Positive and negative modulation of word learning by reward anticipation

Recent evidence from neuroscience indicates that the anticipation of external rewards may enhance declarative memory consolidation by increasing dopaminergic-modulated plasticity in the hippocampus. A number of studies in psychology, however, have shown that external rewards may have null, or even negative, effects on learning. To shed light on this issue, we developed a novel task, in which native Japanese speakers were rewarded to learn unknown English words inside a functional MRI scanner. Rewards had no effect on recall performance unless we used a rating of reward-induced anxiety as a covariate. In this case, for highly rewarded words, we found a negative correlation between recall performance and anxiety ratings. For those words, high recall performance and low anxiety ratings were associated with enhanced activity in the midbrain dopaminergic centers, the hippocampus, and the amygdala. On the other hand, low recall performance and high anxiety ratings were associated with enhanced activity in the anterior cingulate and middle frontal gyrus, brain regions that have been shown to be involved with anxiety and divided attention, respectively. A connectivity analysis indicated positive functional connectivity between the midbrain dopaminergic centers and both the hippocampus and the amygdala, as well as negative connectivity between the anterior cingulate and the amygdala. Thus, both our behavioral and imaging results suggest that the anticipation of rewards can, depending on the individual level of reward-induced anxiety, have either a beneficial effect or a negative effect on word learning.