Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials

Brown, Matthew R.G.; Goltz, Herbert C.; Vilis, Tutis; Ford, Kristen A.; Everling, Stefan

doi:10.1016/j.neuroimage.2006.07.002

Cited by 143Neural and Behavioral Psychology StudiesMotor Control and AdaptationVisual perception and processing mechanisms

Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials

Brown, Matthew R.G., Goltz, Herbert C., Vilis, Tutis, Ford, Kristen A., Everling, Stefan·2006·NeuroImage

DOI 10.1016/j.neuroimage.2006.07.002

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Abstract

Flexible, adaptive behavior often requires the inhibition of automatic responses in favor of voluntary response generation. The antisaccade task requires active inhibition of the automatic saccade to a peripheral stimulus followed by generation of a voluntary antisaccade to the opposite location. Previous studies demonstrated greater functional magnetic resonance imaging (fMRI) activation for antisaccades than prosaccades in cortical saccade areas but did not distinguish the relative contributions of saccadic inhibition and generation. To address this question, we compared prosaccades, antisaccades, and nogo trials in a rapid event-related fMRI experiment with ten human subjects (6 female, 4 male). Trials were compound, containing a colored fixation point to cue trial type, followed by a 200-ms gap and then peripheral stimulus presentation and response. Required responses for prosaccade, antisaccade, and nogo trials, respectively, were to generate a saccade to the stimulus, look away from it, and inhibit the automatic saccade while maintaining central fixation. Frontal and supplementary eye fields, anterior cingulate cortex, intraparietal sulcus, and precuneus, exhibited surprisingly similar activation patterns for prosaccade and nogo responses, suggesting that BOLD signal in cortical saccade regions might predominantly reflect visual detection and attention processes rather than saccade generation or inhibition. These regions displayed greater activation for antisaccade responses versus prosaccade or nogo responses, possibly due to visuospatial remapping or increased attention levels in the antisaccade task. In right superior frontal sulcus, right supramarginal gyrus, and posterior cingulate sulcus, activation was greater for nogo compared to prosaccade responses, suggesting a role in active saccadic inhibition.

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Antisaccade performance is supported by a distributed circuit including frontal, supplementary, and parietal eye fields, prefrontal cortex, and subcortical structures such as striatum, thalamus, and cerebellum.
“Work in humans and non-human primates have delineated a widely-distributed circuitry that supports AS performance including the frontal, supplementary, and parietal eye fields (FEF, SEF, PEF respectively), as well as prefrontal cortex (PFC) and various subcortical structures such as striatum, thalamus, and cerebellum”
From Developmental changes in brain function underlying the influence of reward processing on inhibitory control (2011) · cites this paper as Brown et al., 2006
The brain regions that support voluntary saccadic eye movements and reward processing are well characterized.
“The brain regions supporting the generation of voluntary saccadic eye movements as well as the processing of rewards are well-delineated”
From Developmental changes in brain function underlying the influence of reward processing on inhibitory control (2011) · cites this paper as Brown et al., 2006

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Geier, C., & Luna, B. (2009) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2009.01.021 · Cited by 225 · see citing works
“…cortex, basal ganglia, superior colliculus, and thalamus, among others, as indicated by non-human primate electrophysiology (Munoz and Everling, 2004; Funahashi et al., 1993) and functional imaging work in human (Brown et al., 2006; Luna et al., 2001; Connolly et al., 2002; Ford et al., 2005).”
Background
Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders
Agam, Y., Joseph, R. M., Barton, J. J. S., & Manoach, D. S. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.04.010 · Cited by 224 · see citing works
“Like the FEF, the ACC consistently shows greater activation for antisaccades vs. prosaccades in neuroimaging studies (e.g., Brown et al 2006; Doricchi et al 1997; Ford et al 2005; Manoach et al 2007; Matsuda et al 2004; Paus et al 1993).”
Result
Enhanced visual processing contributes to matrix reasoning in autism
Soulières, I., Dawson, M., Samson, F., Barbeau, É. B., Sahyoun, C. P., Strangman, G. E., Zeffiro, T. A., & Mottron, L. (2009) · Human Brain Mapping · doi:10.1002/hbm.20831 · Cited by 216 · see citing works
“The precuneus is involved in networks responsible for maintaining and updating visuospatial information in working memory, visual detection and attention, mental rotation and visual imagery [Brown et al., 2006; Cavanna and Trimble, 2006; Hufner et al., 2008; Owen, 2004; Suchan et al., 2006; Yeh et al., 2007].”
Background
Remember the future II: Meta-analyses and functional overlap of working memory and delay discounting
Wesley, M. J., & Bickel, W. K. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.08.008 · Cited by 205 · see citing works
Developmental changes in brain function underlying the influence of reward processing on inhibitory control
Padmanabhan, A., Geier, C. F., Ordaz, S. J., Teslovich, T., & Luna, B. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.06.004 · Cited by 202 · see citing works
“…of voluntary saccadic eye movements as well as the processing of rewards are well-delineated (Apicella et al., 1991; Breiter et al., 2001; Brown et al., 2006; Delgado et al., 2000; Delgado et al., 2003; Elliott et al., 2003; Hikosaka & Watanabe, 2000; Knutson et al., 2000; Luna &…”
Influential
Neuroanatomical correlates of executive functions in children and adolescents: A magnetic resonance imaging (MRI) study of cortical thickness
Tamnes, C. K., Østby, Y., Walhovd, K. B., Westlye, L. T., Due-Tønnessen, P., & Fjell, A. M. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.04.024 · Cited by 183 · see citing works
Decomposing the Neural Correlates of Antisaccade Eye Movements Using Event-Related fMRI
Ettinger, U., Ffytche, D. H., Kumari, V., Kathmann, N., Reuter, B., Zelaya, F. O., & Williams, S. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm147 · Cited by 182 · see citing works
“(2006) concluded that the activation observed during antisaccades may thus not be uniquely attributed to simply triggering a saccade but might reflect visual attention and visuospatial remapping of the target into an oculomotor response (Brown et al. 2006).”
BackgroundResultInfluential
Neural Correlates of Impulse Control During Stop Signal Inhibition in Cocaine-Dependent Men
Li, C.-S. R., Huang, C. X., Yan, P., Bhagwagar, Z., Milivojevic, V., & Sinha, R. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301568 · Cited by 179 · see citing works
“For instance, both anti-saccade and ‘no-go’ activated these brain regions to a greater extent then pro-saccade in an oculomotor countermanding task (”
Spatial updating: how the brain keeps track of changing object locations during observer motion
Wolbers, T., Hegarty, M., Büchel, C., & Loomis, J. M. (2008) · Nature Neuroscience · doi:10.1038/nn.2189 · Cited by 174 · see citing works
“Both FEF and the posterior IPS have been associated with spatial attention, spatial working memory and spatial updating across saccadic eye movement”
Background
Frontoparietal activation with preparation for antisaccades
Brown, M. R. G., Vilis, T., & Everling, S. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00460.2007 · Cited by 145 · see citing works
“For details of the mixed-effects analysis, see APPENDIX B of Brown et al. (2006) and Worsley et al. (2002).”
MethodResultInfluentialSelf-citation
Social Norms Shift Behavioral and Neural Responses to Foods
Nook, E. C., & Zaki, J. (2015) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00795 · Cited by 145 · see citing works
The Maturation of Task Set-Related Activation Supports Late Developmental Improvements in Inhibitory Control
Velanova, K., Wheeler, M. E., & Luna, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1579-09.2009 · Cited by 129 · see citing works
“Event-related fMRI studies report that AS performance elicits activation in these brain regions (Connolly et al., 2000; Polli et al., 2005; Brown et al., 2006; Curtis and Connolly, 2008), and, in the present study, recruitment of analogous regions was readily evident across age groups (Velanova et al.”
Background
Quantitative meta-analysis of fMRI and PET studies reveals consistent activation in fronto-striatal-parietal regions and cerebellum during antisaccades and prosaccades
Jamadar, S. D., Fielding, J., & Egan, G. F. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00749 · Cited by 127 · see citing works
Test–retest reliability of fMRI activation during prosaccades and antisaccades
Raemaekers, M. A. H., Vink, M., Zandbelt, B. B., Wezel, R. J. A. V., Kahn, R. S., & Ramsey, N. F. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.061 · Cited by 126 · see citing works
“Higher field strengths may be required to detect more robust activation in both individual and group-wise results for the contrast between antisaccades and prosaccades, as is observed in other studies (Brown et al., 2006; Connolly et al., 2002; Curtis and D’Esposito, 2003; Desouza et al., 2003; Ford et al., 2005).”
Result
Saccade Preparation Signals in the Human Frontal and Parietal Cortices
Curtis, C. E., & Connolly, J. D. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00899.2007 · Cited by 117 · see citing works
“The dorsal anterior cingulate and the dorsolateral prefrontal cortex were active during this BOLD contrast, suggesting their involvement in saccade inhibition (Brown et al. 2006; Curtis et al. 2005).”
BackgroundResult
Allocentric versus Egocentric Representation of Remembered Reach Targets in Human Cortex
Chen, Y., Monaco, S., Byrne, P., Yan, X., Henriques, D. Y. P., & Crawford, J. D. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1445-14.2014 · Cited by 105 · see citing works
“2003, 2005a; b; Brown et al., 2004, 2006; Prado et al., 2005; Fernandez-Ruiz et al., 2007; Beurze et al., 2009; Cavina-Pratesi et al., 2010; Fabbri et al., 2012; Konen et al., 2013).”
An effect of context on saccade-related behavior and brain activity
Dyckman, K. A., Camchong, J., Clementz, B. A., & McDowell, J. E. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.023 · Cited by 100 · see citing works
Neural Activity Is Modulated by Trial History: A Functional Magnetic Resonance Imaging Study of the Effects of a Previous Antisaccade
Manoach, D. S., Thakkar, K. N., Cain, M. S., Polli, F. E., Edelman, J. A., Fischl, B. R., & Barton, J. J. S. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3662-06.2007 · Cited by 85 · see citing works
“The SEF also shows increased fMRI activity for antisaccade versus prosaccade trials in this and other studies (Brown et al., 2006).”
Result
Reduced microstructural integrity of the white matter underlying anterior cingulate cortex is associated with increased saccadic latency in schizophrenia
Manoach, D. S., Ketwaroo, G. A., Polli, F. E., Thakkar, K. N., Barton, J. J. S., GOFF, D. C., Fischl, B. R., Vangel, M. G., & Tuch, D. S. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.04.062 · Cited by 81 · see citing works
“The ACC shows increased activation during prosaccades compared to fixation (Brown et al., 2006), greater activation for antisaccades than prosaccades (e.g., Brown et al., 2006; Doricchi et al., 1997; Ford et al., 2005; Manoach et al., 2007; Paus et al., 1993), and reduced activity in association…”
Influential
Functional neuroimaging of acute oculomotor deficits in concussed athletes
Johnson, B. D., Zhang, K., Hallett, M., & Slobounov, S. (2014) · Brain Imaging and Behavior · doi:10.1007/s11682-014-9316-x · Cited by 78 · see citing works
Cortico‐basal ganglia mechanisms for overcoming innate, habitual and motivational behaviors
Isoda, M., & Hikosaka, O. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07698.x · Cited by 76 · see citing works
“…parietal cortex, basal ganglia and thalamus (O’Driscoll et al., 1995; Kimmig et al., 2001; Connolly et al., 2002; Curtis & D’Esposito, 2003; DeSouza et al., 2003; Matsuda et al., 2004; Ford et al., 2005; Miller et al., 2005; Polli et al., 2005; Brown et al., 2006, 2007; Cameron et al., 2009).”
Background
Impaired executive function signals in motor brain regions in Parkinson's disease
Cameron, I. G. M., Pari, G., Alahyane, N., Brien, D. C., Coe, B. C., Stroman, P. W., & Munoz, D. P. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.057 · Cited by 75 · see citing works
“3A) in order to identify regions previously shown with fMRI to display greater activation for antisaccades compared to prosaccades: DLPFC, FEF, SEF, PEF and caudate nucleus (CN) (Brown et al., 2006; Connolly et al., 2002, 2005; Curtis and D'Esposito, 2003; DeSouza et al., 2003; Luna et al., 1998; Luna et al., 1998; Sw…”
Background
Neural correlates of saccadic inhibition in healthy elderly and patients with amnestic mild cognitive impairment
Alichniewicz, K., Brunner, F., Klünemann, H. H., & Greenlee, M. W. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00467 · Cited by 73 · see citing works
“There is some inconsistency; however, whether frontal eye fields (FEF) or intraparietal sulcus (IPS) is more active during anti-saccades compared with prosaccades (Connolly et al., 2002; Cornelissen et al., 2002; Curtis et al., 2004; Brown et al., 2006; Ettinger et al., 2008).”
BackgroundResultInfluential
Probing basal ganglia functions by saccade eye movements
Watanabe, M., & Munoz, D. P. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07691.x · Cited by 73 · see citing works
“When the pro- and antisaccade paradigms are interleaved, CN activation is stronger for antisaccades than prosaccades in normal subjects (Sweeney et al., 1996; Brown et al., 2006; Dyckman et al., 2007; Ettinger et al., 2008; Cameron et al., 2009).”
BackgroundInfluential
Behavioral Evidence of Separate Adaptation Mechanisms Controlling Saccade Amplitude Lengthening and Shortening
Panouilleres, M. T. N., Weiss, T., Urquizar, C., Salemme, R., Munoz, D. P., & Pélisson, D. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90988.2008 · Cited by 72 · see citing works
Human Posterior Parietal Cortex Plans Where to Reach and What to Avoid
Lindner, A., Iyer, A., Kagan, I., & Andersen, R. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2849-09.2010 · Cited by 71 · see citing works
“Human imaging studies on the cancellation of preplanned motor responses confirm a contribution of parietal and premotor cortex to response inhibition (Garavan et al., 1999; Watanabe et al., 2002; Curtis et al., 2005; Brown et al., 2006; Cavina-Pratesi et al., 2006).”
Background
The functional anatomy of cognitive control: A domain‐general brain network for uncertainty processing
Wu, T., Chen, C., Spagna, A., Wu, X., Mackie, M., Russell‐Giller, S., Xu, P., Luo, Y., Liu, X., Hof, P. R., et al. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24804 · Cited by 70 · see citing works
Follow-up evaluation of oculomotor performance with fMRI in the subacute phase of concussion
Johnson, B. D., Hallett, M., & Slobounov, S. (2015) · Neurology · doi:10.1212/wnl.0000000000001968 · Cited by 67 · see citing works
“The higher degree of difficulty of antisaccades has been documented in the fMRI literature as evidence of hyperactivation in NV studies.(7) The presence of increased activation at 30 days postinjury in the visual cortices may point to an inefficiency, and hence increased effort, to resolve directional selectivity.”
Background
What do eye movements tell us about patients with neurological disorders? — An introduction to saccade recording in the clinical setting —
Terao, Y., FUKUDA, H., & Hikosaka, O. (2017) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.93.049 · Cited by 68 · see citing works
Understanding Effector Selectivity in Human Posterior Parietal Cortex by Combining Information Patterns and Activation Measures
Leone, F. T., Heed, T., Toni, I., & Medendorp, W. P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.5242-13.2014 · Cited by 62 · see citing works
“Alternatively, the selection process could reflect motor inhibition of the alternative effectors (Brown et al., 2006).”
Background
Antisaccade performance in patients with obsessive–compulsive disorder and unaffected relatives: further evidence for impaired response inhibition as a candidate endophenotype
Lennertz, L., Rampacher, F., Vogeley, A., Schulze-Rauschenbach, S., Pukrop, R., Ruhrmann, S., Klosterkötter, J., Maier, W., Falkai, P., & Wagner, M. (2012) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-012-0311-1 · Cited by 62 · see citing works
“Some of these regions (SMG, DLPFC) probably take a key position in inhibitory phase of antisaccade tasks [4, 15, 33].”
A Functional and Structural Investigation of the Human Fronto-Basal Volitional Saccade Network
Neggers, S. F. W., van Diepen, R. M., Zandbelt, B. B., Vink, M., Mandl, R. C. W., & Gutteling, T. P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0029517 · Cited by 59 · see citing works
BOLD fMRI activation for anti-saccades in nonhuman primates
Ford, K. A., Gati, J. S., Menon, R. S., & Everling, S. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.12.009 · Cited by 61 · see citing works
“…with pro-saccade trials (Everling and Munoz, 2000) while BOLD fMRI in humans has shown increased activation in the FEF for anti-saccade trials (Brown et al., 2006, 2007; Connolly et al., 2000, 2002, 2005; Curtis and D'Esposito, 2003; Desouza et al., 2003; Ford et al., 2005; Kimmig et al.,…”
BackgroundMethodResultSelf-citation
Age related prefrontal compensatory mechanisms for inhibitory control in the antisaccade task
Fernández-Ruíz, J., Peltsch, A. J., Alahyane, N., Brien, D. C., Coe, B. C., Garcia, A. A., & Munoz, D. P. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.10.001 · Cited by 56 · see citing works
“…on previous functional imaging studies that showed consistent activation in these areas during prosaccade and antisaccade execution and preparation (Brown et al., 2006; Cameron et al., 2012; Connolly et al., 2005; DeSouza et al., 2003; Ford et al., 2006; Hakvoort Schwerdtfeger et al., 2013;…”
Cognitive Deterioration and Functional Compensation in ALS Measured with fMRI Using an Inhibitory Task
Witiuk, K., Fernández-Ruíz, J., McKee, R., Alahyane, N., Coe, B. C., Melanson, M., & Munoz, D. P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1111-14.2014 · Cited by 56 · see citing works
“…in these areas during prosaccade and antisaccade execution and preparation (Luna et al., 1998; DeSouza et al., 2003; Connolly et al., 2005; Ford et al., 2005; Brown et al., 2006, 2007; Raemaekers et al., 2007; Cameron et al., 2012; Hakvoort Schwerdtfeger et al., 2012; Jamadar et al., 2013).”
BackgroundResultInfluential
Preparatory neural networks are impaired in adults with attention-deficit/hyperactivity disorder during the antisaccade task
Schwerdtfeger, R. M. H., Alahyane, N., Brien, D. C., Coe, B. C., Stroman, P. W., & Munoz, D. P. (2012) · NeuroImage Clinical · doi:10.1016/j.nicl.2012.10.006 · Cited by 53 · see citing works
“…findings in the ACC, an area that has been shown consistently to be involved in monitoring antisaccade performance (Polli et al., 2005) and signaling the likelihood and actual occurrence of antisaccade errors (Nieuwenhuis et al., 2001; Ford et al., 2005; Brown et al., 2006; Endrass et al., 2007).”
Background
Females are more vulnerable to Internet gaming disorder than males: Evidence from cortical thickness abnormalities
Wang, Z., Hu, Y., Zheng, H., Yuan, K., Du, X., & Dong, G. (2018) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2018.11.001 · Cited by 49 · see citing works
Different involvement of subregions within dorsal premotor and medial frontal cortex for pro- and antisaccades
Cieslik, E. C., Seidler, I., Laird, A. R., Fox, P. T., & Eickhoff, S. B. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.012 · Cited by 46 · see citing works
Executive Functions Brain System: An Activation Likelihood Estimation Meta-analytic Study
Ardila, A., Bernal, B., & Rosselli, M. (2018) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acx066 · Cited by 46 · see citing works
Cortical thickness and volume abnormalities in Internet gaming disorder: Evidence from comparison of recreational Internet game users
Wang, Z., Wu, L., Yuan, K., Hu, Y., Zheng, H., Du, X., & Dong, G. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13987 · Cited by 46 · see citing works
Neuronavigated Repetitive Transcranial Ultrasound Stimulation Induces Long-Lasting and Reversible Effects on Oculomotor Performance in Non-human Primates
Pouget, P., Frey, S., Ahnine, H., Attali, D., Claron, J., Constans, C., Aubry, J., & Arcizet, F. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.01042 · Cited by 45 · see citing works
Human intraparietal sulcus (IPS) and competition between exogenous and endogenous saccade plans
Anderson, E. J., Masud Husain, B., & Sumner, P. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.10.046 · Cited by 45 · see citing works
“FEF and SEF activity has also been found during antisaccade performance (e.g. Brown et al., 2006; O'Driscoll et al., 1995; Sweeney et al., 1996), and antisaccade deficits have been reported for patients with lesions to these areas (Guitton et al., 1985; Machado and Rafal, 2004a; Parton et al.,…”
Influential
Developmental Changes in Brain Function Underlying Inhibitory Control in Autism Spectrum Disorders
Padmanabhan, A., Garver, K. E., O’Hearn, K. M., Nawarawong, N. N., Liu, R., Minshew, N. J., Sweeney, J. A., & Luna, B. (2014) · Autism Research · doi:10.1002/aur.1398 · Cited by 45 · see citing works
Isolation of saccade inhibition processes: Rapid event-related fMRI of saccades and nogo trials
Brown, M., Vilis, T., & Everling, S. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.09.035 · Cited by 42 · see citing works
“For details of how the mixed effects analysis works, see Appendix B of Brown et al. (2006) and Worsley et al. (2002).”
BackgroundMethodResultInfluentialSelf-citation
Path dependence in risky choice: Affective and deliberative processes in brain and behavior
Hytönen, K., Baltussen, G., van den Assem, M. J., Klucharev, V. A., Sanfey, A. G., & Smidts, A. (2014) · Journal of Economic Behavior & Organization · doi:10.1016/j.jebo.2014.01.016 · Cited by 40 · see citing works
“3 Typically, interstimulus intervals are longer than the intervals that we employed here, although similarly short intervals have been used previously n event-related fMRI experiments (e.g., Brown et al., 2006; Rubia et al., 2005).”
The functional oculomotor network and saccadic cognitive control in healthy elders
Pa, J., Dutt, S., Mirsky, J. B., Heuer, H. W., Keselman, P., Kong, E. L., Trujillo, A. J., Gazzaley, A. H., Kramer, J. H., Seeley, W. W., et al. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.03.051 · Cited by 41 · see citing works
“The right DLPFC and ACC, in addition to other regions, are commonly implicated in performing the AS task (Brown et al., 2006; Ettinger et al., 2008).”
Background
Sensorimotor‐independent prefrontal activity during response inhibition
Cai, W., Cannistraci, C. J., Gore, J. C., & Leung, H. (2013) · Human Brain Mapping · doi:10.1002/hbm.22315 · Cited by 39 · see citing works
“It is relatively well understood that the FEF is involved in both execution and inhibition of saccadic eye movements [Brown et al., 2006, 2008; Cornelissen et al., 2002; Curtis et al., 2005; Ettinger et al., 2008; Heinen, et al., 2006].”
Background
A meta‐analysis of functional magnetic resonance imaging studies of eye movements and visual word reading
Zhou, W., & Hua Shu, A. (2017) · Brain and Behavior · doi:10.1002/brb3.683 · Cited by 38 · see citing works
Activation of the posterior cingulate by semantic priming: A co-registered ERP/fMRI study
O’Hare, A. J., Dien, J., Waterson, L. D., & Savage, C. R. (2007) · Brain Research · doi:10.1016/j.brainres.2007.10.095 · Cited by 37 · see citing works
A drama movie activates brains of holistic and analytical thinkers differentially
Bacha‐Trams, M., Alexandrov, Y. I., Broman, E., Glerean, E., Kauppila, M., Kauttonen, J., Ryyppö, E., Sams, M. E., & Jääskeläinen, I. P. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy099 · Cited by 37 · see citing works
Dorsolateral prefrontal cortex hyperactivity during inhibitory control in children with ADHD in the antisaccade task
Fernández-Ruíz, J., Schwerdtfeger, R. M. H., Alahyane, N., Brien, D. C., Coe, B. C., & Munoz, D. P. (2019) · Brain Imaging and Behavior · doi:10.1007/s11682-019-00196-3 · Cited by 38 · see citing works
Effects of acute alcohol intoxication on saccadic conflict and error processing
Marinković, K., Rickenbacher, E., Azma, S., Artsy, E., & Lee, A. K. C. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3173-y · Cited by 34 · see citing works
Saccadic Eye Movements in Anorexia Nervosa
Phillipou, A., Rossell, S. L., Gurvich, C., Hughes, M. E., Castle, D. J., Nibbs, R. G., & Abel, L. A. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152338 · Cited by 32 · see citing works
“[23]: antisaccade cue> no-go cue, antisaccade cue> prosaccade cue, prosaccade cue> no-go cue, antisaccade response> no-go response, antisaccade response> prosaccade response, and prosaccade response> no-go response.”
Method
Distributed representations of the "preparatory set" in the frontal oculomotor system: a TMS study
Nagel, M., Sprenger, A., Lencer, R., Kömpf, D., Siebner, H. R., & Heide, W. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-89 · Cited by 29 · see citing works
Vector inversion diminishes the online control of antisaccades
Heath, M. D., Weiler, J., Marriott, K., & Welsh, T. N. (2011) · Experimental Brain Research · doi:10.1007/s00221-010-2525-7 · Cited by 28 · see citing works
“Concerning prosaccades, Brown et al. (2006) report that prosaccades and their no-go counterparts exhibit comparable activity in cortical saccade regions (e.g., frontal eye Welds, intraparietal sulcus) and suggest that such a result reXects the importance of high-level saccade networks for discriminating task-speciWc v…”
Background
Role of the basal ganglia in switching a planned response
Cameron, I. G. M., Coe, B. C., Watanabe, M., Stroman, P. W., & Munoz, D. P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06776.x · Cited by 28 · see citing works
“…previous imaging studies have shown greater activation in the FEF for antisaccades relative to prosaccades (O’Driscoll et al., 1995; Sweeney et al., 1996; Curtis & D’Esposito, 2003; DeSouza et al., 2003; Connolly et al., 2005; Ford et al., 2005; Miller et al., 2005; Brown et al., 2006, 2007).”
Background
Functional magnetic resonance imaging of sensorimotor transformations in saccades and antisaccades
Herweg, N. A., Weber, B., Kasparbauer, A., Meyhöfer, I., Steffens, M., Smyrnis, N., & Ettinger, U. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.08.033 · Cited by 26 · see citing works
“This finding is generally consistentwith previous PET and fMRI studies (Brown et al., 2006; DeSouza et al., 2003; Ettinger et al., 2008; Ford et al., 2005; O'Driscoll et al., 1995; Sweeney et al., 1996).”
BackgroundResult
Neural correlates of individual differences in fixation duration during natural reading
Henderson, J. M., Choi, W., Luke, S. G., & Schmidt, J. (2017) · Quarterly Journal of Experimental Psychology · doi:10.1080/17470218.2017.1329322 · Cited by 26 · see citing works
Saccades: Fundamentals and Neural Mechanisms
Pierce, J. E., Clementz, B. A., & McDowell, J. E. (2019) · Studies in neuroscience, psychology and behavioral economics · doi:10.1007/978-3-030-20085-5_2 · Cited by 25 · see citing works
Behavioral and Neural Plasticity of Ocular Motor Control: Changes in Performance and fMRI Activity Following Antisaccade Training
Jamadar, S. D., Johnson, B. P., Clough, M., Egan, G. F., & Fielding, J. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00653 · Cited by 25 · see citing works
“…is involved in the top-down biasing of the oculomotor system in the service of task goals (PierrotDeseilligny et al., 2003, 2004; Ford et al., 2005; Brown et al., 2006; Ettinger et al., 2008; Hwang et al., 2010) and the anterior cingulate is involved in signaling the requirement for increased…”
Background
Power spectrum scale invariance as a neural marker of cocaine misuse and altered cognitive control
Ide, J. S., Hu, S., Zhang, S., Mujica-Parodi, L. R., & Li, C.-S. R. (2016) · NeuroImage Clinical · doi:10.1016/j.nicl.2016.03.004 · Cited by 24 · see citing works
“respond to inhibition of saccadic eye movements in an oculomotor go/ nogo task (Brown et al., 2006; Brown et al., 2008; Ettinger et al., 2008).”
Background
Neural correlates of active vision: An fMRI comparison of natural reading and scene viewing
Choi, W., & Henderson, J. M. (2015) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2015.05.027 · Cited by 24 · see citing works
“Alternatively, some studies using pro- and anti- saccade tasks have observed that right IFG and/or MFG are activated during those tasks, suggesting that these regions are associated with inhibition of responses such as reflexive eye movements during the anti-saccade task (Aichert et al., 2012; Brown et al., 2006; for…”
BackgroundResult
Distinct Neural Correlates for Volitional Generation and Inhibition of Saccades
Reuter, B., Kaufmann, C., Bender, J., Pinkpank, T., & Kathmann, N. (2009) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2009.21235 · Cited by 23 · see citing works
Saccades to a Remembered Location Elicit Spatially Specific Activation in Human Retinotopic Visual Cortex
Geng, J. J., Ruff, C. C., & Driver, J. (2008) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2008.21025 · Cited by 22 · see citing works
“For completeness, we also implemented the reverse contrast (of no-go minus go trials), since saccade inhibition or cancellation on the no-go trials might arguably involve some additional neural processes (e.g. Pare and Hanes, 2003;Brown et al., 2006;Brown et al., 2008).”
Method
Neurobehavioral maturation of motor response inhibition in adolescence – A narrative review
Weiss, H., & Luciana, M. M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104646 · Cited by 23 · see citing works
Effects of Anterior Cingulate Microstimulation on Pro- and Antisaccades in Nonhuman Primates
Phillips, J. M., Johnston, K., & Everling, S. (2010) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21482 · Cited by 20 · see citing works
Self-citation
Repetition Suppression Dissociates Spatial Frames of Reference in Human Saccade Generation
van Pelt, S., Toni, I., Diedrichsen, J., & Medendorp, W. P. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00393.2010 · Cited by 20 · see citing works
“Fitting this design matrix to the resampled data automatically deconvolves the time series of each RS condition (Brown et al. 2006), without making any assumption about the shape of the activation profile, other than its length (15 s in this case).”
Method
Conflict Resolution as Near-Threshold Decision-Making: A Spiking Neural Circuit Model with Two-Stage Competition for Antisaccadic Task
Lo, C., & Wang, X. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1005081 · Cited by 20 · see citing works
Longitudinal multi-modal neuroimaging in opsoclonus–myoclonus syndrome
Oh, S., Boegle, R., zu Eulenburg, P., Ertl, M., Kim, J., & Dieterich, M. (2017) · Journal of Neurology · doi:10.1007/s00415-016-8389-4 · Cited by 21 · see citing works
Differences in MEG gamma oscillatory power during performance of a prosaccade task in adolescents with FASD
Stephen, J. M., Coffman, B. A., Stone, D. B., & Kodituwakku, P. W. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00900 · Cited by 20 · see citing works
“The cortical network includes primary visual cortex, parietal eye fields, putatively located in medial intraparietal sulcus in humans, and supplementary and frontal eye fields (SEF and FEF; Clementz et al., 2001; Brown et al., 2006; Manoach et al., 2007; McDowell et al., 2008).”
Background
Modulation of cognitive control levels via manipulation of saccade trial-type probability assessed with event-related BOLD fMRI
Pierce, J. E., & McDowell, J. E. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00776.2015 · Cited by 20 · see citing works
“…underlying typical saccade production has been thoroughly described in humans using the blood oxygenation level-dependent (BOLD) signal in functional magnetic resonance imaging (fMRI; e.g., Brown et al. 2006; Curtis and Connolly 2008; Dyckman et al. 2007; Matsuda et al. 2004; Reuter et al. 2010).”
Method
Functional connectivity of the Precuneus reflects effectiveness of visual restitution training in chronic hemianopia
Halbertsma, H. N., Elshout, J. A., Bergsma, D. P., Norris, D. G., Cornelissen, F. W., van den Berg, A. V., & Haak, K. V. (2020) · NeuroImage Clinical · doi:10.1016/j.nicl.2020.102292 · Cited by 19 · see citing works
“cue are suppressed and directed towards the mirrored cue location in the opposite hemifield (Brown et al., 2006; Brown et al., 2007; Dyckman et al., 2007; Kimmig et al., 2001).”
Background
Cortical Dynamics during the Preparation of Antisaccadic and Prosaccadic Eye Movements in Humans in a Gap Paradigm
Cordones, I., Gómez, C. M., & Escudero, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063751 · Cited by 19 · see citing works
Differential roles of the frontal and parietal cortices in the control of saccades
Bender, J., Tark, K., Reuter, B., Kathmann, N., & Curtis, C. E. (2013) · Brain and Cognition · doi:10.1016/j.bandc.2013.06.005 · Cited by 18 · see citing works
Neural correlates of proactive and reactive inhibition of saccadic eye movements
Talanow, T., Kasparbauer, A., Lippold, J. V., Weber, B., & Ettinger, U. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9972-3 · Cited by 17 · see citing works
Latent state–trait and latent growth curve modeling of inhibitory control.
Faßbender, K., Meyhöfer, I., & Ettinger, U. (2023) · Journal of Experimental Psychology General · doi:10.1037/xge0001344 · Cited by 16 · see citing works
Investigating inhibitory control in children with epilepsy: An fMRI study
Triplett, R. L., Velanova, K., Luna, B., Padmanabhan, A., Gaillard, W. D., & Asato, M. R. (2014) · Epilepsia · doi:10.1111/epi.12768 · Cited by 17 · see citing works
Having to identify a target reduces latencies in prosaccades but not in antisaccades
Guyader, N., Malsert, J., & Marendaz, C. (2008) · Psychological Research · doi:10.1007/s00426-008-0218-7 · Cited by 17 · see citing works
Stimulus Salience Conflicts and Colludes with Endogenous Goals During Urgent Choices
Oor, E. E., Stanford, T. R., & Salinas, E. (2022) · iScience · doi:10.1016/j.isci.2023.106253 · Cited by 15 · see citing works
The Frontal Eye Field Is Involved in Visual Vector Inversion in Humans – A Theta Burst Stimulation Study
Jaun-Frutiger, K., Cazzoli, D., Müri, R. M., Bassetti, C. L., & Nyffeler, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083297 · Cited by 14 · see citing works
“Other studies using fMRI showed a higher activity during antisaccade tasks than during prosaccade tasks, not only in the PPC, but also in the FEF [11–12].”
Method
Facing competition: Neural mechanisms underlying parallel programming of antisaccades and prosaccades
Talanow, T., Kasparbauer, A., Steffens, M., Meyhöfer, I., Weber, B., Smyrnis, N., & Ettinger, U. (2016) · Brain and Cognition · doi:10.1016/j.bandc.2016.05.006 · Cited by 14 · see citing works
“The interaction also revealed a cluster in the left PCG, close to but inferior (z = 36, MNI) to previously reported FEF coordinates (zP 39, Talairach) (Brown et al., 2006; Desmurget et al., 2000; O’Driscoll et al., 2000).”
BackgroundResult
Functional subdivisions within the human intraparietal sulcus are involved in visuospatial transformation in a non‐context‐dependent manner
Papadopoulos, A., Sforazzini, F., Egan, G. F., & Jamadar, S. D. (2017) · Human Brain Mapping · doi:10.1002/hbm.23847 · Cited by 14 · see citing works
“In the antisaccade task, the IPS is thought to be involved in the process of vector inversion [Brown et al., 2006; Medendorp et al., 2005] that spatially transforms the target for the saccade from the visually presented stimulus location to the mirror opposite location [Domagalik et al., 2012;…”
Background
Spontaneous eye movements during eyes-open rest reduce resting-state-network modularity by increasing visual-sensorimotor connectivity
Koba, C., Notaro, G., Tamm, S., Nilsonne, G., & Hasson, U. (2021) · Network Neuroscience · doi:10.1162/netn_a_00186 · Cited by 14 · see citing works
Neural competition through visual similarity in face selection
Gentile, F., & Jansma, B. M. (2010) · Brain Research · doi:10.1016/j.brainres.2010.06.050 · Cited by 14 · see citing works
“In a slightly different view Brown et al. (2006) proposed that both the insula and IFG are needed to keep attention captured while inhibiting any shift of attention towards the distracting location.”
Cognitive control of saccadic selection and inhibition from within the core cortical saccadic network
Jarvstad, A., & Gilchrist, I. D. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1419-18.2018 · Cited by 14 · see citing works
“The overall very low error rate ( 2.6%, compare 10% in Brown et al., 2006) is also consistent with the paradigm being less demanding than other tasks.”
BackgroundResultInfluential
Different cortical activations during visuospatial attention and the intention to perform a saccade
Konen, C. S., Kleiser, R., Bremmer, F., & Seitz, R. J. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-0995-z · Cited by 14 · see citing works
“However, an event-related fMRI study suggested that the stronger activation during anti-saccades might also reXect visuospatial remapping or increased attention levels (Brown et al. 2006).”
Background
Response Suppression Delays the Planning of Subsequent Stimulus-Driven Saccades
Weiler, J., Mitchell, T., & Heath, M. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086408 · Cited by 13 · see citing works
Parieto-Occipital Cortex Shows Early Target Selection to Faces in a Reflexive Orienting Task
Morand, S. M., Harvey, M., & Grosbras, M. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhs368 · Cited by 13 · see citing works
“…fields (FEFs) and intraparietal sulcus (IPS) are more selectively involved in the preparation and generation of voluntary antisaccades (Pierrot-Deseilligny et al. 2002; Connolly et al. 2002; Cornelissen et al. 2002; DeSouza et al. 2003; Ploner et al. 2005; Brown et al. 2006; Ettinger et al. 2008).”
Background
Neural correlates of impaired volitional action control in schizophrenia patients
Bender, J., Reuter, B., Möllers, D., Kaufmann, C., Gallinat, J., & Kathmann, N. (2013) · Psychophysiology · doi:10.1111/psyp.12060 · Cited by 12 · see citing works
Medio-Frontal and Anterior Temporal abnormalities in children with attention deficit hyperactivity disorder (ADHD) during an acoustic antisaccade task as revealed by electro-cortical source reconstruction
Goepel, J., Kissler, J. M., Rockstroh, B. S., & Paul-Jordanov, I. (2011) · BMC Psychiatry · doi:10.1186/1471-244x-11-7 · Cited by 11 · see citing works
The effect of electromagnetic field emitted by a mobile phone on the inhibitory control of saccades
Okano, T., Terao, Y., Furubayashi, T., Yugeta, A., Hanajima, R., & Ugawa, Y. (2010) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.12.006 · Cited by 12 · see citing works
Cortical control of saccades in Parkinson disease and essential tremor
Yerram, S., Glazman, S., & Bodis-Wollner, I. G. (2012) · Journal of Neural Transmission · doi:10.1007/s00702-012-0870-3 · Cited by 12 · see citing works

Muscle biopsy, macro EMG and clinical characteristics in patients with schizophrenia
Flyckt, L., Borg, J., Borg, K., Ansved, T., Edman, G., Bjerkenstedt, L., & Wiesel, F.-A. (2000) · Schizophrenia Research · doi:10.1016/s0920-9964(00)90681-9 · Cited by 3 · see citing works
Isolation of saccade inhibition processes: Rapid event-related fMRI of saccades and nogo trials
Brown, M., Vilis, T., & Everling, S. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.09.035 · Cited by 42 · see citing works
Self-citation
fMRI Investigations of Flexible Behavioural Control Based on Eye Movement Models
Brown, M. R. G. (2007) · Scholarship@Western (Western University)
Self-citation
fMRI Investigations of Flexible Behavioural Control Based on Eye
Robert, M., & Brown, G. (2008)
Cerebral Cortex doi:10.1093/cercor/bhm147 Decomposing the Neural Correlates of Antisaccade Eye Movements Using Event-Related fMRI
Ettinger, U., Ffytche, D. H., Kumari, V., Kathmann, N., Reuter, B., Zelaya, O., & Williams, S. (2016)

Authors: Brown, M. R. G., Goltz, H. C., Vilis, T., Ford, K. A., & Everling, S.
Affiliations: Western University (CA)
Corresponding author: Brown, Matthew R.G.
ORCID: Brown, Matthew R.G.
Goltz, Herbert C.
Everling, Stefan
Venue: NeuroImage
Publisher: Elsevier BV
Published: 2006-11
Volume: 33
Issue: 2
Pages: 644-659
ISSN: 1053-8119 (ISSN-L)
DOI: 10.1016/j.neuroimage.2006.07.002
OpenAlex: W1990113525
Cited by: 143
References: 78
Citations by year: 2026: 4 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 5 · 2021: 3 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 7 · 2016: 9 · 2015: 8 · 2014: 13 · 2013: 11 · 2012: 8
FWCI: 5.48
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: NeuroImage (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords: saccades, antisaccade task, prosaccades, saccadic inhibition, oculomotor control, supplementary eye field, anterior cingulate cortex, intraparietal sulcus, precuneus, superior frontal sulcus, supramarginal gyrus, posterior cingulate cortex, attention, BOLD signal
MeSH terms: Adult, Brain Mapping, Evoked Potentials, Female, Humans, Kinetics, Magnetic Resonance Imaging, Male, Photic Stimulation, Reaction Time, Reference Values, Saccades

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Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials

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