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Cited by 1,394Neural and Behavioral Psychology StudiesHemispheric Asymmetry in NeuroscienceNeurobiology of Language and Bilingualism

Right hemispheric dominance of inhibitory control: An event-related functional MRI study

Open access
Garavan, H., Ross, T. J., Stein, E. A.·1999·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.96.14.8301PMC PMC22229
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Abstract

Normal human behavior and cognition are reliant on a person’s ability to inhibit inappropriate thoughts, impulses, and actions. The temporal and spatial advantages of event-related functional MRI (fMRI) were exploited to identify cortical regions that showed a transient change in fMRI signal after the withholding of a prepotent motor response. The temporal specificity of the event-related fMRI design also minimized possible contamination from response inhibition errors (i. e., commission errors) and other extraneous processes. Regions identified were strongly lateralized to the right hemisphere and included the middle and inferior frontal gyri, frontal limbic area, anterior insula, and inferior parietal lobe. Contrary to the prominence traditionally given to ventral frontal regions for response inhibition, the results suggest that response inhibition is accomplished by a distributed cortical network.

AI snapshot

Written from the paper’s full text.

TL;DR

Event-related fMRI during withholding of a prepotent motor response identified a distributed, predominantly right-lateralized cortical network for response inhibition, including middle and inferior frontal gyri, frontal limbic area, anterior insula, and inferior parietal lobe. The authors conclude that response inhibition is not confined to ventral frontal regions but depends on a distributed network.

Key findings

  • Correct response inhibitions activated predominantly right-hemisphere regions: right middle frontal gyrus (Brodmann area 9; clusters of 783, 109, and 100 mm³), right inferior frontal gyrus (BA 10; 102 mm³), right insula (504 mm³), bilateral frontal limbic area (BA 32; 554 mm³), right inferior parietal lobe (BA 40; 116 and 399 mm³), and others listed in Table 1.
  • Behavioral performance was good: mean commission errors = 1.9 (SD = 1.0; range 0–3), mean omission errors = 1.4 (SD = 2.5; range 0–9), and mean target response time = 460 msec (SD = 46).
  • Faster target responses correlated with greater inhibition-related signal in right inferior frontal gyrus (r = −0.63, P = 0.02) and left inferior parietal lobule (r = −0.67, P = 0.009).
  • Response execution activated an anticipated motor circuit (left primary motor, SMA, striatal, cerebellar regions) with little overlap with inhibition activations; all lure-activation clusters showed significantly greater activation for lures than targets (P values from 2.0 × 10⁻⁴ to 6.0 × 10⁻¹¹).

Methods

  • Fourteen right-handed subjects (6 female; mean age 31 ± 8; range 19–44) performed an event-related fMRI task with serial letters every 500 msec; subjects responded to alternating X/Y targets and inhibited responses to nonresponse targets (lures), with 150 targets and 25 lures across four runs.
  • fMRI data were acquired on a 1.5T scanner with 7-mm sagittal slices (TE = 40 msec; TR = 2,000 msec; FOV = 24 cm; 64 × 64 matrix; 3.75 × 3.75 mm in-plane resolution).
  • Analyses used AFNI 2.2, motion correction, time-locking to lures, gamma-variate modeling, percentage area-under-the-curve maps, Talairach transformation, one-sample t tests, and a cluster-size threshold of 100 μl; the false-positive threshold was t = 4.9 (P = 4.0 × 10⁻⁵). Target-response analyses used signal deconvolution.

Limitations

  • The paper states that magnetic susceptibility artifact diminished functional signal in orbitofrontal regions and in more anterior and medial ventral brain areas, probably reducing sensitivity to detect functional changes there.
  • The paper describes some functional interpretations as speculative, including the proposed role of the insula and the decomposition of response inhibition into subprocesses.
  • Evident from the text: the sample was small (14 subjects), all right-handed, and the correlation analyses between response times and cluster signal intensity were correlational rather than causal; the task also included a working-memory component that the authors discuss as a possible confound or overlapping mechanism.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1073/pnas.96.14.8301

Cites

40 of 40 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 27 cited sources checked · 0 supported · 0 flagged

  • Findingown data
    § RESULTS

    Activation associated with response inhibition was predominantly right-lateralized.

    “A number of discrete areas of activation, predominantly right-lateralized, were observed to underlie response inhibition.”
    • Also stated in: § Abstract · boosted
      “Regions identified were strongly lateralized to the right hemisphere and included the middle and inferior frontal gyri, frontal limbic area, anterior insula, and inferior parietal lobe.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS

    All lure activation clusters showed significantly greater activation in response to lures than in response to targets.

    “All clusters showed significantly greater activation in response to the lures than in response to the targets (P values ranged from 2.0 × 10−4 to 6.0 × 10−11), further suggesting the specificity of the regions activated during response inhibition.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS

    Of the 14 clusters, the right inferior frontal gyrus and left inferior parietal lobule showed significant correlations between mean target response times and mean cluster signal intensity.

    “Of the 14 clusters, 2, located on the right inferior frontal gyrus [r = −0.63, P = 0.02] and in the left inferior parietal lobule [r = −0.67, P = 0.009], showed significant correlations.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS

    Activation associated with response inhibition was observed in a distributed network including middle and inferior frontal gyri, frontal limbic area, anterior insula, inferior parietal lobe, angular gyrus, and fusiform gyri.

    “Activation was most pronounced in frontal and parietal regions, specifically on the middle and inferior frontal gyri and in the inferior parietal lobule and angular gyrus. The insula, frontal limbic area, and fusiform gyri were also activated.”
    • Also stated in: § Abstract · plain
      “Regions identified were strongly lateralized to the right hemisphere and included the middle and inferior frontal gyri, frontal limbic area, anterior insula, and inferior parietal lobe.”
    Quote in the paperSubstantial claim
  • Findingown data
    § RESULTS

    Activation for response execution did not include the regions identified with lure activations.

    “Critically, activation did not include those regions identified with the lure activations (see Fig. 5).”
    Quote in the paperSubstantial claim
  • May combine two claims. 5
  • Classified as probably not a substantial claim. 10

  • May combine two claims.

    Findingown data
    § DISCUSSION

    All medial wall activation during response inhibition was rostral to the anterior commissure, whereas almost all medial wall activation during response execution was caudal to the anterior commissure.

    “All of the medial wall activation during response inhibition was rostral to the anterior commissure, whereas almost all medial wall activation during response execution was caudal to the anterior commissure”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning
    § Abstract

    The event-related fMRI design allows response inhibitions to be distributed throughout the testing session rather than grouped together as in a block design.

    “The ER–fMRI design allows response inhibitions to be distributed throughout the testing session rather than grouped together, as in a block design.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § DISCUSSION

    Animal lesion research has implicated ventral prefrontal regions in response inhibition.

    “Animal lesion research has implicated ventral prefrontal regions in response inhibition (16, 17).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [16] Butters N, Butter C, Rosen J, Stein Exp Neurol. 1973;39:204–214. doi: 10.1016/0014-4886(73)90223-9. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [17] Iversen S D, Mishkin M. Exp Brain Res. 1970;11:376–386. doi: 10.1007/BF00237911. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given
    § RESULTS

    No errors of commission were due to the subject missing the previous target.

    “No errors of commission were due to the subject missing the previous target (in which case, the subsequent lure would be considered a valid target by the subject).”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data
    § RESULTS

    Subjects made few omission errors (mean = 1.4; SD = 2.5; range = 0-9).

    “few omission errors (mean = 1.4; SD = 2.5; range = 0–9)”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Premisecitation
    § Abstract

    Animal lesion literature typically ascribes response inhibition to predominantly ventral frontal regions.

    “This widespread activation is somewhat at odds with the animal lesion literature, which typically ascribes response inhibition to predominantly ventral frontal regions (16, 17).”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [16] Butters N, Butter C, Rosen J, Stein Exp Neurol. 1973;39:204–214. doi: 10.1016/0014-4886(73)90223-9. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [17] Iversen S D, Mishkin M. Exp Brain Res. 1970;11:376–386. doi: 10.1007/BF00237911. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data
    § Abstract

    Response inhibition is accomplished by a distributed cortical network, contrary to the prominence traditionally given to ventral frontal regions.

    “Contrary to the prominence traditionally given to ventral frontal regions for response inhibition, the results suggest that response inhibition is accomplished by a distributed cortical network.”
    • Also stated in: § DISCUSSION · plain
      “As listed in Table 1, activation associated with response inhibition was observed in a distributed network of brain regions.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Study design and conductcitation
    § Abstract

    Including commission errors in a block design adds unwanted variance to the response inhibition condition and unknown post-error processes.

    “Including these errors in a block design adds both unwanted variance to the response inhibition condition and unknown post-error processes, as subjects are typically aware when they have committed errors.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Vaidya C J, Austin G, Kirkorian G, Ridlehuber H W, Desmond J E, Glover G H, Gabrieli J D E. Proc Nat Acad Sci USA. 1998;95:14494–14499. doi: 10.1073/pnas.95.24.14494. [DOI] [PMC free article] [PubMed] [Google Scholar] source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data
    § RESULTS

    Subjects made few commission errors (mean = 1.9; SD = 1.0; range = 0-3).

    “making few commission errors (mean = 1.9; SD = 1.0; range = 0–3)”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Abstract

    Activation in ventral prefrontal regions separates subjects with high false-alarm rates from those with low false-alarm rates on a discrimination task.

    “Activation in ventral prefrontal regions has also been shown to separate subjects with high false-alarm rates from those with low false-alarm rates on a discrimination task (8).”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [8] Casey B J, Trainor R, Orendi J, Schubert A. Soc Neurosci Abstr. 1996;22:1107. [Google Scholar]

      Not checked in the free run.

  • May combine two claims.

    Study design and conductown data
    § DISCUSSION

    Magnetic susceptibility artifact can diminish functional signal in orbitofrontal regions and did so in the more anterior and medial ventral brain areas in the present study, probably reducing sensitivity to detect changes in functional signal in these areas.

    “On a cautionary note, magnetic susceptibility artifact can diminish functional signal in orbitofrontal regions and did so in the more anterior and medial ventral brain areas in the present study. This loss of signal probably reduced the sensitivity to detect changes in functional signal in these areas.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § DISCUSSION

    Dorsolateral prefrontal regions have frequently been implicated to be essential for working memory processes.

    “Dorsolateral prefrontal regions have frequently been implicated to be essential for working memory processes (42, 43).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [42] D’Esposito M, Aguirre G K, Zarahn E, Ballard D, Shin R K, Lease J. Cogn Brain Res. 1998;7:1–13. doi: 10.1016/s0926-6410(98)00004-4. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

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      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Abstract

    Response-inhibition deficits have been implicated in attention deficit hyperactivity disorder, Tourette's syndrome, obsessive-compulsive disorders, and assorted disinhibition syndromes.

    “Response-inhibition deficits have been implicated in such clinical syndromes as attention deficit hyperactivity disorder (1), Tourette’s syndrome (2), obsessive-compulsive disorders (3), and assorted “disinhibition syndromes” (4).”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [1] Barkley R A. Psychol Bull. 1997;121:65–94. doi: 10.1037/0033-2909.121.1.65. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

    • cites [2] Peterson B S, Skudlarski P, Anderson A W, Zhang H, Gatenby J C, Lacadie C M, Leckman J F, Gore J C. Arch Gen Psychiatry. 1998;55:326–333. doi: 10.1001/archpsyc.55.4.326. [DOI] [PubMed] [Google Scholar] source

      Not checked in the free run.

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      Not checked in the free run.

  • May combine two claims.

    Interpretationcitation
    § DISCUSSION

    We identified the pre-SMA as critical for response inhibition and the SMA proper for response execution.

    “Consistent with the conclusions of Humberstone et al. (9), we have identified the pre-SMA as critical for response inhibition and SMA proper for response execution.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [9] Humberstone M, Sawle G V, Clare S, Hykin J, Coxon R, Bowtell R, Macdonald I A, Morris P G. Ann Neurol. 1997;42:632–637. doi: 10.1002/ana.410420414. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation
    § Abstract

    The distributed network thought to underlie response inhibition includes the supplementary motor area, dorsal and ventral frontal regions, anterior cingulate, and occipital and parietal lobes.

    “The distributed network thought to underlie response inhibition, as observed with neuroimaging studies, includes the supplementary motor area (SMA) (9–11), dorsal and ventral frontal regions (7, 10–13), anterior cingulate (8, 11, 14, 15), and the occipital and parietal lobes (9, 14, 16).”
    Quote in the paperNot a substantial claim0 of 5 sources checked
    • cites [9] Humberstone M, Sawle G V, Clare S, Hykin J, Coxon R, Bowtell R, Macdonald I A, Morris P G. Ann Neurol. 1997;42:632–637. doi: 10.1002/ana.410420414. [DOI] [PubMed] [Google Scholar]

      Not checked in the free run.

    • cites [10] Kawashima R, Satoh K, Itoh H, Ono S, Furumoto S, Gotoh R, Koyama M, Yoshioka S, Takahashi T, Takahashi K, et al. Brain Res. 1996;728:79–89. [PubMed] [Google Scholar]

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      Not checked in the free run.

    • cites [7] Casey B J, Forman S D, Kye C, Badgaivan R D, Franzen P L, King S W, Schubert A B, Braver T S, Noll D C. Soc Neurosci Abstr. 1997;23:1119. [Google Scholar]

      Not checked in the free run.

    • cites [8] Casey B J, Trainor R, Orendi J, Schubert A. Soc Neurosci Abstr. 1996;22:1107. [Google Scholar]

      Not checked in the free run.

15 of 15

  • The paper relies on this without support.

    Inhibitory control is a fundamental executive function essential for normal thinking and successful living.

    “The ability to suppress irrelevant or interfering stimuli or impulses is a fundamental executive function essential for normal thinking processes and, ultimately, for successful living.”
1 of 1

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Cites

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Research works printed but not linked: 9

  1. B J Casey, S D Forman, C Kye, R D Badgaivan, P L Franzen, S W King, A B Schubert, T S Braver, D C Noll Soc Neurosci Abstr 23, 1119 (1997).
  2. B J Casey, R Trainor, J Orendi, A Schubert Soc Neurosci Abstr 22, 1107 (1996).
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Cited by

Sorted by citations

Authors
Garavan, H., Ross, T. J., & Stein, E. A.
Affiliations
Medical College of Wisconsin (US)
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
1999-07-06
Volume
96
Issue
14
Pages
8301-8306
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.96.14.8301
PMC
PMC22229
OpenAlex
W2124945869
Semantic Scholar
d2f65e67e49a88a3b9f689c7c688a90788b8f547
Cited by
1,394
References
40
Citations by year
2026: 14 · 2025: 24 · 2024: 26 · 2023: 29 · 2022: 39 · 2021: 52 · 2020: 36 · 2019: 53 · 2018: 59 · 2017: 49 · 2016: 40 · 2015: 66 · 2014: 64 · 2013: 77 · 2012: 72
FWCI
13.90
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institute on Drug Abuse (R01DA009465, DA 09465, DA10214, R01DA010214)
  • National Center for Research Resources (RR00058, M01RR000058)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neurobiology of Language and Bilingualism
Keywords
response inhibition, inhibitory control, right hemisphere dominance, hemispheric lateralization, frontal cortex, inferior frontal gyrus, anterior insula, inferior parietal lobule, distributed cortical networks, event-related fMRI
MeSH terms
Adult, Brain, Brain Mapping, Dominance, Cerebral, Female, Humans, Inhibition, Psychological, Magnetic Resonance Imaging, Male, Regression Analysis, Prefrontal Cortex

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