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. However, 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 cingulate 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 optogenetic 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.

Keywords: affective empathy; amygdala; anterior cingulate cortex; hippocampus; observational fear; theta rhythm synchrony.