Microsaccadic inhibition and P300 enhancement in a visual oddball task.

It has recently been demonstrated that the presentation of visual oddballs induces a prolonged inhibition of microsaccades. The amplitude of the P300 component in event-related potentials (ERPs) has been shown to be sensitive to the category (target vs. nontarget) of the eliciting stimulus, its overall probability, and the preceding stimulus sequence. In the present study we further specify the functional underpinnings of the prolonged microsaccadic inhibition in the visual oddball task, showing that the stimulus category, the frequency of a stimulus, and the preceding stimulus sequence influence microsaccade rate. Furthermore, by co-recording ERPs and eye movements, we were able to demonstrate that, despite being largely sensitive to the same experimental manipulation, the amplitude of P300 and the microsaccadic inhibition predict each other only weakly.

[1]  Salil H. Patel,et al.  Impact of instructed relevance on the visual ERP. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[2]  Ralf Engbert,et al.  Microsaccade Orientation Supports Attentional Enhancement Opposite a Peripheral Cue: Commentary on Tse, Sheinberg, and Logothetis (2003) , 2004, Psychological science.

[3]  M. Scherg,et al.  Localizing P300 Generators in Visual Target and Distractor Processing: A Combined Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[4]  D. Hubel,et al.  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[5]  F. Møller,et al.  Binocular quantification and characterization of microsaccades , 2002, Graefe’s Archive for Clinical and Experimental Ophthalmology.

[6]  G. Gratton.  Dealing with artifacts: The EOG contamination of the event-related brain potential , 1998 .

[7]  Ralf Engbert.  Microsaccades: A microcosm for research on oculomotor control, attention, and visual perception. , 2006, Progress in brain research.

[8]  Nikos K. Logothetis,et al.  Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex , 1998, Experimental Brain Research.

[9]  Ralf Engbert,et al.  Crossmodal coupling of oculomotor control and spatial attention in vision and audition , 2005, Experimental Brain Research.

[10]  M K McGue,et al.  P300 event-related potential heritability in monozygotic and dizygotic twins. , 1997, Psychophysiology.

[11]  Ralf Engbert,et al.  Microsaccades Are an Index of Covert Attention , 2007, Psychological science.

[12]  Avi Caspi,et al.  Scaling of horizontal and vertical fixational eye movements. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[14]  M. Turatto,et al.  Are you ready? I can tell by looking at your microsaccades , 2006, Neuroreport.

[15]  Ralf Engbert,et al.  Microsaccade dynamics during covert attention , 2005, Vision Research.

[16]  M. Turatto,et al.  Microsaccadic response to visual events that are invisible to the superior colliculus. , 2007, Behavioral neuroscience.

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

[18]  B. L. Zuber,et al.  Microsaccades and the Velocity-Amplitude Relationship for Saccadic Eye Movements , 1965, Science.

[19]  Input and central processing expressed in ERP and heart rate changes to rare target and rare nontarget stimuli. , 1998, Psychophysiology.

[20]  P. Jurák,et al.  Intracerebral P3-like waveforms and the length of the stimulus–response interval in a visual oddball paradigm , 2005, Clinical Neurophysiology.

[21]  C. Rennie,et al.  Dynamics of SCR, EEG, and ERP activity in an oddball paradigm with short interstimulus intervals. , 1999, Psychophysiology.

[22]  Ishihara Shinobu,et al.  Ishihara's tests for colour deficiency : the series of plates designed as a test for colour deficiency , 1999 .

[23]  Luigi Tamè,et al.  Microsaccades distinguish between global and local visual processing , 2007, Neuroreport.

[24]  Ralf Engbert,et al.  Microsaccades Keep the Eyes' Balance During Fixation , 2004, Psychological science.

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

[26]  Ralf Engbert,et al.  Modeling the control of fixational eye movements with neurophysiological delays. , 2007, Physical review letters.

[27]  E. Donchin,et al.  On quantifying surprise: the variation of event-related potentials with subjective probability. , 1977, Psychophysiology.

[28]  H. Barlow.  Eye movements during fixation , 1952, The Journal of physiology.

[29]  N. Squires,et al.  The effect of stimulus sequence on the waveform of the cortical event-related potential. , 1976, Science.

[30]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[31]  M. Turatto,et al.  Microsaccadic response during inhibition of return in a target–target paradigm , 2007, Vision Research.

[32]  E Donchin,et al.  A metric for thought: a comparison of P300 latency and reaction time. , 1981, Science.

[33]  Xoana G. Troncoso,et al.  Microsaccades Counteract Visual Fading during Fixation , 2005, Neuron.

[34]  R. Benson,et al.  Responses to rare visual target and distractor stimuli using event-related fMRI. , 2000, Journal of neurophysiology.

[35]  M. Turatto,et al.  Inhibition of return in microsaccades , 2004, Experimental Brain Research.

[36]  J. Ford,et al.  The relationship between P300 amplitude and regional gray matter volumes depends upon the attentional system engaged. , 1994, Electroencephalography and clinical neurophysiology.

[37]  James J. Clark,et al.  Microsaccades as an overt measure of covert attention shifts , 2002, Vision Research.

[38]  R. Miall,et al.  Modulation of saccadic intrusions by exogenous and endogenous attention , 2007, Brain Research.

[39]  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.

[40]  R. Kliegl,et al.  Shortening and prolongation of saccade latencies following microsaccades , 2006, Experimental Brain Research.

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

[42]  J. Wolfe,et al.  Fixational Eye Movements Are Not an Index of Covert Attention , 2007, Psychological science.

[43]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[44]  Guideline Thirteen: Guidelines for Standard Electrode Position Nomenclature , 1994, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[45]  Rainer Goebel,et al.  Attentional systems in target and distractor processing: a combined ERP and fMRI study , 2004, NeuroImage.

[46]  Ralf Engbert,et al.  Microsaccades uncover the orientation of covert attention , 2003, Vision Research.

[47]  H. Ives.  XC. Studies in the photometry of lights of different colours.—IV. The addition of luminosities of different colour , 1912 .

[48]  E. Donchin,et al.  On the dependence of P300 latency on stimulus evaluation processes. , 1984, Psychophysiology.

[49]  P. Skudlarski,et al.  Event-related fMRI of auditory and visual oddball tasks. , 2000, Magnetic resonance imaging.

[50]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[51]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[52]  R. Knight,et al.  Mechanisms of human attention: event-related potentials and oscillations , 2001, Neuroscience & Biobehavioral Reviews.

[53]  G. Stenberg.  Extraversion and the P300 in a visual classification task , 1994 .

[54]  D. Hubel,et al.  The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[55]  E Gordon,et al.  Evoked related potentials associated with and without an orienting reflex , 1997, Neuroreport.

[56]  Matteo Valsecchi,et al.  Microsaccadic responses in a bimodal oddball task , 2009, Psychological research.

[57]  R. Verleger.  Event-related potentials and cognition: A critique of the context updating hypothesis and an alternative interpretation of P3 , 1988, Behavioral and Brain Sciences.

[58]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[59]  B. Ardekani,et al.  Functional magnetic resonance imaging of brain activity in the visual oddball task. , 2002, Brain research. Cognitive brain research.

[60]  Reinhold Kliegl,et al.  Microsaccade orientation supports attentional enhancement opposite to a peripheral cue , 2004 .

[61]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[62]  H Lyytinen,et al.  Event-related potentials and autonomic responses to a change in unattended auditory stimuli. , 1992, Psychophysiology.

[63]  J. Fleiss,et al.  Effect of stimulus uncertainty on the pupillary dilation response and the vertex evoked potential. , 1973, Electroencephalography and clinical neurophysiology.

[64]  N. Mott,et al.  The metal-non-metal transition in nickel sulphide (NiS) , 1971 .

[65]  P. Berg,et al.  The correction of ocular artifacts: a topographic perspective , 2000, Clinical Neurophysiology.

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

[67]  G. McCarthy,et al.  Augmenting mental chronometry: the P300 as a measure of stimulus evaluation time. , 1977, Science.

[68]  M. Turatto,et al.  Visual oddballs induce prolonged microsaccadic inhibition , 2007, Experimental Brain Research.

[69]  E. Halgren,et al.  Generators of the late cognitive potentials in auditory and visual oddball tasks. , 1998, Electroencephalography and clinical neurophysiology.

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

[71]  Ralf Engbert,et al.  Microsaccades are triggered by low retinal image slip. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[72]  I. Jentzsch,et al.  Sequence-sensitive subcomponents of P300: topographical analyses and dipole source localization. , 2001, Psychophysiology.

[73]  S A Hillyard,et al.  P3 waves to the discrimination of targets in homogeneous and heterogeneous stimulus sequences. , 1977, Psychophysiology.

[74]  D. Robinson.  Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.