In the blink of an eye: the contribution of microsaccadic activity to the induced γ band response.

In 2008 an article by Yuval-Greenberg and colleagues initiated a lively debate within the field of induced gamma band research. Their article suggested that scalp-recorded induced gamma band responses (iGBRs) to visual stimuli could be obscured by minute movements of extraocular muscles, called microsaccades, which are associated with the saccadic spike potentials (SPs). Yuval-Greenberg et al. (2008) proposed that the temporal and spectral characteristics of SPs could mask and have been previously mistaken for cortical induced gamma band activity. This review summarises the main findings of the report by Yuval-Greenberg et al. (2008) and the research that has emerged since its publication. Microsaccades and the associated SP waveforms are described in detail and their contribution to the iGBR discussed. Different lines of argument are considered that suggest that the scalp-recorded iGBR exists separate from ocular contributions. The article then considers techniques that are widely used to remove electroencephalogram (EEG) artefacts and their potential adaptation for the removal of SPs. The review closes by pointing to future directions that researchers may explore in order to disentangle neural iGBRs and artefactual, SP-related iGBRs, and to several routes which researchers may consider in order to increase the informative value of their scalp-recorded iGBR data. We conclude that further investigation and testing is necessary to develop signal processing tools that successfully identify and correct SPs in EEG data without distorting the neural iGBR.

[1]  R. Kliegl,et al.  Human Microsaccade-Related Visual Brain Responses , 2009, The Journal of Neuroscience.

[2]  S. Makeig,et al.  Imaging human EEG dynamics using independent component analysis , 2006, Neuroscience & Biobehavioral Reviews.

[3]  Yanda Li,et al.  Automatic removal of the eye blink artifact from EEG using an ICA-based template matching approach , 2006, Physiological measurement.

[4]  T. Elbert,et al.  Comparison of data transformation procedures to enhance topographical accuracy in time-series analysis of the human EEG , 2002, Journal of Neuroscience Methods.

[5]  Robert Oostenveld,et al.  Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming , 2008, NeuroImage.

[6]  J. Nottage,et al.  Uncovering Gamma in Visual Tasks , 2010, Brain Topography.

[7]  R. Barry,et al.  EOG correction: a comparison of four methods. , 2005, Psychophysiology.

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

[9]  B. Maess,et al.  Sources of synchronized induced Gamma-Band responses during a simple object recognition task: A replication study in human MEG , 2008, Brain Research.

[10]  F Pulvermüller,et al.  Nouns and verbs in the intact brain: evidence from event-related potentials and high-frequency cortical responses. , 1999, Cerebral cortex.

[11]  Michael J. Jutras,et al.  Synchronous neural activity and memory formation , 2010, Current Opinion in Neurobiology.

[12]  Kenneth J. Pope,et al.  Relation of Gamma Oscillations in Scalp Recordings to Muscular Activity , 2009, Brain Topography.

[13]  Elana Zion-Golumbic,et al.  Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces , 2007, NeuroImage.

[14]  T. Elbert,et al.  Visual stimulation alters local 40-Hz responses in humans: an EEG-study , 1995, Neuroscience Letters.

[15]  A. Keil,et al.  Modulation of Induced Gamma Band Responses in a Perceptual Learning Task in the Human EEG , 2002, Journal of Cognitive Neuroscience.

[16]  Maxim Bazhenov,et al.  Perceptual priming leads to reduction of gamma frequency oscillations , 2010, Proceedings of the National Academy of Sciences.

[17]  Catherine Tallon-Baudry,et al.  The roles of gamma-band oscillatory synchrony in human visual cognition. , 2009, Frontiers in bioscience.

[18]  M. Rolfs Microsaccades: Small steps on a long way , 2009, Vision Research.

[19]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[20]  H. Semlitsch,et al.  A solution for reliable and valid reduction of ocular artifacts, applied to the P300 ERP. , 1986, Psychophysiology.

[21]  Richard J. Davidson,et al.  Identifying robust and sensitive frequency bands for interrogating neural oscillations , 2010, NeuroImage.

[22]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[23]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[24]  Ralf Engbert,et al.  Flick-Induced Flips in Perception , 2006, Neuron.

[25]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[26]  T. Katila,et al.  Magnetic fields produced by the human eye (invited) , 1981 .

[27]  Alexander Maye,et al.  Temporal dynamics of access to consciousness in the attentional blink , 2007, NeuroImage.

[28]  Caspar M. Schwiedrzik,et al.  (Micro)Saccades, corollary activity and cortical oscillations , 2009, Trends in Cognitive Sciences.

[29]  Shlomit Yuval-Greenberg,et al.  Saccadic spike potentials in gamma-band EEG: Characterization, detection and suppression , 2010, NeuroImage.

[30]  Werner Lutzenberger,et al.  Task- and performance-related modulation of domain-specific auditory short-term memory representations in the gamma-band , 2009, NeuroImage.

[31]  T. Gasser,et al.  The transfer of EOG activity into the EEG for eyes open and closed. , 1985, Electroencephalography and clinical neurophysiology.

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

[33]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[34]  G. Thickbroom,et al.  Presaccadic ‘spike’ potential: Investigation of topography and source , 1985, Brain Research.

[35]  Sven Hoffmann,et al.  The Correction of Eye Blink Artefacts in the EEG: A Comparison of Two Prominent Methods , 2008, PloS one.

[36]  S. Bentin,et al.  Dissociated neural mechanisms for face detection and configural encoding: evidence from N170 and induced gamma-band oscillation effects. , 2007, Cerebral cortex.

[37]  G. Thickbroom,et al.  Presaccadic spike potential. Relation to eye movement direction. , 1986, Electroencephalography and clinical neurophysiology.

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

[39]  B. Hjorth An on-line transformation of EEG scalp potentials into orthogonal source derivations. , 1975, Electroencephalography and clinical neurophysiology.

[40]  S. Debener,et al.  Late auditory evoked potentials asymmetry revisited , 2007, Clinical Neurophysiology.

[41]  Ingo Fründ,et al.  Human gamma-band activity: A review on cognitive and behavioral correlates and network models , 2010, Neuroscience & Biobehavioral Reviews.

[42]  C. Im,et al.  Dysfunctional gamma-band activity during face structural processing in schizophrenia patients , 2010, Schizophrenia Research.

[43]  A. Mognon,et al.  ADJUST: An automatic EEG artifact detector based on the joint use of spatial and temporal features. , 2011, Psychophysiology.

[44]  Matthias M. Müller,et al.  Modulation of oscillatory brain activity and evoked potentials in a repetition priming task in the human EEG , 2004, The European journal of neuroscience.

[45]  R. Steinman,et al.  Voluntary Control of Microsaccades during Maintained Monocular Fixation , 1967, Science.

[46]  R. Reid,et al.  Saccadic Eye Movements Modulate Visual Responses in the Lateral Geniculate Nucleus , 2002, Neuron.

[47]  T. Bachmann,et al.  Occipital EEG correlates of conscious awareness when subjective target shine-through and effective visual masking are compared: Bifocal early increase in gamma power and speed-up of P1 , 2009, Brain Research.

[48]  Burkhard Maess,et al.  Memory-matches evoke human gamma-responses , 2004, BMC Neuroscience.

[49]  R. Steinman,et al.  Small saccades serve no useful purpose: Reply to a letter by R. W. Ditchburn , 1980, Vision Research.

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

[51]  Matthias M. Müller,et al.  Modulation of induced gamma band activity in the human EEG by attention and visual information processing. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[53]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[54]  J. Schwind,et al.  Off-line removal of ocular artifacts from event-related potentials using a multiple linear regression model. , 1986, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[56]  S. Yuval-Greenberg,et al.  The Broadband-Transient Induced Gamma-Band Response in Scalp EEG Reflects the Execution of Saccades , 2009, Brain Topography.

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

[58]  Clay B. Holroyd,et al.  Detection of synchronized oscillations in the electroencephalogram: an evaluation of methods. , 2004, Psychophysiology.

[59]  Ralf Engbert,et al.  Toward a model of microsaccade generation: the case of microsaccadic inhibition. , 2008, Journal of vision.

[60]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[61]  Philippe Kahane,et al.  Saccade Related Gamma-Band Activity in Intracerebral EEG: Dissociating Neural from Ocular Muscle Activity , 2009, Brain Topography.

[62]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[63]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[64]  J. Pernier,et al.  Stimulus Specificity of Phase-Locked and Non-Phase-Locked 40 Hz Visual Responses in Human , 1996, The Journal of Neuroscience.

[65]  Richard J. Davidson,et al.  Electromyogenic Artifacts and Electroencephalographic Inferences , 2009, Brain Topography.

[66]  Tal Golan,et al.  Human face preference in gamma-frequency EEG activity , 2008, NeuroImage.

[67]  Matthias M. Müller,et al.  A cross-laboratory study of event-related gamma activity in a standard object recognition paradigm , 2006, NeuroImage.

[68]  Werner Lutzenberger,et al.  Words and pseudowords elicit distinct patterns of 30-Hz EEG responses in humans , 1994, Neuroscience Letters.

[69]  J C Armington,et al.  Relations between the amplitudes of spontaneous saccades and visual responses. , 1974, Journal of the Optical Society of America.

[70]  R. Barry,et al.  Removal of ocular artifact from the EEG: a review , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[71]  N V Reva,et al.  The coincidence between late non-phase-locked gamma synchronization response and saccadic eye movements. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[72]  S. Debener,et al.  Source localization of auditory evoked potentials after cochlear implantation. , 2007, Psychophysiology.

[73]  T. Sejnowski,et al.  Analysis and visualization of single‐trial event‐related potentials , 2001, Human brain mapping.

[74]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[75]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[76]  Matthias M. Müller,et al.  Selective visual-spatial attention alters induced gamma band responses in the human EEG , 1999, Clinical Neurophysiology.

[77]  O. Bertrand,et al.  Attention modulates gamma-band oscillations differently in the human lateral occipital cortex and fusiform gyrus. , 2005, Cerebral cortex.

[78]  Andreas K. Engel,et al.  EEG gamma-band activity in rapid serial visual presentation , 2006, Experimental Brain Research.

[79]  A. A. Skavenski,et al.  Quality of retinal image stabilization during small natural and artificial body rotations in man , 1979, Vision Research.

[80]  Tom Eichele,et al.  Semi-automatic identification of independent components representing EEG artifact , 2009, Clinical Neurophysiology.

[81]  D. Hubel,et al.  The role of fixational eye movements in visual perception , 2004, Nature Reviews Neuroscience.

[82]  Till R. Schneider,et al.  Using ICA for the Analysis of Multi-Channel EEG Data , 2010 .

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

[84]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[85]  S. Debener,et al.  Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[86]  R. Eckhorn,et al.  Visual stimulation elicits locked and induced gamma oscillations in monkey intracortical- and EEG-potentials, but not in human EEG , 1999, Experimental Brain Research.