Separate neural systems for behavioral change and for emotional responses to failure during behavioral inhibition

Wanlu Deng, Edmund T. Rolls, Xiaoxi Ji, Trevor W. Robbins, Tobias Banaschewski, Arun L. W. Bokde, Uli Bromberg, Christian Buechel, Sylvane Desrivières, Patricia Conrod, Herta Flor, Vincent Frouin, Juergen Gallinat, Hugh Garavan, Penny Gowland, Andreas Heinz, Bernd Ittermann, Jean‐Luc Martinot, Herve Lemaitre, Frauke Nees, Dimitri Papadopoulos Orfanos, Luise Poustka, Michael N. Smolka, Henrik Walter, Robert Whelan, Gunter Schumann, Jianfeng Feng

To analyze the involvement of different brain regions in behavioral inhibition and impulsiveness, differences in activation were investigated in fMRI data from a response inhibition task, the stop-signal task, in 1709 participants. First, areas activated more in stop-success (SS) than stop-failure (SF) included the lateral orbitofrontal cortex (OFC) extending into the inferior frontal gyrus (ventrolateral prefrontal cortex, BA 47/12), and the dorsolateral prefrontal cortex (DLPFC). Second, the anterior cingulate and anterior insula (AI) were activated more on failure trials, specifically in SF versus SS. The interaction between brain region and SS versus SF activations was significant (P = 5.6 * 10(-8) ). The results provide new evidence from this "big data" investigation consistent with the hypotheses that the lateral OFC is involved in the stop-related processing that inhibits the action; that the DLPFC is involved in attentional processes that influence task performance; and that the AI and anterior cingulate are involved in emotional processes when failure occurs. The investigation thus emphasizes the role of the human lateral OFC BA 47/12 in changing behavior, and inhibiting behavior when necessary. A very similar area in BA47/12 is involved in changing behavior when an expected reward is not obtained, and has been shown to have high functional connectivity in depression. Hum Brain Mapp, 2017. © 2017 Wiley Periodicals, Inc.