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Imaging Response Inhibition in a Stop-Signal Task: Neural Correlates Independent of Signal Monitoring and Post-Response Processing
Open accessAbstract
Execution of higher cortical functions requires inhibitory control to restrain habitual responses and meet changing task demands. We used functional magnetic resonance imaging to show the neural correlates of response inhibition during a stop-signal task. The task has a frequent "go" stimulus to set up a pre-potent response tendency and a less frequent "stop" signal for subjects to withhold their response. We contrasted brain activation between successful and failed inhibition for individual subjects and compared groups of subjects with short and long stop-signal reaction times. The two groups of subjects did not differ in their inhibition failure rates or the extent of signal monitoring, error monitoring, or task-associated frustration ratings. The results showed that short stop-signal reaction time or more efficient response inhibition was associated with greater activation in the superior medial and precentral frontal cortices. Moreover, activation of these inhibitory motor areas correlated negatively with stop-signal reaction time. These brain regions may represent the neural substrata of response inhibition independent of other cognitive and affective functions.
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“Recent studies using a variety of methods suggest that stopping is associated with activation of a fronto-basal-ganglia circuit that includes inferior frontal gyrus (IFG; ventrolateral prefrontal cortex), middle frontal gyrus (dorsolateral prefrontal cortex), medial frontal gyrus (MFG), and basal ganglia [14–18].”
From Response inhibition in the stop-signal paradigm (2008) · cites this paper as [16]
In the citing paper
“Event-related fMRI studies showed that (mainly) parietal and frontal brain regions are more activated when inhibition is unsuccessful [15, 16, 18, 19].”
From Response inhibition in the stop-signal paradigm (2008) · cites this paper as [16]
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Cites
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“With the staircase procedure, a “critical” SSD could be computed that represented the time delay required for the subject to succeed in withholding a response in the stop trials half of the time (Levitt, 1970).”
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OCHSNER, K., & GROSS, J. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2005.03.010 · Cited by 4,495 · cited 2×
“One would thus expect the anterior cingulate cortex to participate in a wide variety of cognitive and affective tasks in which inhibitory control assumes an integral position (Schall et al., 2002; Phillips et al., 2003; Dalley et al., 2004; Isomura and Takada, 2004; Nieuwenhuis et al., 2004; Ridderinkhof et al., 2004;…”
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BackgroundAbstract 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
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“But perhaps most relevant to the current study is the hypothesis that the IFC mediates outcome monitoring of behavior (Kringelbach and Rolls, 2004).”
BackgroundNonlinear spatial normalization using basis functions
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“Although signal monitoring can explain the activation of the IFC in these previous neuroimaging studies and the work of Aron et al. (2003) found that patients with right inferior frontal lesions were impaired in stop-signal inhibitions, a general attention mechanism could also be at play in causing…”
ResultRidderinkhof, K. R., van den Wildenberg, W. P. M., Segalowitz, S. J., & Carter, C. S. (2004) · Brain and Cognition · doi:10.1016/j.bandc.2004.09.016 · Cited by 1,407 · cited 2×
“One would thus expect the anterior cingulate cortex to participate in a wide variety of cognitive and affective tasks in which inhibitory control assumes an integral position (Schall et al., 2002; Phillips et al., 2003; Dalley et al., 2004; Isomura and Takada, 2004; Nieuwenhuis et al., 2004; Ridderinkhof et al., 2004;…”
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MethodErrors and error correction in choice-response tasks.
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RUSHWORTH, M., WALTON, M., KENNERLEY, S., & BANNERMAN, D. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.07.009 · Cited by 1,004 · cited 2×
“Activation in the anterior cingulate did not correlate with SSRT, EM effect, or frustrating rating, suggesting that this brain region probably plays a more complicated role that would require additional studies to understand (Bush et al., 2000; Rushworth et al., 2004).”
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“However, the exact locale of the activated IFC area varied from one study to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001,…”
BackgroundThe problem of functional localization in the human brain
Morgan, T. (2002) · Cited by 968
Frontal lobe and cognitive development
Fuster, J. M. (2002) · Journal of Neurocytology · doi:10.1023/a:1024190429920 · Cited by 916 · cited 1×
“These findings speak broadly to a role of the frontal cortex in the temporal organization of motor sets and inhibitions (Fuster, 2002).”
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“However, the exact locale of the activated IFC area varied from one study to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001,…”
BackgroundKonishi, S., Nakajima, K., Uchida, I., Kikyo, H., Kameyama, M., & Miyashita, Y. (1999) · Brain · doi:10.1093/brain/122.5.981 · Cited by 823 · cited 1×
“However, the exact locale of the activated IFC area varied from one study to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001,…”
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“Lesions of the IFC could thus result in indiscriminating responses to unexpected sudden onsets that mimic behavioral perseveration, as demonstrated by these monkeys in the go/nogo task (Iversen and Mishkin, 1970).”
ResultA physiological correlate of the 'spotlight' of visual attention
Brefczynski, J. A., & DeYoe, E. A. (1999) · Nature Neuroscience · doi:10.1038/7280 · Cited by 723 · cited 1×
“Previous imaging studies have shown that attention modulates visual cortical activation and allocation of attention to central vision can lead to concurrent deactivation of peripheral visual cortices (Brefczynski and DeYoe, 1999; Smith et al., 2000; Slotnick et al., 2003).”
BackgroundAron, A. R., & Poldrack, R. A. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2004.10.026 · Cited by 602 · cited 1×
“Previous studies have shown that patients with a variety of psychiatric and neurological conditions, including attention deficit hyperactivity disorder, have impaired response inhibition during such tasks (Aron and Poldrack, 2005).”
BackgroundNieuwenhuis, S., Holroyd, C. B., Mol, N., & Coles, M. G. H. (2004) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2004.05.003 · Cited by 557 · cited 1×
“…to participate in a wide variety of cognitive and affective tasks in which inhibitory control assumes an integral position (Schall et al., 2002; Phillips et al., 2003; Dalley et al., 2004; Isomura and Takada, 2004; Nieuwenhuis et al., 2004; Ridderinkhof et al., 2004; Ochsner and Gross, 2005).”
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“However, the exact locale of the activated IFC area varied from one study to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001,…”
BackgroundDissociable prefrontal brain systems for attention and emotion
Yamasaki, H., LaBar, K. S., & McCarthy, G. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.182176499 · Cited by 489 · cited 1×
“These results suggest that the function of the IFC may extend beyond signal monitoring and mediate other aspects of attention function such as detection of behaviorally relevant, salient stimuli (Corbetta and Shulman, 2002; Yamasaki et al., 2002).”
BackgroundInteractions between decision making and performance monitoring within prefrontal cortex
Walton, M. E., Devlin, J. T., & Rushworth, M. F. S. (2004) · Nature Neuroscience · doi:10.1038/nn1339 · Cited by 445 · cited 1×
“Related to this hypothesis, a recent fMRI study showed greater activation in the IFC when subjects had to select an externally guided response and monitor its outcome compared with when they selected an instructed response and had already known the outcome of their selection (Walton et al., 2004).”
ResultKonishi, S., Nakajima, K., Uchida, I., Sekihara, K., & Miyashita, Y. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00167.x · Cited by 386 · cited 2×
“However, the exact locale of the activated IFC area varied from one study to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001,…”
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Kuchinke, L., Jacobs, A. M., Grubich, C., Võ, M. L. ‐., Conrad, M., & Herrmann, M. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.06.050 · Cited by 371 · cited 1×
“Indeed, the IFC has been implicated in affective processing (Fulbright et al., 2001; Nomura et al., 2003; Hennenlotter et al., 2005; Kuchinke et al., 2005; Wood et al., 2005).”
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Durston, S., Thomas, K. M., Worden, M. S., Yang, Y., & Casey, B. J. (2002) · NeuroImage · doi:10.1006/nimg.2002.1074 · Cited by 357 · cited 3×
“…to another (Konishi et al., 1998, 1999; Garavan et al., 1999, 2001; Rubia et al., 2001, 2003, 2005; Watanabe et al., 2002; Fassbender et al., 2004), including activation of the left IFC in some studies (Rubia et al., 2001, 2005; Durston et al., 2002; Watanabe et al., 2002; Fassbender et al., 2004).”
BackgroundMethodVolition and Conflict in Human Medial Frontal Cortex
Nachev, P., Rees, G. E., Parton, A. D., Kennard, C., & Husain, M. (2005) · Current Biology · doi:10.1016/j.cub.2005.01.006 · Cited by 331 · cited 1×
“Moreover, a recent study using an oculomotor paradigm found greater activation in the rostral pre-SMA in trials requiring a change in motor plan compared with those trials not requiring such a change (Nachev et al., 2005).”
ResultMonitoring and Control of Action by the Frontal Lobes
Schall, J. D., Stuphorn, V., & Brown, J. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00964-9 · Cited by 286 · cited 1×
“…cingulate cortex to participate in a wide variety of cognitive and affective tasks in which inhibitory control assumes an integral position (Schall et al., 2002; Phillips et al., 2003; Dalley et al., 2004; Isomura and Takada, 2004; Nieuwenhuis et al., 2004; Ridderinkhof et al., 2004;…”
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Shima, K., Mushiake, H., Saito, N., & Tanji, J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.16.8694 · Cited by 245 · cited 1×
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BackgroundA common neural basis for receptive and expressive communication of pleasant facial affect
Hennenlotter, A., Schröeder, U., Erhard, P., Castrop, F., Haslinger, B., Stöcker, D., Lange, K. W., & Ceballos-Baumann, A. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.01.057 · Cited by 231 · cited 2×
“Indeed, the IFC has been implicated in affective processing (Fulbright et al., 2001; Nomura et al., 2003; Hennenlotter et al., 2005; Kuchinke et al., 2005; Wood et al., 2005).”
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Attentional suppression of activity in the human visual cortex
Smith, A. T., Singh, K. D., & Greenlee, M. W. (2000) · Neuroreport · doi:10.1097/00001756-200002070-00010 · Cited by 224 · cited 1×
“Previous imaging studies have shown that attention modulates visual cortical activation and allocation of attention to central vision can lead to concurrent deactivation of peripheral visual cortices (Brefczynski and DeYoe, 1999; Smith et al., 2000; Slotnick et al., 2003).”
BackgroundCortical electrical stimulation in humans. The negative motor areas.
Lüders, H. O., Dinner, D. S., Morris, H. H., Wyllie, E., & Comair, Y. G. (1995) · PubMed · Cited by 193
Attentional inhibition of visual processing in human striate and extrastriate cortex
Slotnick, S. D., Schwarzbach, J. V., & Yantis, S. (2003) · NeuroImage · doi:10.1016/s1053-8119(03)00187-3 · Cited by 166 · cited 1×
“Previous imaging studies have shown that attention modulates visual cortical activation and allocation of attention to central vision can lead to concurrent deactivation of peripheral visual cortices (Brefczynski and DeYoe, 1999; Smith et al., 2000; Slotnick et al., 2003).”
BackgroundToma, K., Honda, M., Hanakawa, T., Okada, T., Fukuyama, H., Ikeda, A., Nishizawa, S., Konishi, J., & Shibasaki, H. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03527.1999 · Cited by 156 · cited 1×
“Consistent with the current results, a previous imaging study implicated pre-SMA in mediating the motor inhibition required for voluntary muscle relaxation (Toma et al., 1999).”
ResultYazawa, S., Ikeda, A., Kunieda, T., Ohara, S., Mima, T., Nagamine, T., Taki, W., Kimura, J., Hori, T., & Shibasaki, H. (2000) · Experimental Brain Research · doi:10.1007/s002219900311 · Cited by 154 · cited 2×
“These “negative motor areas,” including a medial frontal region that has been identified as a presupplementary motor area (pre-SMA) and a lateral frontal region located anterior to the face motor cortex, appeared to correspond to the IMA identified in the current study (Ikeda et al., 2000; Yazawa et al., 2000).”
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“The middle/inferior frontal cortices have also been implicated in EM and feedback processing (O’Doherty et al., 2001; Jimura et al., 2004; Kemmotsu et al., 2005; Paulus et al., 2005).”
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Fulbright, R. K., Troche, C. J., Skudlarski, P., Gore, J. C., & Wexler, B. E. (2001) · American Journal of Roentgenology · doi:10.2214/ajr.177.5.1771205 · Cited by 120 · cited 1×
“Indeed, the IFC has been implicated in affective processing (Fulbright et al., 2001; Nomura et al., 2003; Hennenlotter et al., 2005; Kuchinke et al., 2005; Wood et al., 2005).”
BackgroundSearching for activations that generalize over tasks
Shulman, G. L., Corbetta, M., Fiez, J. A., Buckner, R. L., Miezin, F. M., Raichle, M. E., & Petersen, S. E. (1997) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(1997)5:4 · Cited by 85
Role of primary sensorimotor cortices in generating inhibitory motor response in humans
Ikeda, A. (2000) · Brain · doi:10.1093/brain/123.8.1710 · Cited by 78 · cited 1×
“…motor areas,” including a medial frontal region that has been identified as a presupplementary motor area (pre-SMA) and a lateral frontal region located anterior to the face motor cortex, appeared to correspond to the IMA identified in the current study (Ikeda et al., 2000; Yazawa et al., 2000).”
ResultFrontal lobe networks for effective processing of ambiguously expressed emotions in humans
Nomura, M., Iidaka, T., Kakehi, K., Tsukiura, T., Hasegawa, T., Maeda, Y., & Matsue, Y. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00768-7 · Cited by 63 · cited 1×
“Indeed, the IFC has been implicated in affective processing (Fulbright et al., 2001; Nomura et al., 2003; Hennenlotter et al., 2005; Kuchinke et al., 2005; Wood et al., 2005).”
BackgroundActivity and functional connectivity of inferior frontal cortex associated with response conflict
Kemmotsu, N., Villalobos, M., Gaffrey, M. S., Courchesne, E., & Müller, R.-A. (2005) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2005.02.015 · Cited by 61 · cited 1×
“The middle/inferior frontal cortices have also been implicated in EM and feedback processing (O’Doherty et al., 2001; Jimura et al., 2004; Kemmotsu et al., 2005; Paulus et al., 2005).”
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Single-neuron activity in the human supplementary motor area underlying preparation for action
Amador, N., & Fried, I. (2004) · Journal of neurosurgery · doi:10.3171/jns.2004.100.2.0250 · Cited by 55 · cited 1×
“Electrophysiological studies in awake monkeys and humans have long shown neural activities in the medial frontal and premotor cortices during changes in motor plans and execution of movement sequences (Amador and Fried, 2004; Leuthold and Jentzsch, 2002; Shima et al., 1996; Wise and Mauritz, 1985).”
BackgroundNeural Mechanisms of Versatile Functions in Primate Anterior Cingulate Cortex
Isomura, Y., & Takada, M. (2004) · Reviews in the Neurosciences · doi:10.1515/revneuro.2004.15.4.279 · Cited by 46 · cited 2×
“One would thus expect the anterior cingulate cortex to participate in a wide variety of cognitive and affective tasks in which inhibitory control assumes an integral position (Schall et al., 2002; Phillips et al., 2003; Dalley et al., 2004; Isomura and Takada, 2004; Nieuwenhuis et al., 2004; Ridderinkhof et al., 2004;…”
BackgroundWood, J. N., Romero, S. G., Knutson, K. M., & Grafman, J. H. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.11.011 · Cited by 43 · cited 1×
“Indeed, the IFC has been implicated in affective processing (Fulbright et al., 2001; Nomura et al., 2003; Hennenlotter et al., 2005; Kuchinke et al., 2005; Wood et al., 2005).”
BackgroundJimura, K., Konishi, S., & Miyashita, Y. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.04.012 · Cited by 31 · cited 1×
“The middle/inferior frontal cortices have also been implicated in EM and feedback processing (O’Doherty et al., 2001; Jimura et al., 2004; Kemmotsu et al., 2005; Paulus et al., 2005).”
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“Electrophysiological studies in awake monkeys and humans have long shown neural activities in the medial frontal and premotor cortices during changes in motor plans and execution of movement sequences (Amador and Fried, 2004; Leuthold and Jentzsch, 2002; Shima et al., 1996; Wise and Mauritz, 1985).”
BackgroundLiddle (2001) · doi:10.1002/1097-0193(200102)12:2
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“Both change-of-plan and stop tasks for hand and eye movements have demonstrated pre-SMA and/or SEF activity that is related specifically to altering movement plan”
BackgroundInhibition and impulsivity: behavioral and neural basis of response control
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“In particular, suppression produced significant responses in areas of right ventrolateral PFC previously related to inhibitory motor control (24-31).”
Verdejo‐García, A., Lawrence, A. J., & Clark, L. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.11.003 · Cited by 1,502
“, 2007), increased stop signal reaction time on the Stop Signal task (Fillmore and Rush, 2002; Li et al., 2006), and increased interference scores on the Stroop (Bolla et al.”
Background
Metadata
- Authors
- Ray Li, C.-S., Huang, C., Constable, R. T., & Sinha, R.
- Affiliations
- Yale University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-01-04
- Volume
- 26
- Issue
- 1
- Pages
- 186-192
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674298
- OpenAlex
- W2124906793
- Cited by
- 600
- References
- 61
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 38 · 2023: 18 · 2022: 26 · 2021: 27 · 2020: 29 · 2019: 33 · 2018: 35 · 2017: 32 · 2016: 33 · 2015: 36 · 2014: 43 · 2013: 37 · 2012: 43
- FWCI
- 11.81
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Yale University
- National Institutes of Health
- National Institute on Drug Abuse (K02 DA17232, P50DA016556, K02DA017232, K12DA014038, K12-DA-14038, P50-DA16556)
- Office of Research on Women's Health
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- response inhibition, stop-signal task, inhibitory control, stop-signal reaction time, error monitoring, signal monitoring, frustration, neural correlates of inhibition
- MeSH terms
- Adult, Brain Mapping, Cerebral Cortex, Female, Humans, Inhibition, Psychological, Magnetic Resonance Imaging, Male, Monitoring, Physiologic, Neural Pathways, Psychomotor Performance, Reaction Time, Regression Analysis
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