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Hum Brain Mapp. 2017 Jul;38(7):3527-3537. doi: 10.1002/hbm.23607. Epub 2017 Apr 21.

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

Author information

1
Shanghai Center for Mathematical Sciences, Fudan University, Shanghai, People's Republic of China.
2
Department of Computer Science, University of Warwick, Coventry, United Kingdom.
3
Oxford Centre for Computational Neuroscience, Oxford, United Kingdom.
4
Centre for Computational Systems Biology, School of Mathematical Sciences, School of Life Science and the Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, People's Republic of China.
5
Department of Psychology, University of Cambridge, CB2 3EB, United Kingdom.
6
Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, 68159, Germany.
7
Discipline of Psychiatry, School of Medicine and Trinity College Institute of Neurosciences, Trinity College Dublin, Ireland.
8
University Medical Centre Hamburg-Eppendorf, Hamburg, 20246, Germany.
9
Medical Research Council-Social, Genetic and Developmental Psychiatry Centre, Institute of Psychiatry, Psychology & Neuroscience, King's College London, United Kingdom.
10
Department of Psychiatry, Université de Montreal, CHU Ste Justine Hospital, Montréal, Quebec, H3T 1C4, Canada.
11
Department of Psychological Medicine and Psychiatry, Institute of Psychiatry, Psychology & Neuroscience, King's College London, United Kingdom.
12
Department of Cognitive and Clinical Neuroscience, Central Institute of Mental Health, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
13
Neurospin, Commissariat à l'Energie Atomique, CEA-Saclay Center, Paris, France.
14
Department of Psychiatry and Psychotherapy, University Medical Center Hamburg-Eppendorf (UKE), Hamburg, 20246, Germany.
15
Departments of Psychiatry and Psychology, University of Vermont, 05405 Burlington, Vermont.
16
Sir Peter Mansfield Imaging Centre School of Physics and Astronomy, University of Nottingham, University Park, Nottingham, United Kingdom.
17
Department of Psychiatry and Psychotherapy, Campus Charité Mitte, Charité, Universitätsmedizin Berlin, Charitéplatz 1, Berlin, Germany.
18
Physikalisch-Technische Bundesanstalt (PTB), Braunschweig and Berlin, Germany [or depending on journal requirements can be: Physikalisch-Technische Bundesanstalt (PTB)], Berlin, Germany.
19
Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging & Psychiatry", University Paris Sud, University Paris Descartes - Sorbonne Paris Cité; and Maison de Solenn, Paris, France.
20
Institut National de la Santé et de la Recherche Médicale, INSERM Unit 1000 "Neuroimaging & Psychiatry", University Paris Sud, University Paris Descartes-Sorbonne Paris Cité, Paris, France.
21
Maison de Solenn, Paris, France.
22
Department of Child and Adolescent Psychiatry and Psychotherapy, Medical University of Vienna, Austria.
23
Department of Psychiatry and Neuroimaging Center, Technische Universität Dresden, Germany.
24
Department of Psychology, University College Dublin, Ireland.

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. Hum Brain Mapp 38:3527-3537, 2017.

KEYWORDS:

cingulate cortex; depression; impulsive behavior; inhibition; insula; orbitofrontal cortex

PMID:
28429498
DOI:
10.1002/hbm.23607

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