A human colliculus-pulvinar-amygdala pathway encodes negative emotion

Animals must rapidly respond to threats to survive. In rodents, threat-related signals are processed through a subcortical pathway from the superior colliculus to the amygdala, a putative "low road" to affective behavior. This pathway has not been well characterized in humans. We developed a novel pathway identification framework that uses pattern recognition to identify connected neural populations and optimize measurement of inter-region connectivity. We first verified that the model identifies known thalamocortical pathways with high sensitivity and specificity in 7 T (n = 56) and 3 T (n = 48) fMRI experiments. Then we identified a human functional superior colliculus-pulvinar-amygdala pathway. Activity in this pathway encodes the intensity of normative emotional responses to negative images and sounds but not pleasant images or painful stimuli. These results provide a functional description of a human "low road" pathway selective for negative exteroceptive events and demonstrate a promising method for characterizing human functional brain pathways.