Human occipital cortices differentially exert saccadic suppression: Intracranial recording in children

By repeating saccades unconsciously, humans explore the surrounding world every day. Saccades inevitably move external visual images across the retina at high velocity; nonetheless, healthy humans don't perceive transient blurring of the visual scene during saccades. This perceptual stability is referred to as saccadic suppression. Functional suppression is believed to take place transiently in the visual systems, but it remains unknown how commonly or differentially the human occipital lobe activities are suppressed at the large-scale cortical network level. We determined the spatial-temporal dynamics of intracranially-recorded gamma activity at 80-150 Hz around spontaneous saccades under no-task conditions during wakefulness and those in darkness during REM sleep. Regardless of wakefulness or REM sleep, a small degree of attenuation of gamma activity was noted in the occipital regions during saccades, most extensively in the polar and least in the medial portions. Longer saccades were associated with more intense gamma-attenuation. Gamma-attenuation was subsequently followed by gamma-augmentation most extensively involving the medial and least involving the polar occipital region. Such gamma-augmentation was more intense during wakefulness and temporally locked to the offset of saccades. The polarities of initial peaks of perisaccadic event-related potentials (ERPs) were frequently positive in the medial and negative in the polar occipital regions. The present study, for the first time, provided the electrophysiological evidence that human occipital cortices differentially exert perisaccadic modulation. Transiently suppressed sensitivity of the primary visual cortex in the polar region may be an important neural basis for saccadic suppression. Presence of occipital gamma-attenuation even during REM sleep suggests that saccadic suppression might be exerted even without external visual inputs. The primary visual cortex in the medial region, compared to the polar region, may be more sensitive to an upcoming visual scene provided at the offset of each saccade.

[1]  Robert T. Knight,et al.  Localization of neurosurgically implanted electrodes via photograph–MRI–radiograph coregistration , 2008, Journal of Neuroscience Methods.

[2]  Qing Yang,et al.  Saccade–vergence dynamics and interaction in children and in adults , 2004, Experimental Brain Research.

[3]  Philippe Kahane,et al.  Exploring the electrophysiological correlates of the default ‐ mode network with intracerebral EEG , 2022 .

[4]  Ivan Bodis-Wollner,et al.  Perisaccadic Parietal and Occipital Gamma Power in Light and in Complete Darkness , 2008, Perception.

[5]  Philippe Kahane,et al.  Task‐related gamma‐band dynamics from an intracerebral perspective: Review and implications for surface EEG and MEG , 2009, Human brain mapping.

[6]  Lina Shihabuddin,et al.  MRI assessment of gray and white matter distribution in Brodmann's areas of the cortex in patients with schizophrenia with good and poor outcomes. , 2003, The American journal of psychiatry.

[7]  R. Simes,et al.  An improved Bonferroni procedure for multiple tests of significance , 1986 .

[8]  J M K SPALDING,et al.  WOUNDS OF THE VISUAL PATHWAY , 1952, Journal of neurology, neurosurgery, and psychiatry.

[9]  François Mauguière,et al.  Relationship between intracerebral gamma oscillations and slow potentials in the human sensorimotor cortex , 2006, The European journal of neuroscience.

[10]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[11]  Otto Muzik,et al.  Quantitative brain surface mapping of an electrophysiologic/metabolic mismatch in human neocortical epilepsy , 2009, Epilepsy Research.

[12]  Eishi Asano,et al.  Clinical significance and developmental changes of auditory-language-related gamma activity , 2013, Clinical Neurophysiology.

[13]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[14]  J. Gotman,et al.  High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type. , 2009, Brain : a journal of neurology.

[15]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[16]  Steven F. Kalik,et al.  Analysis of perisaccadic field potentials in the occipitotemporal pathway during active vision. , 2003, Journal of neurophysiology.

[17]  B. Bridgeman,et al.  Saccadic Suppression of Displacement is Strongest in Central Vision , 1990, Perception.

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

[19]  Philippe Kahane,et al.  Intracerebral dynamics of saccade generation in the human frontal eye field and supplementary eye field , 2006, NeuroImage.

[20]  Michael R. Ibbotson,et al.  Saccadic Modulation of Neural Responses: Possible Roles in Saccadic Suppression, Enhancement, and Time Compression , 2008, The Journal of Neuroscience.

[21]  R P Lesser,et al.  Cortical somatosensory evoked potentials in response to hand stimulation. , 1983, Journal of neurosurgery.

[22]  Rajesh P. N. Rao,et al.  Cortical electrode localization from X-rays and simple mapping for electrocorticographic research: The “Location on Cortex” (LOC) package for MATLAB , 2007, Journal of Neuroscience Methods.

[23]  Xoana G. Troncoso,et al.  Saccades and microsaccades during visual fixation, exploration, and search: foundations for a common saccadic generator. , 2008, Journal of vision.

[24]  F. C. Volkmann,et al.  Time course of visual inhibition during voluntary saccades. , 1968, Journal of the Optical Society of America.

[25]  A Villringer,et al.  Saccadic Suppression Induces Focal Hypooxygenation in the Occipital Cortex , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[26]  Akitoshi Hanazawa,et al.  Occipital gamma-oscillations modulated during eye movement tasks: Simultaneous eye tracking and electrocorticography recording in epileptic patients , 2011, NeuroImage.

[27]  M. B. Bender,et al.  BOOK REVIEWS , 2003 .

[28]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[29]  J. Horton,et al.  The representation of the visual field in human striate cortex. A revision of the classic Holmes map. , 1991, Archives of ophthalmology.

[30]  K. Hoffmann,et al.  Neural Dynamics of Saccadic Suppression , 2009, Journal of Neuroscience.

[31]  D. Burr,et al.  Selective suppression of the magnocellular visual pathway during saccadic eye movements , 1994, Nature.

[32]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[33]  Andreas Schulze-Bonhage,et al.  Signal quality of simultaneously recorded invasive and non-invasive EEG , 2009, NeuroImage.

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

[35]  Eishi Asano,et al.  Independent predictors of neuronal adaptation in human primary visual cortex measured with high-gamma activity , 2012, NeuroImage.

[36]  Otto Muzik,et al.  Short-latency median-nerve somatosensory-evoked potentials and induced gamma-oscillations in humans. , 2008, Brain : a journal of neurology.

[37]  J. M. Lina,et al.  Recording and analysis techniques for high-frequency oscillations , 2012, Progress in Neurobiology.

[38]  G. Karmos,et al.  Transient cortical excitation at the onset of visual fixation. , 2008, Cerebral cortex.

[39]  S. Klein,et al.  Detection and discrimination of the direction of motion in central and peripheral vision of normal and amblyopic observers , 1984, Vision Research.

[40]  Alan B Saul,et al.  Effects of fixational saccades on response timing in macaque lateral geniculate nucleus , 2010, Visual Neuroscience.

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

[42]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

[43]  C C Wood,et al.  Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. , 1989, Journal of neurophysiology.

[44]  F. Duffy,et al.  Eye movement-related inhibition of primate visual neurons , 1975, Brain Research.

[45]  G. Rees,et al.  Saccades Differentially Modulate Human LGN and V1 Responses in the Presence and Absence of Visual Stimulation , 2005, Current Biology.

[46]  Yehezkel Yeshurun,et al.  Antagonistic relationship between gamma power and visual evoked potentials revealed in human visual cortex. , 2011, Cerebral cortex.

[47]  E. Halgren,et al.  High-frequency neural activity and human cognition: Past, present and possible future of intracranial EEG research , 2012, Progress in Neurobiology.

[48]  M. Morrone,et al.  Development of saccadic suppression in children. , 2006, Journal of neurophysiology.

[49]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[50]  Kazuhiko Fukuda,et al.  Proposed supplements and amendments to ‘A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects’, the Rechtschaffen & Kales (1968) standard , 2001, Psychiatry and clinical neurosciences.

[51]  R. Sperry Neural basis of the spontaneous optokinetic response produced by visual inversion. , 1950, Journal of comparative and physiological psychology.

[52]  Xoana G. Troncoso,et al.  Microsaccades: a neurophysiological analysis , 2009, Trends in Neurosciences.

[53]  A. Dekaban,et al.  Changes in brain weights during the span of human life: Relation of brain weights to body heights and body weights , 1978, Annals of neurology.

[54]  Michael R. Ibbotson,et al.  Effects of saccades on visual processing in primate MSTd , 2010, Vision Research.

[55]  Terry A. Bahill,et al.  Variability and development of a normative data base for saccadic eye movements. , 1981, Investigative ophthalmology & visual science.

[56]  Bart Krekelberg,et al.  Neural Correlates of Saccadic Suppression in Humans , 2004, Current Biology.

[57]  J. Bullier,et al.  Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey , 2001, Visual Neuroscience.

[58]  Eishi Asano,et al.  Gamma activity modulated by picture and auditory naming tasks: Intracranial recording in patients with focal epilepsy , 2013, Clinical Neurophysiology.

[59]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[60]  Brindley Gs,et al.  The visual sensations produced by electrical stimulation of the medial occipital cortex. , 1968, The Journal of physiology.

[61]  Daniel Yoshor,et al.  Receptive fields in human visual cortex mapped with surface electrodes. , 2007, Cerebral cortex.

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

[63]  F. Duffy,et al.  Electrophysiological Evidence for Visual Suppression prior to the Onset of a Voluntary Saccadic Eye Movement , 1968, Nature.

[64]  S. Klein,et al.  Neural saccadic response estimation during natural viewing. , 2012, Journal of neurophysiology.

[65]  C. Rowell,et al.  Saccadic suppression by corollary discharge in the locust , 1979, Nature.

[66]  E. Niebur,et al.  Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography , 2008, The Journal of Neuroscience.

[67]  Christopher K. Kovach,et al.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings , 2011, NeuroImage.

[68]  Juan R. Vidal,et al.  Category-Specific Visual Responses: An Intracranial Study Comparing Gamma, Beta, Alpha, and ERP Response Selectivity , 2010, Front. Hum. Neurosci..

[69]  Fatih M Uckun,et al.  Evaluating dissolution profiles of an anti-HIV agent using ANOVA and non-linear regression models in JMP software. , 2003, International journal of pharmaceutics.

[70]  J L Ringo,et al.  Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons. , 1994, Journal of neurophysiology.

[71]  N Papp,et al.  Critical evaluation of complex demodulation techniques for the quantification of bioelectrical activity. , 1977, Biomedical sciences instrumentation.

[72]  Tomoyuki Akiyama,et al.  Cortical gamma‐oscillations modulated by auditory–motor tasks‐intracranial recording in patients with epilepsy , 2010, Human brain mapping.

[73]  C. Elger,et al.  Digital Photography and 3D MRI–based Multimodal Imaging for Individualized Planning of Resective Neocortical Epilepsy Surgery , 2002, Epilepsia.

[74]  J Gotman,et al.  High-frequency oscillations mirror disease activity in patients with epilepsy , 2009, Neurology.

[75]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

[76]  K. Miller,et al.  Direct electrophysiological measurement of human default network areas , 2009, Proceedings of the National Academy of Sciences.

[77]  Eishi Asano,et al.  Role of subdural electrocorticography in prediction of long-term seizure outcome in epilepsy surgery. , 2009, Brain : a journal of neurology.

[78]  Yi Lu,et al.  Multimodality Data Integration in Epilepsy , 2007, Int. J. Biomed. Imaging.

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

[80]  Bertrand Gaymard,et al.  Do the eyes scan dream images during rapid eye movement sleep? Evidence from the rapid eye movement sleep behaviour disorder model. , 2010, Brain : a journal of neurology.

[81]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[82]  R. Hari,et al.  Spatiotemporal characteristics of sensorimotor neuromagnetic rhythms related to thumb movement , 1994, Neuroscience.

[83]  Juan R. Vidal,et al.  Transient Suppression of Broadband Gamma Power in the Default-Mode Network Is Correlated with Task Complexity and Subject Performance , 2011, The Journal of Neuroscience.

[84]  J. Biernaskie,et al.  Habitat assessment ability of bumble-bees implies frequency-dependent selection on floral rewards and display size , 2007, Proceedings of the Royal Society B: Biological Sciences.

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

[86]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[87]  J. Gotman,et al.  Effect of sleep stage on interictal high‐frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy , 2009, Epilepsia.

[88]  D. Snodderly,et al.  Saccades and drifts differentially modulate neuronal activity in V1: effects of retinal image motion, position, and extraretinal influences. , 2008, Journal of vision.

[89]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

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

[91]  C. Svarer,et al.  Parieto-occipital cortex activation during self-generated eye movements in the dark. , 1998, Brain : a journal of neurology.

[92]  Eishi Asano,et al.  Gamma-oscillations modulated by picture naming and word reading: Intracranial recording in epileptic patients , 2011, Clinical Neurophysiology.

[93]  M. Schlag-Rey,et al.  Through the eye, slowly; Delays and localization errors in the visual system , 2002, Nature Reviews Neuroscience.