The amygdalostriatal and corticostriatal effective connectivity in anticipation and evaluation of facial attractiveness

• Connectivity of ventral striatum is investigated with an attractiveness guessing task.
• Anticipating attractive face elicits activation in amygdala and ventral striatum (VS).
• Choice-related information enters amygdala and is projected to VS.
• Feedback enters ventral medial prefrontal cortex (vmPFC) and is projected to VS.
• The VS-to-vmPFC connectivity is weakened by unattractive feedback faces.

Decision-making consists of several stages of information processing, including an anticipation stage and an outcome evaluation stage. Previous studies showed that the ventral striatum (VS) is pivotal to both stages, bridging motivation and action, and it works in concert with the ventral medial prefrontal cortex (vmPFC) and the amygdala. However, evidence concerning how the VS works together with the vmPFC and the amygdala came mainly from neuropathology and animal studies; little is known about the dynamics of this network in the functioning human brain. Here we used fMRI combined with dynamic causal modeling (DCM) to investigate the information flow along amygdalostriatal and corticostriatal pathways in a facial attractiveness guessing task. Specifically, we asked participants to guess whether a blurred photo of female face was attractive and to wait for a few seconds (“anticipation stage”) until an unblurred photo of feedback face, which was either attractive or unattractive, was presented (“outcome evaluation stage”). At the anticipation stage, the bilateral amygdala and VS showed higher activation for the “attractive” than for the “unattractive” guess. At the outcome evaluation stage, the vmPFC and the bilateral VS were more activated by feedback faces whose attractiveness was congruent with the initial guess than by incongruent faces; however, this effect was only significant for attractive faces, not for unattractive ones. DCM showed that at the anticipation stage, the choice-related information entered the amygdalostriatal pathway through the amygdala and was projected to the VS. At the evaluation stage, the outcome-related information entered the corticostriatal pathway through the vmPFC. Bidirectional connectivities existed between the vmPFC and VS, with the VS-to-vmPFC connectivity weakened by unattractive faces. These findings advanced our understanding of the reward circuitry by demonstrating the pattern of information flow along the amygdalostriatal and corticostriatal pathways at different stages of decision-making.