Abstract
We investigated how moment-to-moment fluctuations in fMRI amplitude and interregional coupling are linked to behavioral performance during a stop signal task. To quantify the relationship between single-trial amplitude and behavior on a trial-by-trial basis, we modeled the probability of successful inhibition as a function of response amplitude via logistic regression analysis. At the group level, significant logistic slopes were observed in, among other regions, the inferior frontal gyrus (IFG), caudate, and putamen, all bilaterally. Furthermore, we investigated how trial-by-trial fluctuations in responses in attentional regions covaried with fluctuations in inhibition-related regions. The coupling between several frontoparietal attentional regions and the right IFG increased during successful versus unsuccessful performance, suggesting that efficacious network interactions are important in determining behavioral outcome during the stop signal task. In particular, the link between responses in the right IFG and behavior were moderated by moment-to-moment fluctuations in evoked responses in the left intraparietal sulcus. A supplemental figure for this article may be downloaded from http:// cabn.psychonomic-journals.org/content/supplemental.
References
Aron, A. R., Durston, S., Eagle, D. W., Logan, G. D., Stinear, C. M., & Stuphorn, V. (2007). Converging evidence for a frontobasal-ganglia network for inhibitory control of action and cognition. Journal of Neuroscience, 27, 11860–11864.
Aron, A. R., Fletcher, P. C., Bullmore, E. T., Sahakian, B. J., & Robbins, T. W. (2003). Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nature Neuroscience, 6, 115–116.
Aron, A. R., & Poldrack, R. A. (2006). Cortical and subcortical contributions to stop signal response inhibition: Role of the subthalamic nucleus. Journal of Neuroscience, 26, 2424–2433.
Boehler, C. N., Münte, T. F., Krebs, R. M., Heinze, H.-J., Schoenfeld, M. A., & Hopf, J.-M. (2009). Sensory MEG responses predict successful and failed inhibition in a stop-signal task. Cerebral Cortex, 19, 134–145.
Booth, J. R., Burman, D. D., Meyer, J. R., Lei, Z., Trommer, B. L., Davenport, N. D., et al. (2005). Larger deficits in brain networks for response inhibition than for visual selective attention in attention deficit hyperactivity disorder (ADHD). Journal of Child Psychology & Psychiatry, 46, 94–111.
Boucher, L., Palmeri, T. J., Logan, G. D., & Schall, J. D. (2007). Inhibitory control in mind and brain: An interactive race model of countermanding saccades. Psychological Review, 114, 376–397.
Brass, M., Derrfuss, J., Forstmann, B., & von Cramon, D. Y. (2005). The role of the inferior frontal junction area in cognitive control. Trends in Cognitive Sciences, 9, 314–316.
Brass, M., Wenke, D., Spengler, S., & Waszak, F. (2009). Neural correlates of overcoming interference from instructed and implemented stimulus-response associations. Journal of Neuroscience, 29, 1766–1772.
Britten, K. H., Newsome, W. T., Shadlen, M. N., Celebrini, S., & Movshon, J. A. (1996). A relationship between behavioral choice and the visual responses of neurons in macaque MT. Visual Neuroscience, 13, 87–100.
Brown, J. W., & Braver, T. S. (2005). Learned predictions of error likelihood in the anterior cingulate cortex. Science, 307, 1118–1121.
Casey, B. J., Trainor, R. J., Orendi, J. L., Schubert, A. B., Nystrom, L. E., Giedd, J. N., et al. (1997). A developmental functional MRI study of prefrontal activation during performance of a go-no-go task. Journal of Cognitive Neuroscience, 9, 835–847.
Chamberlain, S. R., Hampshire, A., Müller, U., Rubia, K., Del Campo, N., Craig, K., et al. (2009). Atomoxetine modulates right inferior frontal activation during inhibitory control: A pharmacological functional magnetic resonance imaging study. Biological Psychiatry, 65, 550–555.
Chambers, C. D., Bellgrove, M. A., Gould, I. C., English, T., Garavan, H., McNaught, E., et al. (2007). Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. Journal of Neurophysiology, 98, 3638–3647.
Chambers, C. D., Bellgrove, M. A., Stokes, M. G., Henderson, T. R., Garavan, H., Robertson, I. H., et al. (2006). Executive “brake failure” following deactivation of human frontal lobe. Journal of Cognitive Neuroscience, 18, 444–455.
Chambers, C. D., Garavan, H., & Bellgrove, M. A. (2009). Insights into the neural basis of response inhibition from cognitive and clinical neuroscience. Neuroscience & Biobehavioral Reviews, 33, 631–646.
Chen, C.-Y., Muggleton, N. G., Tzeng, O. J. L., Hung, D. L., & Juan, C.-H. (2009). Control of prepotent responses by the superior medial frontal cortex. NeuroImage, 44, 537–545.
Chikazoe, J., Jimura, K., Asari, T., Yamashita, K., Morimoto, H., Hirose, S., et al. (2009). Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cerebral Cortex, 19, 146–152.
Cohen, M. S. (1997). Parametric analysis of fMRI data using linear systems methods. NeuroImage, 6, 93–103.
Colzato, L. S., van den Wildenberg, W. P., & Hommel, B. (2007). Impaired inhibitory control in recreational cocaine users. PLoS ONE, 2, e1143.
Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215.
Cox, R. W. (1996). AFNI: Software for the analysis and visualization of functional magnetic resonance neuroimages. Computers & Biomedical Research, 29, 162–173.
Dehaene, S., Posner, M. I., & Tucker, D. M. (1994). Localization of a neural system for error detection and compensation. Psychological Science, 5, 303–305.
Duann, J.-R., Ide, J. S., Luo, X., & Li, C.-S. R. (2009). Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. Journal of Neuroscience, 29, 10171–10179.
Eagle, D. M., Baunez, C., Hutcheson, D. M., Lehmann, O., Shah, A. P., & Robbins, T. W. (2008). Stop-signal reaction-time task performance: Role of prefrontal cortex and subthalamic nucleus. Cerebral Cortex, 18, 178–188.
Eagle, D. M., & Robbins, T. W. (2003). Inhibitory control in rats performing a stop-signal reaction-time task: Effects of lesions of the medial striatum and d-amphetamine. Behavioral Neuroscience, 117, 1302–1317.
Eimer, M. (1993). Effects of attention and stimulus probability on ERPs in a Go/Nogo task. Biological Psychology, 35, 123–138.
Floden, D., & Stuss, D. T. (2006). Inhibitory control is slowed in patients with right superior medial frontal damage. Journal of Cognitive Neuroscience, 18, 1843–1849.
Forstmann, B. U., Jahfari, S., Scholte, H. S., Wolfensteller, U., van den Wildenberg, W. P. M., & Ridderinkhof, K. R. (2008). Function and structure of the right inferior frontal cortex predict individual differences in response inhibition: A model-based approach. Journal of Neuroscience, 28, 9790–9796.
Garavan, H., Ross, T. J., Kaufman, J., & Stein, E. A. (2003). A midline dissociation between error-processing and response-conflict monitoring. NeuroImage, 20, 1132–1139.
Garavan, H., Ross, T. J., Murphy, K., Roche, R. A. P., & Stein, E. A. (2002). Dissociable executive functions in the dynamic control of behavior: Inhibition, error detection, and correction. NeuroImage, 17, 1820–1829.
Garavan, H., Ross, T. J., & Stein, E. A. (1999). Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proceedings of the National Academy of Sciences, 96, 8301–8306.
Gehring, W., Goss, B., Coles, M., Meyer, D., & Donchin, E. (1993). A neural system for error detection and compensation. Psychological Science, 4, 385–390.
Gelman, A., & Hill, J. (2007). Data analysis using regression and multilevel/hierarchical models. Cambridge: Cambridge University Press.
Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage, 15, 870–878.
Hester, R., Fassbender, C., & Garavan, H. (2004). Individual differences in error processing: A review and reanalysis of three eventrelated fMRI studies using the GO/NOGO task. Cerebral Cortex, 14, 986–994.
Hester, R., Madeley, J., Murphy, K., & Mattingley, J. B. (2009). Learning from errors: Error-related neural activity predicts improvements in future inhibitory control performance. Journal of Neuroscience, 29, 7158–7165.
Hosmer, D. W., & Lemeshow, S. (2000). Applied logistic regression (2nd ed.). New York: Wiley.
Kalaska, J. F., & Crammond, D. J. (1995). Deciding not to GO: Neuronal correlates of response selection in a GO/NOGO task in primate premotor and parietal cortex. Cerebral Cortex, 5, 410–428.
Kastner, S., & Ungerleider, L. G. (2001). The neural basis of biased competition in human visual cortex. Neuropsychologia, 39, 1263–1276.
Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., & Baker, C. I. (2009). Circular analysis in systems neuroscience: The dangers of double dipping. Nature Neuroscience, 12, 535–540.
Leber, A. B., Turk-Browne, N. B., & Chun, M. M. (2008). Neural predictors of moment-to-moment fluctuations in cognitive flexibility. Proceedings of the National Academy of Sciences, 105, 13592–13597.
Leung, H.-C., & Cai, W. (2007). Common and differential ventrolateral prefrontal activity during inhibition of hand and eye movements. Journal of Neuroscience, 27, 9893–9900.
Li, C.-S. R., Huang, C., Constable, R. T., & Sinha, R. (2006). Imaging response inhibition in a stop-signal task: Neural correlates independent of signal monitoring and post-response processing. Journal of Neuroscience, 26, 186–192.
Li, C.-S. R., Yan, P., Chao, H. H., Sinha, R., Paliwal, P., Constable, R. T., et al. (2008). Error-specific medial cortical and subcortical activity during the stop signal task: A functional magnetic resonance imaging study. Neuroscience, 155, 1142–1151.
Li, C.-S. R., Yan, P., Sinha, R., & Lee, T.-W. (2008). Subcortical processes of motor response inhibition during a stop signal task. NeuroImage, 41, 1352–1363.
Liddle, P. F., Kiehl, K. A., & Smith, A. M. (2001). Event-related fMRI study of response inhibition. Human Brain Mapping, 12, 100–109.
Lim, S. L., Padmala, S., & Pessoa, L. (2009). Segregating the significant from the mundane on a moment-to-moment basis via direct and indirect amygdala contributions. Proceedings of the National Academy of Sciences, 106, 16841–16846.
Loftus, G. R., & Masson, M. E. (1994). Using confidence intervals in within-subject designs. Psychonomic Bulletin & Review, 1, 476–490.
Logan, G. D. (1994). On the ability to inhibit thought and action: A user’s guide to the stop signal paradigm. In D. Dagenbach & T. H. Carr (Eds.), Inhibitory processes in attention, memory, and language (pp. 189–239). San Diego: Academic Press.
Logan, G. D., & Cowan, W. B. (1984). On the ability to inhibit thought and action: A theory of an act of control. Psychological Review, 91, 295–327.
Logan, G. D., Schachar, R. J., & Tannock, R. (1997). Impulsivity and inhibitory control. Psychological Science, 8, 60–64.
Maddock, R. J. (1999). The retrosplenial cortex and emotion: New insights from functional neuroimaging of the human brain. Trends in Neurosciences, 22, 310–316.
Magno, E., Foxe, J. J., Molholm, S., Robertson, I. H., & Garavan, H. (2006). The anterior cingulate and error avoidance. Journal of Neuroscience, 26, 4769–4773.
Menon, V., Adleman, N. E., White, C. D., Glover, G. H., & Reiss, A. L. (2001). Error-related brain activation during a go/nogo response inhibition task. Human Brain Mapping, 12, 131–143.
Nachev, P., Wydell, H., O’Neill, K., Husain, M., & Kennard, C. (2007). The role of the pre-supplementary motor area in the control of action. NeuroImage, 36(Suppl. 2), T155-T163.
Padmala, S., & Pessoa, L. (2008). Affective learning enhances visual detection and responses in primary visual cortex. Journal of Neuroscience, 28, 6202–6210.
Padmala, S., & Pessoa, L. (2010). Interactions between cognition and motivation during response inhibition. Neuropsychologia, 48, 558–565.
Pessoa, L., Gutierrez, E., Bandettini, P. B., & Ungerleider, L. G. (2002). Neural correlates of visual working memory: fMRI amplitude predicts task performance. Neuron, 35, 975–987.
Pessoa, L., & Padmala, S. (2005). Quantitative prediction of perceptual decisions during near-threshold fear detection. Proceedings of the National Academy of Sciences, 102, 5612–5617.
Pessoa, L., & Ungerleider, L. G. (2004). Top-down mechanisms for working memory and attentional processes. In M. S. Gazzaniga (Ed.), The new cognitive neurosciences (3rd ed., pp. 919–930). Cambridge, MA: MIT Press.
Picton, T. W., Stuss, D. T., Alexander, M. P., Shallice, T., Binns, M. A., & Gillingham, S. (2007). Effects of focal frontal lesions on response inhibition. Cerebral Cortex, 17, 826–838.
Preuschoff, K., Quartz, S. R., & Bossaerts, P. (2008). Human insula activation reflects risk prediction errors as well as risk. Journal of Neuroscience, 28, 2745–2752.
Purushothaman, G., & Bradley, D. C. (2005). Neural population code for fine perceptual decisions in area MT. Nature Neuroscience, 8, 99–106.
Ramautar, J. R., Slagter, H. A., Kok, A., & Ridderinkhof, K. R. (2006). Probability effects in the stop-signal paradigm: The insula and the significance of failed inhibition. Brain Research, 1105, 143–154.
Ratcliffe, S. J., & Shults, J. (2008). GEEQBOX: A MATLAB toolbox for generalized estimating equations and quasi-least squares. Journal of Statistical Software, 25, 1–14.
Ray, N. J., Jenkinson, N., Brittain, J., Holland, P., Joint, C., Nandi, D., et al. (2009). The role of the subthalamic nucleus in response inhibition: Evidence from deep brain stimulation for Parkinson’s disease. Neuropsychologia, 47, 2828–2834.
Ress, D., Backus, B. T., & Heeger, D. J. (2000). Activity in primary visual cortex predicts performance in a visual detection task. Nature Neuroscience, 3, 940–945.
Rubia, K., Smith, A. B., Brammer, M. J., & Taylor, E. (2003). Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. NeuroImage, 20, 351–358.
Rubia, K., Smith, A. B., Taylor, E., & Brammer, M. (2007). Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes. Human Brain Mapping, 28, 1163–1177.
Swick, D., Ashley, V., & Turken, A. U. (2008). Left inferior frontal gyrus is critical for response inhibition. BMC Neuroscience, 9, 102.
Sylvester, C. M., Shulman, G. L., Jack, A. I., & Corbetta, M. (2007). Asymmetry of anticipatory activity in visual cortex predicts the locus of attention and perception. Journal of Neuroscience, 27, 14424–14433.
Talairach, J., & Tournoux, P. (1988). A co-planar stereotaxic atlas of the human brain. New York: Thieme.
van den Wildenberg, W. P., van Boxtel, G. J., van der Molen, M. W., Bosch, D. A., Speelman, J. D., & Brunia, C. H. (2006). Stimulation of the subthalamic region facilitates the selection and inhibition of motor responses in Parkinson’s disease. Journal of Cognitive Neuroscience, 18, 626–636.
Verbruggen, F., & Logan, G. D. (2008). Response inhibition in the stop-signal paradigm. Trends in Cognitive Sciences, 12, 418–424.
Vink, M., Kahn, R. S., Raemaekers, M., van den Heuvel, M., Boersma, M., & Ramsey, N. F. (2005). Function of striatum beyond inhibition and execution of motor responses. Human Brain Mapping, 25, 336–344.
Williams, B., Ponesse, J., Schachar, R., Logan, G., & Tannock, R. (1999). Development of inhibitory control across the life span. Developmental Psychology, 35, 205–213.
Xue, G., Aron, A. R., & Poldrack, R. A. (2008). Common neural substrates for inhibition of spoken and manual responses. Cerebral Cortex, 18, 1923–1932.
Zeger, S. L., & Liang, K. Y. (1986). Longitudinal data analysis for discrete and continuous outcomes. Biometrics, 42, 121–130.
Zhou, D., Thompson, W. K., & Siegle, G. (2009). MATLAB toolbox for functional connectivity. NeuroImage, 47, 1590–1607.
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Support for this work was provided in part by the National Institute of Mental Health (Grant R01 MH071589) and the Indiana METACyt Initiative of Indiana University, funded in part through a major grant from the Lilly Endowment, Inc.
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Padmala, S., Pessoa, L. Moment-to-moment fluctuations in fMRI amplitude and interregion coupling are predictive of inhibitory performance. Cognitive, Affective, & Behavioral Neuroscience 10, 279–297 (2010). https://doi.org/10.3758/CABN.10.2.279
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DOI: https://doi.org/10.3758/CABN.10.2.279
Keywords
- Response Inhibition
- Inferior Frontal Gyrus
- Stop Signal Task
- Stop Trial
- Successful Inhibition