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

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Wanlu Deng - , Fudan University, University of Warwick (Author)
  • Edmund T. Rolls - , University of Warwick, University of Oxford (Author)
  • Xiaoxi Ji - , Fudan University (Author)
  • Trevor W. Robbins - , University of Cambridge (Author)
  • Tobias Banaschewski - , Heidelberg University  (Author)
  • Arun L.W. Bokde - , Trinity College Dublin (Author)
  • Uli Bromberg - , University of Hamburg (Author)
  • Christian Buechel - , University of Hamburg (Author)
  • Sylvane Desrivières - , King's College London (KCL) (Author)
  • Patricia Conrod - , University of Montreal, King's College London (KCL) (Author)
  • Herta Flor - , Heidelberg University  (Author)
  • Vincent Frouin - , French Alternative Energies and Atomic Energy Commission (CEA) (Author)
  • Juergen Gallinat - , University of Hamburg (Author)
  • Hugh Garavan - , University of Vermont (Author)
  • Penny Gowland - , University of Nottingham (Author)
  • Andreas Heinz - , Charité – Universitätsmedizin Berlin (Author)
  • Bernd Ittermann - , Physikalisch-Technische Bundesanstalt (Author)
  • Jean Luc Martinot - , INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Herve Lemaitre - , INSERM - Institut national de la santé et de la recherche médicale, Maison de Solenn (Author)
  • Frauke Nees - , Heidelberg University  (Author)
  • Dimitri Papadopoulos Orfanos - , French Alternative Energies and Atomic Energy Commission (CEA) (Author)
  • Luise Poustka - , Heidelberg University , Medical University of Vienna (Author)
  • Michael N. Smolka - , Neuroimaging Center, Department of Psychiatry and Psychotherapy (Author)
  • Henrik Walter - , Charité – Universitätsmedizin Berlin (Author)
  • Robert Whelan - , University College Dublin (Author)
  • Gunter Schumann - , King's College London (KCL) (Author)
  • Jianfeng Feng - , Fudan University, University of Warwick (Author)

Abstract

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.

Details

Original languageEnglish
Pages (from-to)3527-3537
Number of pages11
JournalHuman brain mapping
Volume38
Issue number7
Publication statusPublished - 2017
Peer-reviewedYes

External IDs

PubMed 28429498
ORCID /0000-0001-5398-5569/work/161890755

Keywords

Keywords

  • Cingulate cortex, Depression, Impulsive behavior, Inhibition, Insula, Orbitofrontal cortex