Time of Day Differences in Neural Reward Functioning in Healthy Young Men

Reward function appears to be modulated by the circadian system, but little is known about the neural basis of this interaction. Previous research suggests that the neural reward response may be different in the afternoon; however, the direction of this effect is contentious. Reward response may follow the diurnal rhythm in self-reported positive affect, peaking in the early afternoon. An alternative is that daily reward response represents a type of prediction error, with neural reward activation relatively high at times of day when rewards are unexpected (i.e., early and late in the day). The present study measured neural reward activation in the context of a validated reward task at 10.00 h, 14.00 h, and 19.00 h in healthy human males. A region of interest BOLD fMRI protocol was used to investigate the diurnal waveform of activation in reward-related brain regions. Multilevel modeling found, as expected, a highly significant quadratic time-of-day effect focusing on the left putamen (p < 0.001). Consistent with the "prediction error" hypothesis, activation was significantly higher at 10.00 h and 19.00 h compared with 14.00 h. It is provisionally concluded that the putamen may be particularly important in endogenous priming of reward motivation at different times of day, with the pattern of activation consistent with circadian-modulated reward expectancies in neural pathways (i.e., greater activation to reward stimuli at unexpected times of day). This study encourages further research into circadian modulation of reward and underscores the methodological importance of accounting for time of day in fMRI protocols.SIGNIFICANCE STATEMENT This is one of the first studies to use a repeated-measures imaging procedure to explore the diurnal rhythm of reward activation. Although self-reported reward (most often operationalized as positive affect) peaks in the afternoon, the present findings indicate that neural activation is lowest at this time. We conclude that the diurnal neural activation pattern may reflect a prediction error of the brain, where rewards at unexpected times (10.00 h and 19.00 h) elicit higher activation in reward brain regions than at expected (14.00 h) times. These data also have methodological significance, suggesting that there may be a time of day influence, which should be accounted for in neural reward studies.