Positive and negative modulation of word learning by reward anticipation

Callan, Daniel E.; Schweighofer, Nicolas · 2008 · Crossref

DOI: 10.1002/hbm.20383

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Summary

This study investigates the conflicting evidence regarding the impact of reward anticipation on declarative memory. While neuroscience suggests that reward enhances hippocampal plasticity via dopamine, psychological research often reports null or detrimental effects of external rewards on learning. The authors hypothesize that reward-induced anxiety mediates this discrepancy, potentially canceling the beneficial effects of reward through divided attention. To test this, the researchers employed a functional MRI (fMRI) study with 15 native Japanese speakers learning English vocabulary. Participants underwent a pretest to identify unknown words, which were then assigned to three reward conditions (300, 100, or 0 yen) or a known-word control condition during an encoding phase inside the scanner. A distracter task prevented rehearsal, followed by a delayed recall posttest. Crucially, subjects provided qualitative ratings of anxiety associated with each reward level. Behavioral analysis revealed no main effect of reward on recall performance. However, when anxiety was used as a covariate, high-reward conditions showed significantly better recall than no-reward conditions. Specifically, for the 300-yen condition, recall performance was negatively correlated with anxiety ratings ($r = -0.65, p < 0.01$). Neuroimaging results elucidated the neural mechanisms underlying these behavioral findings. Multiple regression analyses indicated that high recall performance and low anxiety in the high-reward condition were associated with enhanced activity in the midbrain dopaminergic centers (SN/VTA), the hippocampus, and the amygdala. Conversely, low recall performance and high anxiety were linked to increased activity in the anterior cingulate cortex (ACC) and the middle frontal gyrus (MFG), regions associated with anxiety and divided attention. Psycho-physiological interaction analysis further demonstrated positive functional connectivity between the SN/VTA and both the hippocampus and amygdala during high-performance/low-anxiety states. In contrast, high anxiety was associated with negative connectivity between the ACC and the amygdala. The study concludes that reward anticipation modulates word learning bidirectionally depending on the level of reward-induced anxiety. Low anxiety facilitates a neural pathway involving the amygdala, SN/VTA, and hippocampus that enhances encoding. High anxiety, however, engages the ACC and MFG, which inhibits amygdala activity and disrupts the dopaminergic modulation of the hippocampus, thereby impairing learning. These findings reconcile previous contradictory literature by identifying anxiety as the critical variable determining whether external rewards benefit or hinder declarative memory consolidation.

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• stress arousal performance