Distractor P3 is associated with attentional capture by stimulus deviance

OBJECTIVE A simple distractor elicits a large P3 when the standard and target are difficult to discriminate in the three-stimulus oddball paradigm. This study investigated whether the distractor P3 reflects attentional capture by stimulus deviance or cognitive interference with maintaining the standard representation. METHODS Event-related brain potentials were recorded from 12 participants who performed a visual three-stimulus oddball paradigm. Four task conditions were defined by a combination of two presentation types of distractor stimuli (central or bilateral) and two levels of standard/target discrimination difficulty (easy or difficult). Bilateral distractors had stimulus deviance but did not interfere with maintenance of the standard representation. RESULTS Central distractors elicited a P3, the amplitude of which was larger in the difficult task than in the easy task. In contrast, bilateral distractors elicited a large P3 in both the easy and difficult tasks. CONCLUSIONS Distractor P3 reflects attentional capture by stimulus deviance, rather than cognitive interference with maintaining the standard representation. SIGNIFICANCE This is the first report showing that simple distractors can elicit large anteriorly distributed P3 in an easy task. The present findings contribute to the clinical application of distractor P3 to assess the cognitive function of deviant processing.

[1]  S. Yantis,et al.  Abrupt visual onsets and selective attention: Evidence from visual search. , 1984 .

[2]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[3]  R. Knight.  Contribution of human hippocampal region to novelty detection , 1996, Nature.

[4]  Risa Sawaki,et al.  Severity of AD/HD symptoms and efficiency of attentional resource allocation , 2006, Neuroscience Letters.

[5]  E. Donchin,et al.  A componential analysis of the ERP elicited by novel events using a dense electrode array. , 1999, Psychophysiology.

[6]  A. Kok.  On the utility of P3 amplitude as a measure of processing capacity. , 2001, Psychophysiology.

[7]  Brian A. Lopez,et al.  P3a from visual stimuli: task difficulty effects. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  S. Kobayashi,et al.  Event-related brain potentials in response to novel sounds in dementia , 2000, Clinical Neurophysiology.

[9]  J. Polich,et al.  P3a and P3b Auditory ERPs in HIV Patients Receiving Anti-Viral Medication , 2002, Clinical EEG.

[10]  S. Luck,et al.  Spatio‐temporal dynamics of attention to color: Evidence from human electrophysiology , 1998, Human brain mapping.

[11]  E. N. Sokolov,et al.  Perception and the Conditioned Reflex , 1965 .

[12]  J. Polich,et al.  P300 from one-, two-, and three-stimulus auditory paradigms. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[13]  E. Donchin,et al.  Spatiotemporal analysis of the late ERP responses to deviant stimuli. , 2001, Psychophysiology.

[14]  J. Polich,et al.  P3a, perceptual distinctiveness, and stimulus modality. , 1998, Brain research. Cognitive brain research.

[15]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[16]  E Courchesne,et al.  Effects of rare non-target stimuli on brain electrophysiological activity and performance. , 1990, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[17]  J. Polich,et al.  Attention, probability, and task demands as determinants of P300 latency from auditory stimuli. , 1986, Electroencephalography and clinical neurophysiology.

[18]  J. Polich.  Detection of change : event-related potential and fMRI findings , 2003 .

[19]  S. Yantis,et al.  Visual attention: control, representation, and time course. , 1997, Annual review of psychology.

[20]  John Polich,et al.  P3a from auditory white noise stimuli , 2006, Clinical Neurophysiology.

[21]  Jun'ichi Katayama,et al.  Difficulty of discrimination modulates attentional capture for deviant information. , 2007, Psychophysiology.

[22]  R. Verleger.  On the utility of P3 latency as an index of mental chronometry. , 1997, Psychophysiology.

[23]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[24]  Risa Sawaki,et al.  Stimulus context determines whether non-target stimuli are processed as task-relevant or distractor information , 2006, Clinical Neurophysiology.

[25]  J. Theeuwes.  Stimulus-driven capture and attentional set: selective search for color and visual abrupt onsets. , 1994, Journal of experimental psychology. Human perception and performance.

[26]  Motohiro Kimura,et al.  Positive difference in ERPs reflects independent processing of visual changes. , 2005, Psychophysiology.

[27]  István Czigler,et al.  Memory-based detection of task-irrelevant visual changes. , 2002, Psychophysiology.

[28]  Dominique Lamy,et al.  Attentional capture in singleton-detection and feature-search modes. , 2003, Journal of experimental psychology. Human perception and performance.

[29]  J. Theeuwes.  Cross-dimensional perceptual selectivity , 1991, Perception & psychophysics.

[30]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[31]  J. Ford,et al.  Age-related changes in auditory event-related potentials. , 1980, Electroencephalography and clinical neurophysiology.

[32]  J. C. Johnston,et al.  Involuntary covert orienting is contingent on attentional control settings. , 1992, Journal of experimental psychology. Human perception and performance.

[33]  T W Picton,et al.  The P300 Wave of the Human Event‐Related Potential , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[34]  Nilli Lavie,et al.  Temporal attentional capture: Effects of irrelevant singletons on rapid serial visual search , 2006, Psychonomic bulletin & review.

[35]  J. Polich,et al.  P3a and P3b from typical auditory and visual stimuli , 1999, Clinical Neurophysiology.

[36]  Leslie G. Ungerleider,et al.  Mechanisms of visual attention in the human cortex. , 2000, Annual review of neuroscience.

[37]  C. Pernet,et al.  Lateral masking, levels of processing and stimulus category: A comparative study between normal and dyslexic readers , 2006, Neuropsychologia.

[38]  J. Polich,et al.  P300, probability, and the three-tone paradigm. , 1996, Electroencephalography and clinical neurophysiology.

[39]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[40]  E. Donchin,et al.  Parsing the late positive complex: mental chronometry and the ERP components that inhabit the neighborhood of the P300. , 2004, Psychophysiology.

[41]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[42]  J. Polich,et al.  Auditory and visual P300 topography from a 3 stimulus paradigm , 1999, Clinical Neurophysiology.

[43]  R. Näätänen.  Attention and brain function , 1992 .

[44]  J. Polich,et al.  Stimulus context determines P3a and P3b. , 1998, Psychophysiology.

[45]  J. Polich,et al.  Neuropsychology and neuropharmacology of P3a and P3b. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[46]  J. Nigg,et al.  An integrative theory of attention-deficit/ hyperactivity disorder based on the cognitive and affective neurosciences , 2005, Development and Psychopathology.

[47]  E. Courchesne,et al.  Stimulus novelty, task relevance and the visual evoked potential in man. , 1975, Electroencephalography and clinical neurophysiology.

[48]  R. J. Doherty,et al.  Separation of the components of the late positive complex in an ERP dishabituation paradigm , 2005, Clinical Neurophysiology.

[49]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[50]  R. Simons,et al.  On the relationship of P3a and the Novelty-P3 , 2001, Biological Psychology.

[51]  R. Näätänen,et al.  Electrophysiological evidence of enhanced distractibility in ADHD children , 2005, Neuroscience Letters.

[52]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[53]  E. Donchin.  Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

[54]  S. Yantis,et al.  Stimulus-driven attentional capture: evidence from equiluminant visual objects. , 1994, Journal of experimental psychology. Human perception and performance.

[55]  Ahmet Ademoglu,et al.  Wavelet Analysis of P3a and P3b , 2004, Brain Topography.

[56]  J-M Hopf,et al.  Dynamics of feature binding during object-selective attention , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[57]  K. R. Ridderinkhof,et al.  The Role of the Medial Frontal Cortex in Cognitive Control , 2004, Science.

[58]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[59]  H. Egeth,et al.  Overriding stimulus-driven attentional capture , 1994, Perception & psychophysics.

[60]  D. Friedman,et al.  A developmental study of the effect of temporal order on the ERPs elicited by novel environmental sounds. , 1997, Electroencephalography and clinical neurophysiology.

[61]  E. Donchin,et al.  The influence of stimulus deviance and novelty on the P300 and novelty P3. , 2002, Psychophysiology.

[62]  J. Polich,et al.  P3a from Visual Stimuli: Typicality, Task, and Topography , 2004, Brain Topography.

[63]  John Polich,et al.  P3a from a passive visual stimulus task , 2001, Clinical Neurophysiology.

[64]  D. C. Howell.  Statistical Methods for Psychology , 1987 .