Visually evoked responses from the blind field of hemianopic patients

Hemianopia is a visual field defect characterized by decreased vision or blindness in the contralesional visual field of both eyes. The presence of well documented above-chance unconscious behavioural responses to visual stimuli presented to the blind hemifield (blindsight) has stimulated a great deal of research on the neural basis of this important phenomenon. The present study is concerned with electrophysiological responses from the blind field. Since previous studies found that transient Visual Evoked Potentials (VEPs) are not entirely suitable for this purpose here we propose to use Steady-State VEPs (SSVEPs). A positive result would have important implications for the understanding of the neural bases of conscious vision. We carried out a passive SSVEP stimulation with healthy participants and hemianopic patients. Stimuli consisted of four black-and-white sinusoidal Gabor gratings presented one in each visual field quadrant and flickering one at a time at a 12 Hz rate. To assess response reliability a Signal-to-Noise Ratio analysis was conducted together with further analyses in time and frequency domains to make comparisons between groups (healthy participants and patients), side of brain lesion (left and right) and visual fields (sighted and blind). The important overall result was that stimulus presentation to the blind hemifield yielded highly reliable responses with time and frequency features broadly similar to those found for cortical extrastriate areas in healthy controls. Moreover, in the intact hemifield of hemianopics and in healthy controls there was evidence of a role of prefrontal structures in perceptual awareness. Finally, the presence of different patterns of brain reorganization depended upon the side of lesion.

[1]  M. Kenward,et al.  An Introduction to the Bootstrap , 2007 .

[2]  E. Làdavas,et al.  Unseen fearful faces facilitate visual discrimination in the intact field , 2017, Neuropsychologia.

[3]  A. Neetens,et al.  Visual evoked potentials. , 1982, Bulletin de la Societe belge d'ophtalmologie.

[4]  Alex R. Wade,et al.  The effects of visuospatial attention measured across visual cortex using source-imaged, steady-state EEG. , 2010, Journal of vision.

[5]  R. Wurtz,et al.  Functional Identification of a Pulvinar Path from Superior Colliculus to Cortical Area MT , 2010, The Journal of Neuroscience.

[6]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[7]  Mark D'Esposito,et al.  Corrections to: Top–down flow of visual spatial attention signals from parietal to occipital cortex , 2010 .

[8]  I. Bodis-Wollner,et al.  Visual contrast sensitivity , 1988, Neurology.

[9]  R. Tibshirani,et al.  An introduction to the bootstrap , 1993 .

[10]  Minfen Shen,et al.  Independent component analysis of electroencephalographic signals , 2002, 6th International Conference on Signal Processing, 2002..

[11]  T. Schenkenberg,et al.  Line bisection and unilateral visual neglect in patients with neurologic impairment , 1980, Neurology.

[12]  F. Russo,et al.  Short-term visual cortical plasticity in visual and non-visual areas induced by monovision , 2017 .

[13]  R. Held,et al.  Residual Visual Function after Brain Wounds involving the Central Visual Pathways in Man , 1973, Nature.

[14]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[15]  F. Di Russo,et al.  Immediate cortical adaptation in visual and non‐visual areas functions induced by monovision , 2018, The Journal of physiology.

[16]  J. Brecelj Visual evoked potentials and the localization of visual pathway lesions , 1991, Spektrum der Augenheilkunde.

[17]  Olivier A. Coubard,et al.  An fMRI Investigation of the Cortical Network Underlying Detection and Categorization Abilities in Hemianopic Patients , 2013, Brain Topography.

[18]  Ariel Rokem,et al.  Human blindsight is mediated by an intact geniculo-extrastriate pathway , 2015, eLife.

[19]  C. Gross Contribution of striate cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex , 1991, Neuropsychologia.

[20]  Paola Binda,et al.  Renewed Attention on the Pupil Light Reflex , 2017, Trends in Neurosciences.

[21]  Christopher Kennard,et al.  Visual activation of extra-striate cortex in the absence of V1 activation , 2010, Neuropsychologia.

[22]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[23]  H-J Heinze,et al.  Unmasking Motion-Processing Activity in Human Brain Area V5/MT+ Mediated by Pathways That Bypass Primary Visual Cortex , 2002, NeuroImage.

[24]  Sabrina Pitzalis,et al.  Spatio-Temporal Brain Mapping of Motion-Onset VEPs Combined with fMRI and Retinotopic Maps , 2012, PloS one.

[25]  Krystel R. Huxlin,et al.  Role of inter-hemispheric transfer in generating visual evoked potentials in V1-damaged brain hemispheres , 2015, Neuropsychologia.

[26]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[27]  Lawrence Weiskrantz,et al.  Consciousness Lost and Found: A Neuropsychological Exploration , 1999 .

[28]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[29]  C. Lucas,et al.  The effect of visual training for patients with visual field defects due to brain damage: a systematic review , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[30]  D. Spinelli,et al.  Spatiotemporal analysis of the cortical sources of the steady‐state visual evoked potential , 2007, Human brain mapping.

[31]  Tirin Moore,et al.  Selective Modulation of the Pupil Light Reflex by Microstimulation of Prefrontal Cortex , 2017, The Journal of Neuroscience.

[32]  J. C. Wolters,et al.  Protein biogenesis machinery is a driver of replicative aging in yeast , 2015, eLife.

[33]  F. Russo,et al.  29. ERP generators in an omitted-target oddball task: A simultaneous EEG-fMRI study , 2016, Clinical Neurophysiology.

[34]  Michael X. Cohen,et al.  Rhythmic entrainment source separation: Optimizing analyses of neural responses to rhythmic sensory stimulation , 2016, NeuroImage.

[35]  D. Goodin,et al.  Visual evoked potentials in the investigation of “blindsight” , 1988, Neurology.

[36]  N. Galloway Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine , 1990 .

[37]  L Weiskrantz,et al.  Early extrastriate activity without primary visual cortex in humans , 2000, Neuroscience Letters.

[38]  D. Regan Human brain electrophysiology: Evoked potentials and evoked magnetic fields in science and medicine , 1989 .

[39]  R. Passingham,et al.  Acting, seeing, and conscious awareness , 2017, Neuropsychologia.

[40]  L. Gauthier,et al.  The Bells Test: A quantitative and qualitative test for visual neglect. , 1989 .

[41]  B. Sabel,et al.  Contour-integration deficits on the intact side of the visual field in hemianopia patients , 2008, Behavioural Brain Research.

[42]  Silvia Savazzi,et al.  Lights from the Dark: Neural Responses from a Blind Visual Hemifield , 2017, Front. Neurosci..

[43]  Georgios A Keliris,et al.  Population receptive field analysis of the primary visual cortex complements perimetry in patients with homonymous visual field defects , 2014, Proceedings of the National Academy of Sciences.

[44]  Seungjin Choi,et al.  Independent Component Analysis , 2009, Handbook of Natural Computing.

[45]  Gaspare Galati,et al.  Hemispheric asymmetries in the transition from action preparation to execution , 2017, NeuroImage.

[46]  R. Hays,et al.  Development of the 25-item National Eye Institute Visual Function Questionnaire. , 2001 .

[47]  D. Spinelli,et al.  Brain waves from an “isolated” cortex: contribution of the anterior insula to cognitive functions , 2017, Brain Structure and Function.

[48]  L Weiskrantz,et al.  Visual capacity in the hemianopic field following a restricted occipital ablation. , 1974, Brain : a journal of neurology.

[49]  Steven A. Hillyard,et al.  Steady-State VEP and Attentional Visual Processing , 2003 .

[50]  Ingo Fründ,et al.  Impairments of Gestalt perception in the intact hemifield of hemianopic patients are reflected in gamma-band EEG activity , 2009, Neuropsychologia.

[51]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

[52]  R F Hess,et al.  Spatial and temporal contrast sensitivity in hemianopia. A comparative study of the sighted and blind hemifields. , 1989, Brain : a journal of neurology.

[53]  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.

[54]  S. Chokron,et al.  Hemisphere-dependent ipsilesional deficits in hemianopia: Sightblindness in the ‘intact’ visual field , 2015, Cortex.

[55]  Donatella Spinelli,et al.  Spatiotemporal brain mapping during preparation, perception, and action , 2016, NeuroImage.

[56]  L. Weiskrantz,et al.  Pupil response as a predictor of blindsight in hemianopia , 2013, Proceedings of the National Academy of Sciences.

[57]  C. N. Guy,et al.  Motion specific responses from a blind hemifield. , 1996, Brain : a journal of neurology.

[58]  M. Berchicci,et al.  New insights into old waves. Matching stimulus- and response-locked ERPs on the same time-window , 2016, Biological Psychology.

[59]  H. Diener,et al.  Cortical activation in hemianopia after stroke , 2007, Neuroscience Letters.

[60]  L. Weiskrantz Blindsight revisited , 1996, Current Opinion in Neurobiology.

[61]  D. Tolhurst,et al.  Visual Contrast Sensitivity Deficits in ‘Normal' Visual Field of Patients with Homonymous Visual Field Defects due to Stroke: A Pilot Study , 2013, Cerebrovascular Diseases.

[62]  C. Tagliabue,et al.  Reliability in reporting perceptual experience: Behaviour and electrophysiology in hemianopic patients , 2019, Neuropsychologia.