Abstract
Momentary lapses in attention frequently impair goal-directed behavior, sometimes with serious consequences. Nevertheless, we lack an integrated view of the brain mechanisms underlying such lapses. By investigating trial-by-trial relationships between brain activity and response time in humans, we determined that attentional lapses begin with reduced prestimulus activity in anterior cingulate and right prefrontal regions involved in controlling attention. Less efficient stimulus processing during attentional lapses was also characterized by less deactivation of a 'default-mode' network, reduced stimulus-evoked sensory activity, and increased activity in widespread regions of frontal and parietal cortex. Finally, consistent with a mechanism for recovering from attentional lapses, increased stimulus-evoked activity in the right inferior frontal gyrus and the right temporal-parietal junction predicted better performance on the next trial. Our findings provide a new, system-wide understanding of the patterns of brain activity that are associated with brief attentional lapses, which informs both theoretical and clinical models of goal-directed behavior.
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References
Czeisler, C.A. et al. Modafinil for excessive sleepiness associated with shift-work sleep disorder. N. Engl. J. Med. 353, 476–486 (2005).
Castellanos, F.X. et al. Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biol. Psychiatry 57, 1416–1423 (2005).
Schacter, D.L. The Seven Sins of Memory: How the Mind Forgets and Remembers (Houghton-Mifflin, New York, 2001).
Beede, K.E. & Kass, S.J. Engrossed in conversation: the impact of cell phones on simulated driving performance. Accid. Anal. Prev. 38, 415–421 (2006).
Reimer, B. et al. Behavior differences in drivers with attention deficit hyperactivity disorder: the driving behavior questionnaire. Accid. Anal. Prev. 37, 996–1004 (2005).
Desimone, R. Visual attention mediated by biased competition in extrastriate visual cortex. Phil. Trans. R. Soc. Lond. B. 353, 1245–1255 (1998).
Hopfinger, J.B., Buonocore, M.H. & Mangun, G.R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 3, 284–291 (2000).
Kastner, S., De Weerd, P., Desimone, R. & Ungerleider, L.G. Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI. Science 282, 108–111 (1998).
Woldorff, M.G. et al. Functional parcellation of attentional control regions of the brain. J. Cogn. Neurosci. 16, 149–165 (2004).
Corbetta, M., Miezin, F.M., Dobmeyer, S., Shulman, G.L. & Petersen, S.E. Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J. Neurosci. 11, 2383–2402 (1991).
Woldorff, M.G. et al. Modulation of early sensory processing in human auditory cortex during auditory selective attention. Proc. Natl. Acad. Sci. USA 90, 8722–8726 (1993).
Raichle, M.E. et al. A default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 676–682 (2001).
Carter, C.S. et al. Parsing executive processes: strategic vs. evaluative functions of the anterior cingulate cortex. Proc. Natl. Acad. Sci. USA 97, 1944–1948 (2000).
Banich, M.T. et al. fMRI studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. J. Cogn. Neurosci. 12, 988–1000 (2000).
Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).
MacDonald, A.W., Cohen, J.D., Stenger, V.A. & Carter, C.S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 288, 1835–1838 (2000).
Weissman, D.H., Warner, L.M. & Woldorff, M.G. The neural mechanisms for minimizing cross-modal distraction. J. Neurosci. 24, 10941–10949 (2004).
Corbetta, M. & Shulman, G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).
Kimchi, R. Primacy of wholistic processing and global/local paradigm: a critical review. Psychol. Bull. 112, 24–38 (1992).
Navon, D. Forest before trees: the precedence of global features in visual perception. Cognit. Psychol. 9, 353–383 (1977).
Weissman, D.H. & Banich, M.T. Global-local interference modulated by communication between the hemispheres. J. Exp. Psychol. Gen. 128, 283–308 (1999).
Dockree, P.M. et al. Sustained attention in traumatic brain injury (tbi) and healthy controls: enhanced sensitivity with dual-task load. Exp. Brain Res. 168, 218–229 (2006).
Miezin, F.M., Maccotta, L., Ollinger, J.M., Petersen, S.E. & Buckner, R.L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 11, 735–759 (2000).
Kerns, J.G. et al. Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026 (2004).
Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).
Petrides, M. Functional organization of the human frontal cortex for mnemonic processing. Ann. NY Acad. Sci. 769, 85–96 (1995).
Boynton, G.M., Engel, S.A., Glover, G.H. & Heeger, D.J. Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 16, 4207–4221 (1996).
Greicius, M.D., Srivastava, G., Reiss, A.L. & Menon, V. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI. Proc. Natl. Acad. Sci. USA 101, 4637–4642 (2004).
McKiernan, K.A., Kaufman, J.N., Kucera-Thompson, J. & Binder, J.R. A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. J. Cogn. Neurosci. 15, 394–408 (2003).
Lavie, N. & de Fockert, J.W. Contrasting effects of sensory limits and capacity limits in visual selective attention. Percept. Psychophys. 65, 202–212 (2003).
Corbetta, M., Kincade, J.M., Ollinger, J.M., McAvoy, M.P. & Shulman, G.L. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat. Neurosci. 3, 292–297 (2000).
Indovina, I. & Macaluso, E. Occipital-parietal interactions during shifts of exogenous visuospatial attention: trial-dependent changes of effective connectivity. Magn. Reson. Imaging 22, 1477–1486 (2004).
Rueckert, L. & Grafman, J. Sustained attention deficits in patients with right frontal lesions. Neuropsychologia 34, 953–963 (1996).
Wilkins, A.J., Shallice, T. & McCarthy, R. Frontal lesions and sustained attention. Neuropsychologia 25, 359–365 (1987).
Drummond, S.P. et al. The neural basis of the psychomotor vigilance task. Sleep 28, 1059–1068 (2005).
Lawrence, N.S., Ross, T.J., Hoffman, R., Garavan, H. & Stein, E.A. Multiple neuronal networks mediate spatial attention. J. Cogn. Neurosci. 15, 1028–1038 (2003).
Polli, F.E. et al. Rostral and dorsal anterior cingulate cortex make dissociable contributions during antisaccade error commission. Proc. Natl. Acad. Sci. USA 102, 15700–15705 (2005).
Fox, M.D. et al. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. USA 102, 9673–9678 (2005).
Womelsdorf, T., Fries, P., Mitra, P.P. & Desimone, R. Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439, 733–736 (2006).
Cabeza, R., Anderson, N.D., Locantore, J.K. & McIntosh, A.R. Aging gracefully: compensatory brain activity in high-performing older adults. Neuroimage 17, 1394–1402 (2002).
Klingberg, T., O'Sullivan, B.T. & Roland, P.E. Bilateral activation of fronto-parietal networks by incrementing demand in a working memory task. Cereb. Cortex 7, 465–471 (1997).
Weissman, D.H., Gopalakrishnan, A., Hazlett, C.J. & Woldorff, M.G. Dorsal anterior cingulate cortex resolves conflict from distracting stimuli by boosting attention toward relevant events. Cereb. Cortex 15, 229–237 (2005).
Aron, A.R. & Poldrack, R.A. The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biol. Psychiatry 57, 1285–1292 (2005).
Buckner, R.L. et al. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 20, 285–296 (1998).
Montague, P.R., Hyman, S.E. & Cohen, J.D. Computational roles for dopamine in behavioural control. Nature 431, 760–767 (2004).
Woldorff, M.G. Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. Psychophysiology 30, 98–119 (1993).
Ollinger, J.M., Corbetta, M. & Shulman, G.L. Separating processes within a trial in event-related functional MRI. Neuroimage 13, 218–229 (2001b).
Friston, K.J. et al. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189–210 (1995).
Friston, K.J., Price, C.J., Buchel, C. & Frackowiak, R.S.J. A taxonomy of study design. in Human Brain Function (eds. Frackowiak, R.S.J., Friston, K.J., Frith, C.D., Dolan, R.J. & Mazziotta, J.C.) Ch. 8, 141–159 (Academic Press, San Diego, 1997).
Talairach, J. & Tournoux, P. Co-planar Stereotactic Atlas of the Human Brain (Thieme, New York, 1988).
Acknowledgements
This research was supported by a postdoctoral National Research Service Award to D.H.W. (1 F32 NS41867-01) and by US National Institute of Health grants to M.G.W. (MH60415 and P01 NS41328, Project 2).
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Weissman, D., Roberts, K., Visscher, K. et al. The neural bases of momentary lapses in attention. Nat Neurosci 9, 971–978 (2006). https://doi.org/10.1038/nn1727
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DOI: https://doi.org/10.1038/nn1727
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