Adult; Humans; Visual Acuity; Electrodes; Electroencephalography; Evoked Potentials, Visual; Vision, Low; EEG; face individuation; sweep visual evoked potentials; word recognition; Ophthalmology; Sensory Systems; Cellular and Molecular Neuroscience; General Medicine
Abstract :
[en] [en] PURPOSE: Visual function is typically evaluated in clinical settings with visual acuity (VA), a test requiring to behaviorally match or name optotypes such as tumbling E or Snellen letters. The ability to recognize these symbols has little in common with the automatic and rapid visual recognition of socially important stimuli in real life. Here we use sweep visual evoked potentials to assess spatial resolution objectively based on the recognition of human faces and written words.
METHODS: To this end, we tested unfamiliar face individuation1 and visual word recognition2 in 15 normally sighted adult volunteers with a 68-electrode electroencephalogram system.
RESULTS: Unlike previous measures of low-level visual function including VA, the most sensitive electrode was found at an electrode different from Oz in a majority of participants. Thresholds until which faces and words could be recognized were evaluated at the most sensitive electrode defined individually for each participant. Word recognition thresholds corresponded with the VA level expected from normally sighted participants, and even a VA significantly higher than expected from normally sighted individuals for a few participants.
CONCLUSIONS: Spatial resolution can be evaluated based on high-level stimuli encountered in day-to-day life, such as faces or written words with sweep visual evoked potentials.
Disciplines :
Ophthalmology
Author, co-author :
Hemptinne, Coralie; Institute of Neuroscience, Université catholique de Louvain, Louvain-La-Neuve, Belgium ; Ophthalmology Department, Cliniques Universitaires Saint-Luc, Brussels, Belgium
Hupin, Nathan; Institute of Neuroscience, Université catholique de Louvain, Louvain-La-Neuve, Belgium ; Ophthalmology Department, Cliniques Universitaires Saint-Luc, Brussels, Belgium
LOCHY, Aliette ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Cognitive Science and Assessment
Yüksel, Demet; Institute of Neuroscience, Université catholique de Louvain, Louvain-La-Neuve, Belgium ; Ophthalmology Department, Cliniques Universitaires Saint-Luc, Brussels, Belgium
Rossion, Bruno; Institute of Neuroscience, Université catholique de Louvain, Louvain-La-Neuve, Belgium ; University of Lorraine, CNRS, CRAN, Lorraine, France
External co-authors :
yes
Language :
English
Title :
Spatial Resolution Evaluation Based on Experienced Visual Categories With Sweep Evoked Periodic EEG Activity.
Publication date :
01 March 2023
Journal title :
Investigative Ophthalmology and Visual Science
ISSN :
0146-0404
eISSN :
1552-5783
Publisher :
Association for Research in Vision and Ophthalmology Inc., United States
Liu-Shuang J, Norcia AM, Rossion B. An objective index of individual face discrimination in the right occipitotemporal cortex by means of fast periodic oddball stimulation. Neuropsychologia. 2014;52:57–72, doi:10.1016/j. neuropsychologia.2013.10.022.
Lochy A, Van Belle G, Rossion B. A robust index of lexical representation in the left occipito-temporal cortex as evidenced by EEG responses to fast periodic visual stimulation. Neuropsychologia. 2015;66:18–31, doi:10.1016/ j.neuropsychologia.2014.11.007.
Trick GL. Beyond visual acuity: New and complementary tests of visual function. Neurol Clin. 2003;21(2):363–386, doi:10.1016/S0733-8619(02)00104-4.
Anstice NS, Thompson B. The measurement of visual acuity in children: An evidence-based update. Clin Exp Optom. 2014;97(1):3–11, doi:10.1111/cxo.12086.
Heinrich SP. Similar dependence of acuity measures on exposure duration irrespective of acuity level in artificially degraded vision. Curr Eye Res. 2021;46(4):595–598, doi:10. 1080/02713683.2020.1809003.
De Haan EHF, Heywood CA, Young AW, Edelstyn N, Newcombe F. Ettlinger revisited: The relation between agnosia and sensory impairment. J Neurol Neurosurg Psychiatry. 1995;58(3):350–356, doi:10.1136/jnnp.58.3.350.
Hamilton R, Bach M, Heinrich SP, et al. VEP estimation of visual acuity: A systematic review. Doc Ophthalmol. 2021;142(1):25–74, doi:10.1007/s10633-020-09770-3.
Almoqbel F, Leat SJ, Irving E. The technique, validity and clinical use of the sweep VEP. Ophthalmic Physiol Opt. 2008;28:393–403, doi:10.1111/j.1475-1313.2008.00591.x.
Zheng X, Xu G, Zhang K, et al. Assessment of human visual acuity using visual evoked potential: A review. Sensors. 2020;20(19):5542, doi:10.3390/s20195542.
Odom JV, Bach M, Brigell M, et al. ISCEV standard for clinical visual evoked potentials: (2016 update). Doc Ophthalmol. 2016;133(1):1–9, doi:10.1007/s10633-016-9553-y.
Adrian ED, Matthews BHC. The Berger rhythm: Potential changes from the occipital lobes in man. Brain. 1934;57:355–385, doi:10.1093/brain/57.4.355.
Regan D. Some characteristics of average steady-state and transient responses evoked by modulated light. Electroencephalogr Clin Neurophysiol. 1966;20:238–248, doi:10.1016/ 0013-4694(66)90088-5.
Regan D. Rapid objective refraction using evoked brain potentials. Investig Ophthalmol Vis Sci. 1973;12:669–679.
Norcia AM, Tyler CW. Spatial frequency sweep VEP: Visual acuity during the first year of life. Vision Res. 1985;25:1399–1408, doi:10.1016/0042-6989(85)90217-2.
Rossion B, Boremanse A. Robust sensitivity to facial identity in the right human occipito-temporal cortex as revealed by steady-state visual-evoked potentials. J Vis. 2011;11(2):16, doi:10.1167/11.2.16.
Guillaume M, Mejias S, Rossion B, Dzhelyova M, Schiltz C. A rapid, objective and implicit measure of visual quantity discrimination. Neuropsychologia. 2018;111:180–189, doi:10.1016/j.neuropsychologia.2018.01.044.
Xu B, Liu-Shuang J, Rossion B, Tanaka J. Individual differences in face identity processing with fast periodic visual stimulation. J Cogn Neurosci. 2017;29(8):1368–1377, doi:10. 1162/jocn_a_01126.
Stacchi L, Liu-Shuang J, Ramon M, Caldara R. Reliability of individual differences in neural face identity discrimination. Neuroimage. 2019;189:468–475, doi:10.1016/j.neuroimage. 2019.01.023.
Rossion B. Twenty years of investigation with the case of prosopagnosia PS to understand human face identity recognition. Part II: Neural basis. Neuropsychologia. 2022;173:108279, doi:10.1016/j.neuropsychologia. 2022.108279.
Rossion B. Twenty years of investigation with the case of prosopagnosia PS to understand human face identity recognition. Part I: Function. Neuropsychologia. 2022;173:108278, doi:10.1016/j.neuropsychologia.2022.108278.
Lavallée MM, Gandini D, Rouleau I, et al. A qualitative impairment in face perception in Alzheimer’s disease: Evidence from a reduced face inversion effect. Caramelli P, ed. J Alzheimer’s Dis. 2016;51(4):1225–1236, doi:10.3233/ JAD-151027.
Bullimore MA, Bailey IL, Wacker RT. Face recognition in age-related maculopathy. Investig Ophthalmol Vis Sci. 1991;32(7):2020–2029.
Elliott DB, Patla A, Bullimore MA. Improvements in clinical and functional vision and perceived visual disability after first and second eye cataract surgery. Br J Ophthalmol. 1997;81(10):889–895, doi:10.1136/bjo.81.10.889.
Hirji SH, Hood DC, Liebmann JM, Blumberg DM. Association of patterns of glaucomatous macular damage with contrast sensitivity and facial recognition in patients with glaucoma. JAMA Ophthalmol. 2021;139(1):27–32, doi:10.1001/ jamaophthalmol.2020.4749.
Logan AJ, Gordon GE, Loffler G. The effect of age-related macular degeneration on components of face perception. Invest Ophthalmol Vis Sci. 2020;61(6):38, doi:10.1167/iovs. 61.6.38.
Taylor DJ, Smith ND, Binns AM, Crabb DP. The effect of non-neovascular age-related macular degeneration on face recognition performance. Graefe’s Arch Clin Exp Ophthalmol. 2018;256(4):815–821, doi:10.1007/s00417-017-3879-3.
Cattaneo Z, Vecchi T, Monegato M, Pece A, Merabet LB, Carbon CC. Strabismic amblyopia affects relational but not featural and Gestalt processing of faces. Vision Res. 2013;80:1–12, doi:10.1016/j.visres.2013.01.007.
de Heering A, Maurer D. Face memory deficits in patients deprived of early visual input by bilateral congenital cataracts. Dev Psychobiol. 2014;56(1):96–108, doi:10.1002/ dev.21094.
Rossion B, Retter TL, Liu-Shuang J. Understanding human individuation of unfamiliar faces with oddball fast periodic visual stimulation and electroencephalography. Eur J Neurosci. 2020;52(10):4283–4344, doi:10.1111/ejn.14865.
Lochy A, Van Reybroeck M, Rossion B. Left cortical specialization for visual letter strings predicts rudimentary knowledge of letter-sound association in preschoolers. Proc Natl Acad Sci USA. 2016;113(30):8544–8549, doi:10.1073/ pnas.1520366113.
van de Walle de Ghelcke A, Rossion B, Schiltz C, Lochy A. Impact of learning to read in a mixed approach on neural tuning to words in beginning readers. Front Psychol. 2020;10:3043, doi:10.3389/fpsyg.2019.03043.
Liu-Shuang J, Torfs K, Rossion B. An objective electrophysiological marker of face individualisation impairment in acquired prosopagnosia with fast periodic visual stimulation. Neuropsychologia. 2016;83:100–113, doi:10.1016/j. neuropsychologia.2015.08.023.
Hemptinne C, Liu-Shuang J, Yuksel D, Rossion B. Rapid objective assessment of contrast sensitivity and visual acuity with sweep visual evoked potentials and an extended electrode array. Invest Ophthalmol Vis Sci. 2018;59(2):1144–1157, doi:10.1167/iovs.17-23248.
Quek GL, Liu-Shuang J, Goffaux V, Rossion B. Ultra-coarse, single-glance human face detection in a dynamic visual stream. Neuroimage. 2018;176:465–476, doi:10.1016/ j.neuroimage.2018.04.034.
van de Walle de Ghelcke A, Rossion B, Schiltz C, Lochy A. Developmental changes in neural letter-selectivity: A 1-year follow-up of beginning readers. Dev Sci. 2021;24(1):e12999, doi:10.1111/desc.12999.
Barzegaran E, Norcia AM. Neural sources of letter and Vernier acuity. Sci Rep. 2020;10(1):15449, doi:10.1038/ s41598-020-72370-3.
Brysbaert M. How many words do we read per minute? A review and meta-analysis of reading rate. J Mem Lang. 2019;109:104047, doi:10.1016/j.jml.2019.104047.
Legge GE, Bigelow CA. Does print size matter for reading? A review of findings from vision science and typography. J Vis. 2011;11(5):8–8, doi:10.1167/11.5.8.
Costen NP, Parker DM, Craw I. Spatial content and spatial quantisation effects in face recognition. Perception. 1994;23(2):129–146, doi:10.1068/p230129.
Yan X, Goffaux V, Rossion B. Coarse-to-Fine(r) automatic familiar face recognition in the human brain. Cereb Cortex. 2022;32(8):1560–1573, doi:10.1093/cercor/bhab238.
Whiting S, Jan JE, Wong PKH, Flodmark O, Farrell K, McCormick AQ. Permanent cortical visual impairment in children. Dev Med Child Neurol. 1985;27(6):730–739, doi:10. 1111/j.1469-8749.1985.tb03796.x.
AAPOS. Cortical visual impairment. https://aapos.org/glossary/cortical-visual-impairment. Published 2019. Accessed November 4, 2021.
Saidkasimova S, Bennett DM, Butler S, Dutton GN. Cognitive visual impairment with good visual acuity in children with posterior periventricular white matter injury: A series of 7 cases. J AAPOS. 2007;11(5):426–430, doi:10.1016/j.jaapos. 2007.04.015.
Chandna A, Ghahghaei S, Foster S, Kumar R. Higher visual function deficits in children with cerebral visual impairment and good visual acuity. Front Hum Neurosci. 2021;15(711873):711873, doi:10.3389/fnhum.2021.711873.
Duchaine B, Yovel G. A revised neural framework for face processing. Annu Rev Vis Sci. 2015;1:393–416, doi:10.1146/ annurev-vision-082114-035518.
Grill-Spector K, Weiner KS, Kay K, Gomez J. The functional neuroanatomy of human face perception. Annu Rev Vis Sci. 2017;3:167–196, doi:10.1146/annurev-vision-102016-061214.
Haxby J V., Hoffman EA, Gobbini MI. The distributed human neural system for face perception. Trends Cogn Sci. 2000;4:223–233, doi:10.1016/S1364-6613(00)01482-0.
Rossion B. Face perception. In: Toga AW, ed. Brain Mapping: An Encyclopedic Reference, Vol. 2. Cambridge, MA: Academic Press, Elsevier; 2015:515–522.
Kanwisher N, McDermott J, Chun MM. The fusiform face area: A module in human extrastriate cortex specialized for face perception. J Neurosci. 1997;17:4302–4311, doi:10. 1523/jneurosci.17-11-04302.1997.
Rossion B, Jacques C, Jonas J. Mapping face categorization in the human ventral occipitotemporal cortex with direct neural intracranial recordings. Ann N Y Acad Sci. 2018:5–24, doi:10.1111/nyas.13596.
Wandell BA. The neurobiological basis of seeing words. Ann N Y Acad Sci. 2011;1224:63–80, doi:10.1111/j.1749-6632. 2010.05954.x.
Taylor JSH, Rastle K, Davis MH. Can cognitive models explain brain activation during word and pseudoword reading? A meta-analysis of 36 neuroimaging studies. Psychol Bull. 2013;139:766–791, doi:10.1037/a0030266.
Schuster S, Hawelka S, Richlan F, Ludersdorfer P, Hutzler F. Eyes on words: A fixation-related fMRI study of the left occipito-temporal cortex during self-paced silent reading of words and pseudowords. Sci Rep. 2015;5:12686, doi:10. 1038/srep12686.
Lochy A, Jacques C, Maillard L, Colnat-Coulbois S, Rossion B, Jonas J. Selective visual representation of letters and words in the left ventral occipito-temporal cortex with intracerebral recordings. Proc Natl Acad Sci USA. 2018;115(32):7595–7604, doi:10.1073/pnas.1718987115.
