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Successful response inhibition depends upon the delay between the cues that signal a response and its subsequent inhibition. Previous studies report activity in the right presupplementary motor area (rPreSMA), right anterior insula (rAI), and the right striatum (rSTR) when subjects attempt to inhibit responses. Although these regions are anatomically connected, how they interact during successful and unsuccessful inhibitions has not been studied. In this work, we used a temporal prediction task, functional MRI, and dynamic causal modeling to solve this question. We found selective direct activation of both the rPreSMA and the rAI during successful and unsuccessful inhibitions which also were associated with opposite modulatory effects on insular-striatal and presupplementary-motor striatal descending connections. Moreover, inputs to the rPreSMA during successful inhibitions were propagated to the rAI whereas inputs to the rAI during unsuccessful inhibitions were propagated to the rPreSMA. We interpret that the direct perturbation in the rPreSMA and the modulation of the rPreSMA → rSTR connections would facilitate response inhibition whereas weak insular activity would cause response inhibition to fail despite the existence of strong rAI → rSTR modulations. We discuss that descending connections could be nonlinearly modulated via activity of either the right inferior frontal gyrus or the left anterior cingulate cortex. From a predictive coding perspective, rAI activity during successful and unsuccessful inhibition would signal interoceptive information when subjects unexpectedly need to change behaviors.