Directional interconnectivity of the human amygdala, fusiform gyrus, and orbitofrontal cortex in emotional scene perception

The perception of emotionally arousing scenes modulates neural activity in ventral visual areas via reentrant signals from the amygdala. The orbitofrontal cortex (OFC) shares dense interconnections with amygdala and has been strongly implicated in emotional stimulus processing in primates, but our understanding of the functional contribution of this region to emotional perception in humans is poorly defined. In this study we acquired targeted rapid functional imaging from lateral OFC, amygdala, and fusiform gyrus (FG) over multiple scanning sessions (resulting in over 1,000 trials per participant) in an effort to define the activation amplitude and directional connectivity among these regions during naturalistic scene perception. All regions of interest showed enhanced activation during emotionally arousing, compared with neutral scenes. In addition, we identified bidirectional connectivity between amygdala, FG, and OFC in the great majority of individual subjects, suggesting that human emotional perception is implemented in part via nonhierarchical causal interactions across these three regions. NEW & NOTEWORTHY Due to the practical limitations of noninvasive recording methodologies, there is a scarcity of data regarding the interactions of human amygdala and orbitofrontal cortex (OFC). Using rapid functional MRI sampling and directional connectivity, we found that the human amygdala influences emotional perception via distinct interactions with late-stage ventral visual cortex and OFC, in addition to distinct interactions between OFC and fusiform gyrus. Future efforts may leverage these patterns of directional connectivity to noninvasively distinguish clinical groups from controls with respect to network causal hierarchy.