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Increasing time spent on the task (i.e., the time-on-task (ToT) effect) often results in mental fatigue. Typical effects of ToT are decreasing levels of task-related motivation and the deterioration of cognitive performance. However, a massive body of research indicates that the detrimental effects can be reversed by extrinsic motivators, for example, providing rewards to fatigued participants. Although several attempts have been made to identify brain areas involved in mental fatigue and related reward processing, the neural correlates are still less understood. In this study, we used the psychomotor vigilance task to induce mental fatigue and blood oxygen-level-dependent functional magnetic resonance imaging to investigate the neural correlates of the ToT effect and the reward effect (i.e., providing extra monetary reward after fatigue induction) in a healthy young sample. Our results were interpreted in a recently proposed neurocognitive framework. The activation of the right middle frontal gyrus, right insula and right anterior cingulate gyrus decreased as fatigue emerged and the cognitive performance dropped. However, after providing an extra reward, the cognitive performance, as well as activation of these areas, increased. Moreover, the activation levels of all of the mentioned areas were negatively associated with reaction times. Our results confirm that the middle frontal gyrus, insula and anterior cingulate cortex play crucial roles in cost-benefit evaluations, a potential background mechanism underlying fatigue, as suggested by the neurocognitive framework.