

competing with the vHPC stream for positive synchrony. We will use chemogenetic disconnection in Aim 1 to identify the specific synapses underlying negative synchrony and ex vivo recording in Aim 2 to identify sex differences in the synaptic properties of the superior colliculus visual pathway. This study will generate

fundamental knowledge about sex differences in the integration of social visual information and auditory emotional information and how the brain organizes even simple behaviors through competing circuits.