Separate neural systems for behavioral change and for emotional responses to failure during behavioral inhibition
Open accessAbstract
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 . © 2017 Wiley Periodicals, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The human right lateral OFC/inferior frontal gyrus is activated when behavioural correction is required in the stop-signal task.
“The human right lateral OFC/inferior frontal gyrus is also activated when behavioural correction is required in the stop-signal task (Fig. 4B) (Deng et al., 2017).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Deng et al., 2017
Successful stopping in the stop-signal task is associated with high activation of the inferior frontal gyrus and lateral orbitofrontal cortex.
“successful stopping in the stop-signal task is associated with high activation of the inferior frontal gyrus and lateral OFC (Deng et al., 2017).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Deng et al., 2017
Cites
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002) · NeuroImage · doi:10.1006/nimg.2001.0978 · Cited by 16,319 · see citing works
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Saliency, switching, attention and control: a network model of insula function
Menon, V., & Uddin, L. Q. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0262-0 · Cited by 5,592 · see citing works
The reward circuit: linking primate anatomy and human imaging
Haber, S. N., & Knutson, B. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.129 · Cited by 3,718 · see citing works
Inhibition and the right inferior frontal cortex
Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.02.010 · Cited by 3,197 · see citing works
Self-citationOngur, D. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.206 · Cited by 2,627 · see citing works
Kane, M. J., & Engle, R. W. (2002) · Psychonomic Bulletin & Review · doi:10.3758/bf03196323 · Cited by 2,229 · see citing works
Inhibition and the right inferior frontal cortex: one decade on
Aron, A. R., Robbins, T. W., & Poldrack, R. A. (2014) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2013.12.003 · Cited by 2,166 · see citing works
Self-citationFuster, J. M. (1997) · Cited by 2,095 · see citing works
Abstract reward and punishment representations in the human orbitofrontal cortex
O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., & Andrews, C. (2001) · Nature Neuroscience · doi:10.1038/82959 · Cited by 2,003 · see citing works
Self-citationStop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003) · Nature Neuroscience · doi:10.1038/nn1003 · Cited by 1,771 · see citing works
Self-citationThe Prefrontal Cortex—An Update
Fuster, J. M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00285-9 · Cited by 1,760 · see citing works
Neural mechanisms of autonomic, affective, and cognitive integration
Critchley, H. D. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20749 · Cited by 1,214 · see citing works
Visceral influences on brain and behavior
Critchley, H. D., & Harrison, N. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.008 · Cited by 1,177 · cited 2× · see citing works
“…of the AI located anterior and ventral to the insular taste cortex are part of the visceral cortex involved in autonomic responses [Critchley, 2005; Critchley and Harrison, 2013; Rolls, 2014, 2015b, r 3534 r 2016b; Simmons et al., 2013], which will be engaged by emotional states such as failure in…”
BackgroundFrontal cortex and reward-guided learning and decision-making
Rushworth, M. F. S., Noonan, M. P., Boorman, E. D., Walton, M. E., & Behrens, T. E. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.014 · Cited by 1,111 · see citing works
Goldman-Rakic, P. S. (1996) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1996.0129 · Cited by 1,072 · see citing works
Rolls, E. T., Hornak, J., Wade, D., & McGrath, J. (1994) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.57.12.1518 · Cited by 1,005 · see citing works
Self-citationArchitectonic subdivision of the human orbital and medial prefrontal cortex
Öngür, D., Ferry, A. T., & Price, J. L. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10609 · Cited by 944 · see citing works
The orbitofrontal cortex: Neuronal activity in the behaving monkey
Thorpe, S. J., Rolls, E. T., & Maddison, S. (1983) · Experimental Brain Research · doi:10.1007/bf00235545 · Cited by 836 · see citing works
Self-citationThe orbitofrontal cortex and beyond: From affect to decision-making
Rolls, E. T., & Fabian Grabenhorst, B. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2008.09.001 · Cited by 808 · see citing works
Self-citationInterference resolution: Insights from a meta-analysis of neuroimaging tasks
NEE, D. E., WAGER, T. D., & JONIDES, J. (2007) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.7.1.1 · Cited by 798 · see citing works
Value, pleasure and choice in the ventral prefrontal cortex
Grabenhorst, F., & Rolls, E. T. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2010.12.004 · Cited by 766 · see citing works
Self-citationRolls, E. T., Joliot, M., & Tzourio‐Mazoyer, N. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.07.075 · Cited by 686 · see citing works
Self-citationRole for Cingulate Motor Area Cells in Voluntary Movement Selection Based on Reward
Shima, K., & Tanji, J. (1998) · Science · doi:10.1126/science.282.5392.1335 · Cited by 653 · see citing works
Hornak, J., O'Doherty, J., Bramham, J., Rolls, E. T., Morris, R. G., Bullock, P. R., & Polkey, C. E. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/089892904322926791 · Cited by 603 · see citing works
Self-citationDifferent representations of pleasant and unpleasant odours in the human brain
Rolls, E. T., Kringelbach, M. L., & de Araújo, I. E. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02779.x · Cited by 566 · see citing works
Self-citationConflict-induced behavioural adjustment: a clue to the executive functions of the prefrontal cortex
Mansouri, F. A., Tanaka, K., & Buckley, M. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2538 · Cited by 559 · see citing works
Representations of Pleasant and Painful Touch in the Human Orbitofrontal and Cingulate Cortices
Rolls, E. T. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.3.308 · Cited by 535 · see citing works
Self-citationPrefrontal and cingulate unit activity during timing behavior in the monkey
Niki, H., & Watanabe, M. (1979) · Brain Research · doi:10.1016/0006-8993(79)90328-7 · Cited by 507 · see citing works
Duann, J., Ide, J. S., Luo, X., & Li, C. R. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.1300-09.2009 · Cited by 476 · see citing works
Emotion and Decision-making Explained
Rolls, E. T. (2013) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199659890.001.0001 · Cited by 445 · see citing works
Self-citationLimbic systems for emotion and for memory, but no single limbic system
Rolls, E. T. (2013) · Cortex · doi:10.1016/j.cortex.2013.12.005 · Cited by 428 · see citing works
Self-citationAdolescent impulsivity phenotypes characterized by distinct brain networks
the IMAGEN Consortium, Whelan, R., Conrod, P. J., Poline, J.-B., Lourdusamy, A., Banaschewski, T., Barker, G. J., Bellgrove, M. A., Büchel, C., Byrne, M., et al. (2012) · Nature Neuroscience · doi:10.1038/nn.3092 · Cited by 420 · see citing works
Self-citationThe development of social cognition in adolescence: An integrated perspective
Kilford, E. J., Garrett, E., & Blakemore, S.-J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.08.016 · Cited by 412 · see citing works
The cortical connectivity of the prefrontal cortex in the monkey brain
Yeterian, E. H., Pandya, D. Ν., Tomaiuolo, F., & Petrides, M. (2011) · Cortex · doi:10.1016/j.cortex.2011.03.004 · Cited by 404 · see citing works
Simmons, W. K., Avery, J. A., Barcalow, J. C., Bodurka, J., Drevets, W. C., & Bellgowan, P. (2013) · Human Brain Mapping · doi:10.1002/hbm.22113 · Cited by 401 · see citing works
Cieslik, E. C., Zilles, K., Caspers, S., Roski, C., Kellermann, T. S., Jakobs, O., Langner, R., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs256 · Cited by 391 · cited 1× · see citing works
“The monitoring function of the DLPFC is reported to serve behavior control [Cieslik et al., 2013], such as when we need to adapt our behavior to a changing environment, override habitual responses, or shift between different tasks [Hoshi, 2006; Mansouri et al., 2009; Miller and Cohen, 2001;…”
BackgroundAnatomy of the Prefrontal Cortex
Fuster, J. M. (2008) · The Prefrontal Cortex · doi:10.1016/b978-0-12-373644-4.00002-5 · Cited by 364 · see citing works
Cai, W., Ryali, S., Chen, T., Li, C.-S. R., & Menon, V. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3048-14.2014 · Cited by 362 · see citing works
Petrides, M., Tomaiuolo, F., Yeterian, E. H., & Pandya, D. Ν. (2011) · Cortex · doi:10.1016/j.cortex.2011.07.002 · Cited by 353 · see citing works
Neural correlates of rapid reversal learning in a simple model of human social interaction
Kringelbach, M. L., & Rolls, E. T. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00393-8 · Cited by 306 · see citing works
Self-citationPrefrontal involvement in imitation learning of hand actions: Effects of practice and expertise
Vogt, S., Buccino, G., Wohlschläger, A. M., Canessa, N., Shah, N. J., Zilles, K., Eickhoff, S. B., Freund, H., Rizzolatti, G., & Fink, G. R. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.07.005 · Cited by 300 · see citing works
Cheng, W., Rolls, E. T., Qiu, J., Liu, W., Tang, Y., Huang, C.-C., Wang, X., Zhang, J., Lin, W., Zheng, L., et al. (2016) · Brain · doi:10.1093/brain/aww255 · Cited by 294 · see citing works
Self-citationTaste, olfactory, and food reward value processing in the brain
Rolls, E. T. (2015) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.03.002 · Cited by 287 · see citing works
Self-citationCommon neural substrates for inhibition of spoken and manual responses
Xue, G., Aron, A. R., & Poldrack, R. A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm220 · Cited by 280 · see citing works
Rae, C. L., Hughes, L. E., Anderson, M. C., & Rowe, J. B. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3093-13.2015 · Cited by 270 · see citing works
Functional Organization of the Human Frontal Cortex for Mnemonic Processing.
Petrides, M. (1995) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1995.tb38133.x · Cited by 259 · see citing works
Representation of Umami Taste in the Human Brain
de Araujo, I. E. T., Kringelbach, M. L., Rolls, E. T., & Hobden, P. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00669.2002 · Cited by 254 · see citing works
Self-citationPinning down response inhibition in the brain — Conjunction analyses of the Stop-signal task
Boehler, C. N., Appelbaum, L. G., Krebs, R. M., Hopf, J., & Woldorff, M. G. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.276 · Cited by 212 · see citing works
The prefrontal cortex and working memory: physiology and brain imaging
Passingham, D., & Sakai, K. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.003 · Cited by 207 · see citing works
Memory, Attention, and Decision-Making: A unifying computational neuroscience approach
Rolls, E. T. (2007) · Cited by 205 · see citing works
Self-citationFunctional networks for cognitive control in a stop signal task: Independent component analysis
Zhang, S., & Li, C. R. (2011) · Human Brain Mapping · doi:10.1002/hbm.21197 · Cited by 188 · see citing works
A non-reward attractor theory of depression
Rolls, E. T. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.007 · Cited by 180 · see citing works
Self-citationHoshi, E. (2005) · Neuroscience Research · doi:10.1016/j.neures.2005.10.013 · Cited by 175 · see citing works
Chau, B. K. H., Sallet, J., Papageorgiou, G. K., Noonan, M. P., Bell, A. H., Walton, M. E., & Rushworth, M. F. S. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.018 · Cited by 159 · see citing works
Functions of the anterior insula in taste, autonomic, and related functions
Rolls, E. T. (2015) · Brain and Cognition · doi:10.1016/j.bandc.2015.07.002 · Cited by 157 · see citing works
Self-citationRolls, E. T. (2016) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198784852.001.0001 · Cited by 116 · see citing works
Self-citationPandya, D. Ν., Seltzer, B., Petrides, M., & Cipolloni, P. B. (2015) · Oxford University Press eBooks · doi:10.1093/med/9780195385151.001.0001 · Cited by 114 · see citing works
Cerebral Cortex: Architecture, Connections, and the Dual Origin Concept
Pandya, D. Ν., Seltzer, B., Petrides, M., & Cipolloni, P. B. (2015) · Cited by 106 · see citing works
Nymberg, C., Jia, T., Lubbe, S., Ruggeri, B., Desriviéres, S., Barker, G., Büchel, C., Fauth-Buehler, M., Cattrell, A., Conrod, P., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.03.027 · Cited by 66 · see citing works
Self-citationThe Fractionation of Supervisory Control
Shallice, T. (2004) · UCL Discovery (University College London) · Cited by 64 · see citing works
Rolls, E. T. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.02.013 · Cited by 62 · see citing works
Goldstein, K. E., Hazlett, E. A., Savage, K. R., Berlin, H. A., Hamilton, H., Zelmanova, Y., Look, A. E., Koenigsberg, H. W., Mitsis, E. M., Tang, C. Y., et al. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.11.042 · Cited by 31 · see citing works
Non-reward neural mechanisms in the orbitofrontal cortex
Rolls, E. T., & Deco, G. (2016) · Cortex · doi:10.1016/j.cortex.2016.06.023 · Cited by 25 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The orbitofrontal cortex: reward, emotion and depression
Rolls, E. T., Cheng, W., & Feng, J. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa196 · Cited by 474 · see citing works
Self-citationSpecializations for reward-guided decision-making in the primate ventral prefrontal cortex
Murray, E. A., & Rudebeck, P. H. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0013-4 · Cited by 169 · see citing works
A non-reward attractor theory of depression
Rolls, E. T. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.007 · Cited by 180 · see citing works
Self-citation
- Authors
- Deng, W., Rolls, E. T., Ji, X., Robbins, T. W., Banaschewski, T., Bokde, A. L. W., Bromberg, U., Buechel, C., Desrivières, S., Conrod, P., Flor, H., Frouin, V., Gallinat, J., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Martinot, J., Lemaitre, H., Nees, F., Papadopoulos Orfanos, D., Poustka, L., Smolka, M. N., Walter, H., Whelan, R., Schumann, G., & Feng, J.
- Affiliations
- Fudan University (CN)
- University of Warwick (GB)
- University of Cambridge (GB)
- Heidelberg University (DE)
- Trinity College Dublin (IE)
- University Medical Center Hamburg-Eppendorf (DE)
- University Medical Centre Hamburg‐Eppendorf Hamburg 20246 Germany
- King's College London (GB)
- Commissariat à l'Énergie Atomique et aux Énergies Alternatives (FR)
- University of Vermont (US)
- University of Nottingham (GB)
- Stiftung Charité (DE)
- Physikalisch-Technische Bundesanstalt (DE)
- Inserm (FR)
- 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
- Neurospin, Commissariat à l'Energie Atomique, CEA‐Saclay Center Paris France
- Neuroimaging Center (DE)
- University College Dublin (IE)
- Medical Research Council‐Social, Genetic and Developmental Psychiatry Centre Institute of Psychiatry, Psychology & Neuroscience, King's College London United Kingdom
- Corresponding author
- Feng, Jianfeng
- ORCID
- Rolls, Edmund T.
- Robbins, Trevor W.
- Banaschewski, Tobias
- Bokde, Arun L. W.
- Bromberg, Uli
- Desrivières, Sylvane
- Conrod, Patricia
- Flor, Herta
- Frouin, Vincent
- Garavan, Hugh
- Gowland, Penny
- Heinz, Andreas
- Ittermann, Bernd
- Martinot, Jean‐Luc
- Nees, Frauke
- Poustka, Luise
- Smolka, Michael N.
- Walter, Henrik
- Whelan, Robert
- Feng, Jianfeng
- Venue
- Human Brain Mapping
- Publisher
- Wiley
- Published
- 2017-04-21
- Volume
- 38
- Issue
- 7
- Pages
- 3527-3537
- ISSN
- 1065-9471 (ISSN-L)
- 1097-0193
- PMC
- PMC6866896
- OpenAlex
- W2605763473
- Cited by
- 57
- References
- 64
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 8 · 2023: 2 · 2022: 5 · 2021: 7 · 2020: 10 · 2019: 6 · 2018: 4 · 2017: 2 · 2016: 2 · 2015: 1
- FWCI
- 3.45
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Brain Mapping (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Warwick Research Archive Portal (University of Warwick) (acceptedVersion)
- GRO (submittedVersion)
- Apollo (University of Cambridge) (submittedVersion)
- Apollo
- Funders
- National Natural Science Foundation of China (NSFC No. 91630314)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Clinical Psychology › Historical and Modern Theater Studies
- Keywords
- behavioral inhibition, response inhibition, stop-signal task, lateral orbitofrontal cortex, ventrolateral prefrontal cortex, dorsolateral prefrontal cortex, anterior cingulate cortex, anterior insula, impulsivity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
