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The Journal of Neuroscience, July 1, 2009, 29(26):8604-8611; doi:10.1523/JNEUROSCI.5967-08.2009

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Behavioral/Systems/Cognitive
Uncovering the Neural Signature of Lapsing Attention: Electrophysiological Signals Predict Errors up to 20 s before They Occur

Redmond G. O'Connell,^1,2 Paul M. Dockree,¹ Ian H. Robertson,¹ Mark A. Bellgrove,² John J. Foxe,^3,4 and Simon P. Kelly^3,4,5

¹School of Psychology and Trinity College Institute of Neuroscience, Trinity College Dublin, Dublin 2, Ireland, ²School of Psychology and Queensland Brain Institute, University of Queensland, Brisbane, Queensland 4067, Australia, ³The Cognitive Neurophysiology Laboratory, Nathan S. Kline Institute for Psychiatric Research, New York, New York 10962, ⁴Program in Cognitive Neuroscience, Department of Psychology, City College of the City University of New York, New York, New York 10031, and ⁵Center for Neurobiology and Behavior, Columbia University, New York, New York 10032

Correspondence should be addressed to Dr. Redmond O'Connell, Trinity College Institute of Neuroscience, Lloyd Building, Trinity College Dublin, Dublin 2, Ireland. Email: reoconne{at}tcd.ie

The extent to which changes in brain activity can foreshadow human error is uncertain yet has important theoretical and practical implications. The present study examined the temporal dynamics of electrocortical signals preceding a lapse of sustained attention. Twenty-one participants performed a continuous temporal expectancy task, which involved continuously monitoring a stream of regularly alternating patterned stimuli to detect a rarely occurring target stimulus whose duration was 40% longer. The stimulus stream flickered at a rate of 25 Hz to elicit a steady-state visual-evoked potential (SSVEP), which served as a continuous measure of basic visual processing. Increasing activity in the band (8–14 Hz) was found beginning 20 s before a missed target. This was followed by decreases in the amplitude of two event-related components over a short pretarget time frame: the frontal P3 (3–4 s) and contingent-negative variation (during the target interval). In contrast, SSVEP amplitude before hits and misses was closely matched, suggesting that the efficacy of ongoing basic visual processing was unaffected. Our results show that the specific neural signatures of attentional lapses are registered in the EEG up to 20 s before an error.

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Received Dec. 16, 2008; revised April 17, 2009; accepted May 5, 2009.

Correspondence should be addressed to Dr. Redmond O'Connell, Trinity College Institute of Neuroscience, Lloyd Building, Trinity College Dublin, Dublin 2, Ireland. Email: reoconne{at}tcd.ie

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