Hemispherically lateralized rhythmic oscillations in the cingulate-amygdala circuit drive affective empathy in mice

Abstract

Observational fear, a form of emotional contagion, is thought to be a basic form of affective empathy. How-ever, the neural process engaged at the specific moment when socially acquired information provokes an emotional response remains elusive. Here, we show that reciprocal projections between the anterior cingu-late cortex (ACC) and basolateral amygdala (BLA) in the right hemisphere are essential for observational fear, and 5-7 Hz neural oscillations were selectively increased in those areas at the onset of observational freezing. A closed-loop disruption demonstrated the causal relationship between 5-7 Hz oscillations in the cingulo-amygdala circuit and observational fear responses. The increase/decrease in theta power induced by opto-genetic manipulation of the hippocampal theta rhythm bi-directionally modulated observational fear. Together, these results indicate that hippocampus-dependent 5-7 Hz oscillations in the cingulo-amygdala circuit in the right hemisphere are the essential component of the cognitive process that drives empathic fear, but not freezing, in general.