Individual differences in visual evoked potential latency are associated with variance in brain tissue volume in people with multiple sclerosis: An analysis of brain function-structure correlates

Published:August 14, 2022DOI:


      • Visual evoked potential (VEP) latency predicts whole-brain tissue volume in MS.
      • Combined decrease in gray/white matter was associated with VEP latency delay.
      • Individuals with delayed VEP latency in both eyes had greatest structural disturbance.
      • Delayed VEP latency can serve as a proxy of brain atrophy and lesion load.


      Visual evoked potentials (VEP) index visual pathway functioning, and are often used for clinical assessment and as outcome measures in people with multiple sclerosis (PwMS). VEPs may also reflect broader neural disturbances that extend beyond the visual system, but this possibility requires further investigation. In the present study, we examined the hypothesis that delayed latency of the P100 component of the VEP would be associated with broader structural changes in the brain in PwMS. We obtained VEP latency for a standard pattern-reversal checkerboard stimulus paradigm, in addition to Magnetic Resonance Imaging (MRI) measures of whole brain volume (WBV), gray matter volume (GMV), white matter volume (WMV), and T2-weighted fluid attenuated inversion recovery (FLAIR) white matter lesion volume (FLV). Correlation analyses indicated that prolonged VEP latency was significantly associated with lower WBV, GMV, and WMV, and greater FLV. VEP latency remained significantly associated with WBV, GMV, and WMV even after controlling for the variance associated with inter-ocular latency, age, time between VEP and MRI assessments, and other MRI variables. VEP latency delays were most pronounced in PwMS that exhibited low volume in both white and gray matter simultaneously. Furthermore, PwMS that had delayed VEP latency based on a clinically relevant cutoff (VEP latency ≥ 113 ms) in both eyes had lower WBV, GMV, and WMV and greater FLV in comparison to PwMS that had normal VEP latency in one or both eyes. The findings suggest that PwMS that have delayed latency in both eyes may be particularly at risk for exhibiting greater brain atrophy and lesion volume. These analyses also indicate that VEP latency may index combined gray matter and white matter disturbances, and therefore broader network connectivity and efficiency. VEP latency may therefore provide a surrogate marker of broader structural disturbances in the brain in MS.



      DMT (disease modifying therapy), FLAIR (T2-weighted fluid attenuated inversion recovery), FLV (FLAIR lesion volume), GMV (gray matter volume), IOL (inter-ocular latency), OCT (optical coherence tomography), PwMS (people with multiple sclerosis), VEP (visual evoked potential), WBV (whole brain volume), WMV (white matter volume)
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        • Alshowaeir D.
        • Yiannikas C.
        • Garrick R.
        • et al.
        Latency of multifocal visual evoked potentials in nonoptic neuritis eyes of multiple sclerosis patients associated with optic radiation lesions.
        Investig. Ophthalmol. Vis. Sci. 2014; 55: 3758-3764
        • Andravizou A.
        • Dardiotis E.
        • Artemiadis A.
        • et al.
        Brain atrophy in multiple sclerosis: mechanisms, clinical relevance and treatment options.
        Autoimmun. Highlights. 2019; 10
        • American Clinical Neurophysiology Society
        Guideline 9B: guidelines on visual evoked potentials.
        J. Clin. Neurophysiol. 2006; 23: 138-156
        • Arthurs O.J.
        • Williams E.J.
        • Carpenter T.A.
        • Pickard J.D.
        • Boniface S.J.
        Linear coupling between functional magnetic resonance imaging and evoked potential amplitude in human somatosensory cortex.
        Neuroscience. 2000; 101: 803-806
        • Babiloni C.
        • Blinowska K.
        • Bonanni L.
        • et al.
        What electrophysiology tell us about Alzheimer's disease: a window into the synchronization and connectivity of brain neurons.
        Neurobiol. Aging. 2020; 85: 58-73
        • Backner Y.
        • Levin N.
        Keep your eyes wide open: On visual and vision-related measurements to better understand multiple sclerosis pathophysiology.
        J. Neuroophthalmol. 2018; 38: 85-90
        • Backner Y.
        • Petrou P.
        • Glick-Shames H.
        • et al.
        Vision and vision-related measures in progressive multiple sclerosis.
        Front. Neurol. 2019; 10 (Article 455)
        • Bagnato F.
        • Gauthier S.A.
        • Laule C.
        • et al.
        Imaging mechanisms of disease progression in multiple sclerosis: beyond brain atrophy.
        J. Neuroimaging. 2020; 30: 251-266
        • Barreiro-González A.
        • Sanz M.T.
        • Carratalalà-Boscà S.
        • et al.
        Magnetic resonance imaging and optical coherence tomography correlations in multiple sclerosis beyond anatomical landmarks.
        J. Neurol. Sci. 2020; 419117180
        • Barton J.L.
        • Garber J.Y.
        • Klistorner A.
        • Barnett M.H.
        The electrophysiological assessment of visual function in Multiple Sclerosis.
        Clin. Neurophysiol. Pract. 2019; 4: 90-96
        • Baumhefner R.W.
        • Tourtellotte W.W.
        • Syndulko K.
        • et al.
        Quantitative multiple sclerosis plaque assessment with magnetic resonance imaging: Its correlation with clinical parameters, evoked potentials, and intra-blood-brain barrier IgG synthesis.
        Arch. Neurol. 1990; 47: 19-26
        • Bergsland N.
        • Horakova D.
        • Dwyer M.G.
        • et al.
        Gray matter atrophy patterns in multiple sclerosis: A 10-year source-based morphometry study.
        NeuroImage Clin. 2018; 17: 444-451
        • Berman S.
        • Backner Y.
        • Krupnik R.
        • et al.
        Conduction delays in the visual pathways of progressive multiple sclerosis patients covary with brain structure.
        Neuroimage. 2020; 221117204
        • Bizzo B.C.
        • Arruda-Sanchez T.
        • Tobyne S.M.
        • et al.
        Anterior insular resting-state functional connectivity is related to cognitive reserve in multiple sclerosis.
        J. Neuroimaging. 2021; 31: 98-102
        • Cadavid D.
        • Balcer L.
        • Galetta S.
        • et al.
        for the RENEW Study Investigators. Safety and efficacy of opicinumab in acute optic neuritis (RENEW): a randomized, placebo-controlled, phase 2 trial.
        Lancet Neurol. 2017; 16: 189-199
        • Canham L.J.W.
        • Kane N.
        • Oware A.
        • et al.
        Multimodal neurophysiological evaluation of primary progressive multiple sclerosis – an increasingly valid biomarker, with limits.
        Mult. Scler. Relat. Disord. 2015; 4: 607-613
        • Chiang F.L.
        • Wang Q.
        • Yu F.F.
        • et al.
        Localised grey matter atrophy in multiple sclerosis is network-based: a coordinate-based meta-analysis.
        Clin. Radiol. 2019; 74: 816.e19-816.e28
        • Chirapapaisan N.
        • Laotaweerungsawat S.
        • Chuenkongkaew W.
        • et al.
        Diagnostic value of visual evoked potentials for clinical diagnosis of multiple sclerosis.
        Doc. Ophthalmol. 2015; 19: 25-30
        • Comi G.
        • Filippi M.
        • Martinelli V.
        • et al.
        Brain stem magnetic resonance imaging and evoked potential studies of symptomatic multiple sclerosis patients.
        Eur. Neurol. 1993; 33: 232-237
        • Cooray G.K.
        • Sundgren M.
        • Brismar T.
        Mechanism of visual network dysfunction in relapsing-remitting multiple sclerosis and its relation to cognition.
        Clin. Neurophysiol. 2020; 131: 361-367
        • Cordano C.
        • Sin J.H.
        • Timmons G.
        • et al.
        Validating visual evoked potentials as a preclinical, quantitative biomarker for remyelination efficacy.
        Brain. 2022; (In Press)
        • Covey T.J.
        • Golan D.
        • Doniger G.M.
        • et al.
        The relationship between cognitive impairment, cognitive fatigue, and visual evoked potential latency in multiple sclerosis.
        Mult. Scler. Relat. Disord. 2022; 57 (Article 103349)
        • Covey T.J.
        • Golan D.
        • Doniger G.M.
        • et al.
        Visual evoked potential latency predicts cognitive function in people with multiple sclerosis.
        J. Neurol. 2021; 268: 4311-4320
        • Covey S.
        • Shucard
        Event-related potential indices of cognitive function and brain resource reallocation during working memory in patients with Multiple Sclerosis.
        Clin. Neurophysiol. 2017; 128: 604-621
        • Creel D.
        • Kolb H.
        • Fernandez E.
        • Nelson R.
        Visually Evoked Potentials.
        (editors)Webvision: The Organization of the Retina and Visual System. UT: University of Utah Health Sciences Center, Salt Lake City2012
        • Crnošija L.
        • Gabelić T.
        • Barun B.
        • Adamec I.
        • Krbot Skorić M.
        • Habek M.
        Evoked potentials can predict future disability in people with clinically isolated syndrome.
        Eur. J. Neurol. 2020; 27: 437-444
        • Cruz Gómez Á.J.
        • Ventura Campos N.
        • Belenguer A.
        • Ávila C.
        • Forn C.
        Regional brain atrophy and functional connectivity changes related to fatigue in multiple sclerosis.
        PLoS One. 2013; 8: e77914
        • de Santiago L.
        • Sánchez-Morla E.
        • Blanco R.
        • et al.
        Empirical mode decomposition processing to improve multifocal-visual-evoked-potential signal analysis in multiple sclerosis.
        PLoS One. 2018; 13e0194964
        • Eijlers A.J.C.
        • Meijer K.A.
        • van Geest Q.
        • Geurts J.J.G.
        • Schoonheim M.M.
        Determinants of cognitive impairment in patients with multiple sclerosis with and without atrophy.
        Radiology. 2018; 288: 544-551
        • Elliot C.
        • Belachew S.
        • Wolinsky J.
        • et al.
        Chronic white matter lesion activity predicts clinical progression in primary progressive multiple sclerosis.
        Brain. 2019; 142: 2787-2799
        • Enzinger C.
        • Fazekas F.
        Measuring gray matter and white matter damage in MS: why this is not enough.
        Front. Neurol. 2015; 6
        • Eshaghi A.
        • Marinescu R.V.
        • Young A.L.
        • et al.
        on behalf of the MAGNIMS study group. Progression of regional grey matter atrophy in multiple sclerosis.
        Brain. 2018; 141: 1165-1677
        • Farley B.J.
        • Morozova E.
        • Dion J.
        • et al.
        Evoked potentials as a translatable biomarker to track functional remyelination.
        Mol. Cell. Neurosci. 2019; 99102292
        • Fisniku L.
        • Chard D.T.
        • Jackson J.S.
        • et al.
        Gray matter atrophy is related to long-term disability in multiple sclerosis.
        Ann. Neurol. 2008; 64: 247-254
        • Fuchs T.A.
        • Benedict R.H.B.
        • Bartnik A.
        • et al.
        Preserved network functional connectivity underlies cognitive reserve in multiple sclerosis.
        Hum. Brain Mapp. 2019; 40: 5231-5241
        • Fuhr P.
        • Borggrefe-Chappuis A.
        • Schindler C.
        • Kappos L.
        Visual and motor evoked potentials in the course of multiple sclerosis.
        Brain. 2001; 124: 2162-2168
        • Gareau P.J.
        • Gati J.S.
        • Menon R.S.
        • et al.
        Reduced visual evoked responses in multiple sclerosis patients with optic neuritis: Comparison of functional magnetic resonance imaging and visual evoked potentials.
        Mult. Scler. 1995; 5: 161-164
        • Giesser B.S.
        • Kurtzberg D.
        • Herbert G.
        • et al.
        Trimodal evoked potentials compared with magnetic resonance imaging in the diagnosis of multiple sclerosis.
        Arch. Neurol. 1987; 44: 281-284
        • Giffroy X.
        • Maes N.
        • Albert A.
        • et al.
        Do evoked potentials contribute to the functional follow-up and clinical prognosis of multiple sclerosis?.
        Acta Neurol. Belg. 2016; 117: 53-59
        • Green A.
        • Gelfand J.M.
        • Cree B.A.
        • et al.
        Clemastine fumarate as a remyelinating therapy for multiple sclerosis (ReBUILD): a randomized, controlled, double-blind, crossover trial.
        Lancet. 2017; 390: 2481-2489
        • Hardmeier M.
        • Fuhr P.
        Multimodal evoked potentials as candidate prognostic and response biomarkers in clinical trials of multiple sclerosis.
        J. Clin. Neurophysiol. 2021; 38: 171-180
        • Hardmeier M.
        • Schindler C.
        • Kuhle J.
        • Fuhr P.
        Validation of quantitative scores derived from motor evoked potentials in the assessment of primary progressive multiple sclerosis: a longitudinal study.
        Front. Neurol. 2020; 11: 735
        • Heidari M.
        • Radcliff A.B.
        • McLellan G.J.
        • et al.
        Evoked potentials as a biomarker of remyelination.
        Proc. Natl. Acad. Sci. 2019; 116: 27074-27083
        • Invernizzi P.
        • Bertolasi L.
        • Rachele Bianchi M.
        • Turatti M.
        • Gajofatto A.
        • Donata Benedetti M.
        Prognostic value of multimodal evoked potentials in multiple sclerosis: the EP score.
        J. Neurol. 2011; 258: 1933-1939
        • Jacobsen C.
        • Zivadinov R.
        • Myhr K.M.
        • et al.
        Brain atrophy and clinical characteristics predicting SDMT performance in multiple sclerosis: a 10-year follow-up study.
        Mult. Scler. J. Exp. Transl. Clin. 2021; (January-March:1-10)
        • Jain S.
        • Sima D.
        • Ribbens A.
        • et al.
        Automatic segmentation and volumetry of multiple sclerosis brain lesions from MR images.
        NeuroImage Clin. 2015; 8: 367-375
        • Jakimovski D.
        • Benedict R.H.B.
        • Weinstock-Guttman B.
        • et al.
        Visual deficits and cognitive assessment of multiple sclerosis: confounder, correlate, or both?.
        J. Neurol. 2021; 268: 2578-2588
        • Jung P.
        • Beyerle A.
        • Ziemann U.
        Multimodal evoked potentials measure and predict disability progression in early relapsing-remitting multiple sclerosis.
        Mult. Scler. 2008; 14: 553-556
        • Kallmann B.A.
        • Fackelmann S.
        • Toyka K.V.
        • Rieckmann P.
        • Reiners K.
        Early abnormalities of evoked potentials and future disability in patients with multiple sclerosis.
        Mult. Scler. 2006; 12: 58-65
        • Kira J.-.I.
        • Tobimatsu S.
        • Goto I.
        • Hasuo K.
        Primary progressive versus relapsing remitting multiple sclerosis in Japanese patients: a combined clinical, magnetic resonance imaging and multimodality evoked potential study.
        J. Neurol. Sci. 1993; 117: 179-185
        • Kiiski H.S.M.
        • Riada S.N.
        • Lalor E.C.
        • et al.
        Delayed P100-like latencies in multiple sclerosis: a preliminary investigation using visual evoked spread spectrum analysis.
        PLoS One. 2016; 11e014608
        • Klistorner A.
        • Chai Y.
        • Leocani L.
        • et al.
        Assessment of opicinumab in acute optic neuritis using multifocal visual evoked potential.
        CNS Drugs. 2018; 32: 1159-1171
        • Klistorner A.
        • Triplett J.D.
        • Barnett M.H.
        • et al.
        Latency of multifocal visual evoked potential in multiple sclerosis: a visual pathway biomarker for clinical trials of remyelinating therapies.
        J. Clin. Neurophysiol. 2021; 38: 186-191
        • Kolbe S.
        • Bajraszewski C.
        • Chapman C.
        • et al.
        Diffusion tensor imaging of the optic radiations after optic neuritis.
        Hum. Brain Mapp. 2012; 201233: 2047-2061
        • Kolbe S.C.
        • van der Walt A.
        • Butzkueven H.
        • Klistorner A.
        • Egan G.F.
        • Kilpatrick TJ.
        Serial diffusion tensor imaging of the optic radiations after acute optic Neuritis.
        J. Ophthalmol. 2016; 2764538
        • Koziolek M.J.
        • Tampe D.
        • Bähr M.
        • et al.
        Immunoadsoption therapy in patients with multiple sclerosis with steroid-refractory optical neuritis.
        J. Neuroinflamm. 2012; 9: 1-10
        • Lazeron R.H.C.
        • Boringa J.B.
        • Schouten M.
        • et al.
        Brain atrophy and lesion load as explaining parameters for cognitive impairment in multiple sclerosis.
        Mult. Scler. 2005; 11: 524-531
        • Lebrun C.
        • Bensa C.
        • Debouverie M.
        • et al.
        Association between clinical conversion to multiple sclerosis in radiologically isolated syndrome and magnetic resonance imaging, cerebrospinal fluid, and visual evoked potential.
        Arch. Neurol. 2009; 66: 841-846
        • Leocani L.
        • Guerrieri S.
        • Comi G.
        Visual evoked potentials as a biomarker in multiple sclerosis and associated optic neuritis.
        J. Neuroophthalmol. 2018; 38: 350-357
        • Leocani L.
        • Medaglini S.
        • Comi G.
        Evoked potentials in monitoring multiple sclerosis.
        Neurolog. Sci. 2000; 21: S889-S891
        • Leocani L.
        • Rovaris M.
        • Boneschi F.M.
        • et al.
        Multimodal evoked potentials to assess the evolution of multiple sclerosis: a longitudinal study.
        J. Neurol. Neurosurg. Psychiatry. 2006; 77: 1030-1035
        • Lisicki M.
        • D'Ostilio K.
        • Coppola G.
        • et al.
        Brain correlates of single trial visual evoked potentials in migraine: more than meets the eye.
        Front. Neurol. 2018; 9: 393
        • London F.
        • Sankari S.
        • van Pesch V.
        Early disturbances in multimodal evoked potentials as a prognostic factor for long-term disability in relapsing-remitting multiple sclerosis patients.
        Clin. Neurophysiol. 2017; 128: 561-569
        • Lorefice L.
        • Coghe G.
        • Fenu G.
        • et al.
        Timed up and go’ and brain atrophy: a preliminary MRI study to assess functional mobility performance in multiple sclerosis.
        J. Neurol. 2017; 264: 2201-2204
        • Magnano I.
        • Aiello I.
        • Piras M.R.
        Cognitive impairment and neurophysiological correlates in MS.
        J. Neurol. Sci. 2006; 245: 117-122
        • Margaritella N.
        • Mendozzi L.
        • Garegnani M.
        • et al.
        Sensory evoked potentials to predict short-term progression of disability in multiple sclerosis.
        Neurol. Sci. 2012; 33: 887-892
        • Ngai A.C.
        • Jolley M.A.
        • D'Ambrosio R.
        • Meno J.R.
        • Winn H.R.
        Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat.
        Brain Res. 1999; 837: 221-228
        • Nunez P.L.
        • Srinivasan R.
        • Fields RD.
        EEG functional connectivity, axon delays and white matter disease.
        Clin. Neurophysiol. 2015; 126: 110-120
        • O'Connor P.
        • Marchetti P.
        • Lee L.
        • Perera M.
        Evoked potential abnormality scores are a useful measure of disease burden in relapsing-remitting multiple sclerosis.
        Ann. Neurol. 1998; 44: 404-407
        • O'Connor P.W.
        • Tansey C.M.
        • Detsky A.S.
        • Mushlin A.I.
        • Kucharczyk M.W.
        The effect of spectrum bias on the utility of magnetic resonance imaging and evoked potentials in the diagnosis of suspected multiple sclerosis.
        Neurology. 1996; 47: 140-144
        • Odom J.V.
        • Bach M.
        • Brigell M.
        • et al.
        ISCEV standard for clinical visual evoked potentials: (2016 update).
        Doc. Ophthalmol. 2016; 133: 1-9
        • Ontaneda D.
        • Thompson A.J.
        • Fox R.J.
        • Cohen J.A.
        Progressive multiple sclerosis: prospects for disease therapy, repair, and restoration of function.
        Lancet. 2017; 389: 1357-1366
        • Pelosi L.
        • Geesken J.M.
        • Holly M.
        • et al.
        Working memory impairment in multiple sclerosis: Evidence from an event-related potential study of patients with clinically isolated myelopathy.
        Brain. 1997; 120: 2039-2058
        • Pelayo R.
        • Montalban X.
        • Minoves T.
        • et al.
        Do multimodal evoked potentials add information to MRI in clinically isolated syndromes?.
        Mult. Scler. 2010; 16: 55-61
        • Pinter D.
        • Beckmann C.F.
        • Fazekas F.
        • et al.
        Morphological MRI phenotypes of multiple sclerosis differ in resting-state brain function.
        Sci. Rep. 2019; 9: 16221
        • Popescu V.
        • Agosta F.
        • Hulst H.E.
        • et al.
        on behalf of the MAGNIMS Study Group. Brain atrophy and lesion load predict long term disability in multiple sclerosis.
        J. Neurol. Neurosurg. Psychiatry. 2013; 84: 1082-1091
        • Pokryszko-Dragan A.
        • Zagrajek M.
        • Slotwinski K.
        • et al.
        Event-related potentials and cognitive performance in multiple sclerosis patients with fatigue.
        Neurol. Sci. 2016; 37: 1545-1556
        • Ramanathan S.
        • Lenton K.
        • Burke T.
        • et al.
        The utility of multimodal evoked potentials in multiple sclerosis prognostication.
        J. Clin. Neurosci. 2013; 20: 1576-1581
        • Riederer I.
        • Mühlau M.
        • Hoshi M.-.M.
        • Zimmer C.
        • Kleine JF.
        Detecting optic nerve lesions in clinically isolated syndrome and multiple sclerosis: double-inversion recovery magnetic resonance imaging in comparison with visually evoked potentials.
        J. Neurol. 2019; 266: 148-156
        • Sahraian M.A.
        • Radue E.W.
        • Haller S.
        • Kappos L.
        Black holes in multiple sclerosis: definition, evolution, and clinical correlations.
        Acta Neurol. Scand. 2010; 122: 1-8
        • Sakai R.E.
        • Feller D.J.
        • Galetta K.M.
        • Galetta S.L.
        • Balcer L.J.
        Vision in multiple sclerosis (MS): the story, structure-function correlations, and models for neuroprotection.
        J. Neuroophthalmol. 2011; 31: 362-373
        • Scaioli V.
        • Rumi
        • Cimino C.
        • Angelini L.
        Childhood multiple sclerosis (MS): multimodal evoked potentials (EP) and magnetic resonance imaging (MRI) comparative study.
        Neuropediatrics. 1991; 22: 15-23
        • Schlaeger R.
        • D'Souza M.
        • Schindler C.
        • Grize L.
        • Kappos L.
        • Fuhr P.
        Combined evoked potentials as markers and predictors of disability in early multiple sclerosis.
        Clin. Neurophysiol. 2012; 123: 406-410
        • Schlaeger R.
        • Hardmeier M.
        • D'Souza
        • et al.
        Monitoring multiple sclerosis by multimodal evoked potentials: numerically versus ordinally scaled scoring systems.
        Clin. Neurophysiol. 2016; 127: 1864-1871
        • Shiee N.
        • Bazin P.-.L.
        • Zackowski K.M.
        • et al.
        Revisiting brain atrophy and its relationship to disability in multiple sclerosis.
        PLoS One. 2012; 7: e37049
        • Sinnecker T.
        • Oberwahrenbrock T.
        • Metz I.
        • et al.
        Optic radiation damage in multiple sclerosis is associated with visual dysfunction and retinal thinning – an ultrahigh-field MR pilot study.
        Eur. Radiol. 2015; 25: 122-131
        • Skeen MB.
        Changing paradigms and unmet needs in multiple sclerosis: The role of clinical neurophysiology.
        J. Clin. Neurophysiol. 2021; 38: 162-165
        • Strasser-Fuchs S.
        • Enzinger C.
        • Ropele S.
        • Wallner M.
        • Fazekas F.
        Clinically benign multiple sclerosis despite large T2 lesion load: can we explain this paradox?.
        Mult. Scler. 2006; 14: 205-211
        • Suminaite D.
        • Lyons D.A.
        • Livesey M.R.
        Myelinated axon physiology and regulated of neural circuit function.
        Glia. 2019; 67: 2050-2062
        • Tedeschi G.
        • Dinacci D.
        • Lavorgna L.
        • et al.
        Correlation between fatigue and brain atrophy and lesion load in multiple sclerosis patients independent of disability.
        J. Neurol. Sci. 2007; 263: 15-19
        • Uhlenbrock D.
        • Seidel D.
        • Gehlen W.
        • et al.
        MR imaging in multiple sclerosis: comparison with clinical, CSF, and visual evoked potential findings.
        Am. J. Neuroradiol. 1988; 9: 59-67
        • Vidal-Jordana A.
        • Rovira A.
        • Arrambide G.
        • et al.
        Optic nerve topography in multiple sclerosis diagnosis: The utility of visual evoked potentials.
        Neurology. 2021; 96: e482-e490
        • Wang C.
        • Beadnall H.N.
        • Hatton S.N.
        • et al.
        Automatic brain volumetrics in multiple sclerosis: a step closer to clinical application.
        J. Neurol. Neurosurg. Psychiatry. 2016; 87: 754-757
        • Weinstock-Guttman B.
        • Baier M.
        • Stockton R.
        • et al.
        Pattern reversal visual evoked potentials as a measure of visual pathway pathology in multiple sclerosis.
        Mult. Scler. 2003; 9: 529-534
        • You Y.
        • Klistorner A.
        • Thie J.
        • Graham SI.
        Latency delay of visual evoked potential is a real measurement of demyelination in a rat model of optic neuritis.
        Investig. Ophthalmol. Vis. Sci. 2011; 52: 6911-6918
        • Yperman J.
        • Becker T.
        • Valkenborg D.
        • et al.
        Machine learning analysis of motor evoked potential time series to predict disability progression in multiple sclerosis.
        BMC Neurol. 2020; 20
        • Zaccagna F.
        • Matys T.
        • Massoud TF.
        Optic chiasm morphometry changes in multiple sclerosis: feasibility of a simplified brain magnetic resonance imaging measure of white matter atrophy.
        Clin. Anat. 2019; 32: 1072-1081
        • Zafeiropoulos P.
        • Katsanos A.
        • Kitsos G.
        • Stefaniotou M.
        • Asproudis I.
        The contribution of multifocal evoked potentials in patients with optic neuritis and multiple sclerosis: a review.
        Doc. Ophthalmol. 2021; 142: 283-292