Skip to main content
Top
Published in: Alzheimer's Research & Therapy 1/2023

Open Access 01-12-2023 | Alzheimer's Disease | Research

Disruption of early visual processing in amyloid-positive healthy individuals and mild cognitive impairment

Authors: Daniel C. Javitt, Antigona Martinez, Pejman Sehatpour, Anna Beloborodova, Christian Habeck, Yunglin Gazes, Dalton Bermudez, Qolamreza R. Razlighi, D. P. Devanand, Yaakov Stern

Published in: Alzheimer's Research & Therapy | Issue 1/2023

Login to get access

Abstract

Background

Amyloid deposition is a primary predictor of Alzheimer’s disease (AD) and related neurodegenerative disorders. Retinal changes involving the structure and function of the ganglion cell layer are increasingly documented in both established and prodromal AD. Visual event-related potentials (vERP) are sensitive to dysfunction in the magno- and parvocellular visual systems, which originate within the retinal ganglion cell layer. The present study evaluates vERP as a function of amyloid deposition in aging, and in mild cognitive impairment (MCI).

Methods

vERP to stimulus-onset, motion-onset, and alpha-frequency steady-state (ssVEP) stimuli were obtained from 16 amyloid-positive and 41 amyloid-negative healthy elders and 15 MCI individuals and analyzed using time–frequency approaches. Social cognition was assessed in a subset of individuals using The Awareness of Social Inference Test (TASIT).

Results

Neurocognitively intact but amyloid-positive participants and MCI individuals showed significant deficits in stimulus-onset (theta) and motion-onset (delta) vERP generation relative to amyloid-negative participants (all p < .01). Across healthy elders, a composite index of these measures correlated highly (r =  − .52, p < .001) with amyloid standardized uptake value ratios (SUVR) and TASIT performance. A composite index composed of vERP measures significant differentiated amyloid-positive and amyloid-negative groups with an overall classification accuracy of > 70%.

Discussion

vERP may assist in the early detection of amyloid deposition among older individuals without observable neurocognitive impairments and in linking previously documented retinal deficits in both prodromal AD and MCI to behavioral impairments in social cognition.
Literature
1.
go back to reference Jack CR Jr, Therneau TM, Wiste HJ, Weigand SD, Knopman DS, Lowe VJ, et al. Transition rates between amyloid and neurodegeneration biomarker states and to dementia: a population-based, longitudinal cohort study. Lancet Neurol. 2016;15(1):56–64.PubMedCrossRef Jack CR Jr, Therneau TM, Wiste HJ, Weigand SD, Knopman DS, Lowe VJ, et al. Transition rates between amyloid and neurodegeneration biomarker states and to dementia: a population-based, longitudinal cohort study. Lancet Neurol. 2016;15(1):56–64.PubMedCrossRef
2.
go back to reference Carbonell F, Zijdenbos AP, Charil A, Grand’Maison M, Bedell BJ, Alzheimer’s Disease Neuroimaging I. Optimal target region for subject classification on the basis of amyloid PET images. J Nucl Med. 2015;56(9):1351–8. Carbonell F, Zijdenbos AP, Charil A, Grand’Maison M, Bedell BJ, Alzheimer’s Disease Neuroimaging I. Optimal target region for subject classification on the basis of amyloid PET images. J Nucl Med. 2015;56(9):1351–8.
3.
go back to reference Jansen WJ, Ossenkoppele R, Knol DL, Tijms BM, Scheltens P, Verhey FR, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313(19):1924–38.PubMedPubMedCentralCrossRef Jansen WJ, Ossenkoppele R, Knol DL, Tijms BM, Scheltens P, Verhey FR, et al. Prevalence of cerebral amyloid pathology in persons without dementia: a meta-analysis. JAMA. 2015;313(19):1924–38.PubMedPubMedCentralCrossRef
4.
go back to reference Tolar M, Abushakra S, Sabbagh M. The path forward in Alzheimer’s disease therapeutics: reevaluating the amyloid cascade hypothesis. Alzheimer’s & dementia: the journal of the Alzheimer’s Association. 2020;16(11):1553–60.CrossRef Tolar M, Abushakra S, Sabbagh M. The path forward in Alzheimer’s disease therapeutics: reevaluating the amyloid cascade hypothesis. Alzheimer’s & dementia: the journal of the Alzheimer’s Association. 2020;16(11):1553–60.CrossRef
5.
go back to reference Baldacci F, Mazzucchi S, Della Vecchia A, Giampietri L, Giannini N, Koronyo-Hamaoui M, et al. The path to biomarker-based diagnostic criteria for the spectrum of neurodegenerative diseases. Expert Rev Mol Diagn. 2020;20(4):421–41.PubMedPubMedCentralCrossRef Baldacci F, Mazzucchi S, Della Vecchia A, Giampietri L, Giannini N, Koronyo-Hamaoui M, et al. The path to biomarker-based diagnostic criteria for the spectrum of neurodegenerative diseases. Expert Rev Mol Diagn. 2020;20(4):421–41.PubMedPubMedCentralCrossRef
6.
go back to reference Blennow K, Zetterberg H. Fluid biomarker-based molecular phenotyping of Alzheimer’s disease patients in research and clinical settings. Prog Mol Biol Transl Sci. 2019;168:3–23.PubMedCrossRef Blennow K, Zetterberg H. Fluid biomarker-based molecular phenotyping of Alzheimer’s disease patients in research and clinical settings. Prog Mol Biol Transl Sci. 2019;168:3–23.PubMedCrossRef
7.
go back to reference Romaus-Sanjurjo D, Regueiro U, Lopez-Lopez M, Vazquez-Vazquez L, Ouro A, Lema I, et al. Alzheimer’s disease seen through the eye: ocular alterations and neurodegeneration. Int J Mol Sci. 2022;23(5):2486.PubMedPubMedCentralCrossRef Romaus-Sanjurjo D, Regueiro U, Lopez-Lopez M, Vazquez-Vazquez L, Ouro A, Lema I, et al. Alzheimer’s disease seen through the eye: ocular alterations and neurodegeneration. Int J Mol Sci. 2022;23(5):2486.PubMedPubMedCentralCrossRef
8.
go back to reference Ge YJ, Xu W, Ou YN, Qu Y, Ma YH, Huang YY, et al. Retinal biomarkers in Alzheimer’s disease and mild cognitive impairment: a systematic review and meta-analysis. Ageing Res Rev. 2021;69: 101361.PubMedCrossRef Ge YJ, Xu W, Ou YN, Qu Y, Ma YH, Huang YY, et al. Retinal biomarkers in Alzheimer’s disease and mild cognitive impairment: a systematic review and meta-analysis. Ageing Res Rev. 2021;69: 101361.PubMedCrossRef
9.
go back to reference Fereshetian S, Agranat JS, Siegel N, Ness S, Stein TD, Subramanian ML. Protein and imaging biomarkers in the eye for early detection of Alzheimer’s disease. J Alzheimers Dis Rep. 2021;5(1):375–87.PubMedPubMedCentralCrossRef Fereshetian S, Agranat JS, Siegel N, Ness S, Stein TD, Subramanian ML. Protein and imaging biomarkers in the eye for early detection of Alzheimer’s disease. J Alzheimers Dis Rep. 2021;5(1):375–87.PubMedPubMedCentralCrossRef
10.
go back to reference Gupta VB, Chitranshi N, den Haan J, Mirzaei M, You Y, Lim JK, et al. Retinal changes in Alzheimer’s disease- integrated prospects of imaging, functional and molecular advances. Prog Retin Eye Res. 2021;82:100899.PubMedCrossRef Gupta VB, Chitranshi N, den Haan J, Mirzaei M, You Y, Lim JK, et al. Retinal changes in Alzheimer’s disease- integrated prospects of imaging, functional and molecular advances. Prog Retin Eye Res. 2021;82:100899.PubMedCrossRef
11.
go back to reference López-Cuenca I, Marcos-Dolado A, Yus-Fuertes M, Salobrar-García E, Elvira-Hurtado L, Fernández-Albarral JA, et al. The relationship between retinal layers and brain areas in asymptomatic first-degree relatives of sporadic forms of Alzheimer’s disease: an exploratory analysis. Alzheimers Res Therapy. 2022;14(1):1–18.CrossRef López-Cuenca I, Marcos-Dolado A, Yus-Fuertes M, Salobrar-García E, Elvira-Hurtado L, Fernández-Albarral JA, et al. The relationship between retinal layers and brain areas in asymptomatic first-degree relatives of sporadic forms of Alzheimer’s disease: an exploratory analysis. Alzheimers Res Therapy. 2022;14(1):1–18.CrossRef
12.
go back to reference Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F. Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol. 2001;112(10):1860–7.PubMedCrossRef Parisi V, Restuccia R, Fattapposta F, Mina C, Bucci MG, Pierelli F. Morphological and functional retinal impairment in Alzheimer’s disease patients. Clin Neurophysiol. 2001;112(10):1860–7.PubMedCrossRef
13.
go back to reference Krasodomska K, Lubinski W, Potemkowski A, Honczarenko K. Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease. Doc Ophthalmol. 2010;121(2):111–21.PubMedPubMedCentralCrossRef Krasodomska K, Lubinski W, Potemkowski A, Honczarenko K. Pattern electroretinogram (PERG) and pattern visual evoked potential (PVEP) in the early stages of Alzheimer’s disease. Doc Ophthalmol. 2010;121(2):111–21.PubMedPubMedCentralCrossRef
14.
go back to reference Asanad S, Felix CM, Fantini M, Harrington MG, Sadun AA, Karanjia R. Retinal ganglion cell dysfunction in preclinical Alzheimer’s disease: an electrophysiologic biomarker signature. Sci Rep. 2021;11(1):6344.PubMedPubMedCentralCrossRef Asanad S, Felix CM, Fantini M, Harrington MG, Sadun AA, Karanjia R. Retinal ganglion cell dysfunction in preclinical Alzheimer’s disease: an electrophysiologic biomarker signature. Sci Rep. 2021;11(1):6344.PubMedPubMedCentralCrossRef
15.
go back to reference Byun MS, Park SW, Lee JH, Yi D, Jeon SY, Choi HJ, et al. Association of retinal changes with Alzheimer disease neuroimaging biomarkers in cognitively normal individuals. JAMA Ophthalmol. 2021;139(5):548–56.PubMedPubMedCentralCrossRef Byun MS, Park SW, Lee JH, Yi D, Jeon SY, Choi HJ, et al. Association of retinal changes with Alzheimer disease neuroimaging biomarkers in cognitively normal individuals. JAMA Ophthalmol. 2021;139(5):548–56.PubMedPubMedCentralCrossRef
16.
go back to reference Tulay EE, Guntekin B, Yener G, Bayram A, Basar-Eroglu C, Demiralp T. Evoked and induced EEG oscillations to visual targets reveal a differential pattern of change along the spectrum of cognitive decline in Alzheimer’s disease. Int J Psychophysiol. 2020;155:41–8.PubMedCrossRef Tulay EE, Guntekin B, Yener G, Bayram A, Basar-Eroglu C, Demiralp T. Evoked and induced EEG oscillations to visual targets reveal a differential pattern of change along the spectrum of cognitive decline in Alzheimer’s disease. Int J Psychophysiol. 2020;155:41–8.PubMedCrossRef
17.
go back to reference Kremers J, McKeefry DJ, Murray IJ, Parry NRA. Developments in non-invasive visual electrophysiology. Vision Res. 2020;174:50–6.PubMedCrossRef Kremers J, McKeefry DJ, Murray IJ, Parry NRA. Developments in non-invasive visual electrophysiology. Vision Res. 2020;174:50–6.PubMedCrossRef
18.
go back to reference Butler PD, Martinez A, Foxe JJ, Kim D, Zemon V, Silipo G, et al. Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain. 2007;130(Pt 2):417–30.PubMedCrossRef Butler PD, Martinez A, Foxe JJ, Kim D, Zemon V, Silipo G, et al. Subcortical visual dysfunction in schizophrenia drives secondary cortical impairments. Brain. 2007;130(Pt 2):417–30.PubMedCrossRef
19.
go back to reference Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA. Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp. 2002;15(2):95–111.PubMedCrossRef Di Russo F, Martinez A, Sereno MI, Pitzalis S, Hillyard SA. Cortical sources of the early components of the visual evoked potential. Hum Brain Mapp. 2002;15(2):95–111.PubMedCrossRef
20.
go back to reference Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC. Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry. 2002;59(11):1011–20.PubMedCrossRef Doniger GM, Foxe JJ, Murray MM, Higgins BA, Javitt DC. Impaired visual object recognition and dorsal/ventral stream interaction in schizophrenia. Arch Gen Psychiatry. 2002;59(11):1011–20.PubMedCrossRef
21.
go back to reference Haenschel C, Bittner RA, Haertling F, Rotarska-Jagiela A, Maurer K, Singer W, et al. Contribution of impaired early-stage visual processing to working memory dysfunction in adolescents with schizophrenia: a study with event-related potentials and functional magnetic resonance imaging. Arch Gen Psychiatry. 2007;64(11):1229–40.PubMedCrossRef Haenschel C, Bittner RA, Haertling F, Rotarska-Jagiela A, Maurer K, Singer W, et al. Contribution of impaired early-stage visual processing to working memory dysfunction in adolescents with schizophrenia: a study with event-related potentials and functional magnetic resonance imaging. Arch Gen Psychiatry. 2007;64(11):1229–40.PubMedCrossRef
22.
go back to reference Turetsky BI, Kohler CG, Indersmitten T, Bhati MT, Charbonnier D, Gur RC. Facial emotion recognition in schizophrenia: when and why does it go awry? Schizophr Res. 2007;94(1–3):253–63.PubMedPubMedCentralCrossRef Turetsky BI, Kohler CG, Indersmitten T, Bhati MT, Charbonnier D, Gur RC. Facial emotion recognition in schizophrenia: when and why does it go awry? Schizophr Res. 2007;94(1–3):253–63.PubMedPubMedCentralCrossRef
23.
go back to reference Dias EC, Sheridan H, Martinez A, Sehatpour P, Silipo G, Rohrig S, et al. Neurophysiological, oculomotor, and computational modeling of impaired reading ability in schizophrenia. Schizophr Bull. 2021;47(1):97–107.PubMedCrossRef Dias EC, Sheridan H, Martinez A, Sehatpour P, Silipo G, Rohrig S, et al. Neurophysiological, oculomotor, and computational modeling of impaired reading ability in schizophrenia. Schizophr Bull. 2021;47(1):97–107.PubMedCrossRef
24.
go back to reference Nguyen J, Rothman A, Fitzgerald K, Whetstone A, Syc-Mazurek S, Aquino J, et al. Visual pathway measures are associated with neuropsychological function in multiple sclerosis. Curr Eye Res. 2018;43(7):941–8.PubMedPubMedCentralCrossRef Nguyen J, Rothman A, Fitzgerald K, Whetstone A, Syc-Mazurek S, Aquino J, et al. Visual pathway measures are associated with neuropsychological function in multiple sclerosis. Curr Eye Res. 2018;43(7):941–8.PubMedPubMedCentralCrossRef
25.
go back to reference Martinez A, Tobe R, Dias EC, Ardekani BA, Veenstra-VanderWeele J, Patel G, et al. Differential patterns of visual sensory alteration underlying face emotion recognition impairment and motion perception deficits in schizophrenia and autism spectrum disorder. Biol Psychiatry. 2019;86(7):557–67.PubMedPubMedCentralCrossRef Martinez A, Tobe R, Dias EC, Ardekani BA, Veenstra-VanderWeele J, Patel G, et al. Differential patterns of visual sensory alteration underlying face emotion recognition impairment and motion perception deficits in schizophrenia and autism spectrum disorder. Biol Psychiatry. 2019;86(7):557–67.PubMedPubMedCentralCrossRef
26.
go back to reference Kuba M, Kubová Z, Kremláček J, Langrová J. Motion-onset VEPs: characteristics, methods, and diagnostic use. Vision Res. 2007;47(2):189–202.PubMedCrossRef Kuba M, Kubová Z, Kremláček J, Langrová J. Motion-onset VEPs: characteristics, methods, and diagnostic use. Vision Res. 2007;47(2):189–202.PubMedCrossRef
27.
go back to reference Javitt DC, Siegel SJ, Spencer KM, Mathalon DH, Hong LE, Martinez A, et al. A roadmap for development of neuro-oscillations as translational biomarkers for treatment development in neuropsychopharmacology. Neuropsychopharmacol. 2020;45(9):1411–22.CrossRef Javitt DC, Siegel SJ, Spencer KM, Mathalon DH, Hong LE, Martinez A, et al. A roadmap for development of neuro-oscillations as translational biomarkers for treatment development in neuropsychopharmacology. Neuropsychopharmacol. 2020;45(9):1411–22.CrossRef
28.
go back to reference Martinez A, Gaspar PA, Hillyard SA, Andersen SK, Lopez-Calderon J, Corcoran CM, et al. Impaired motion processing in schizophrenia and the attenuated psychosis syndrome: etiological and clinical implications. Am J Psychiatry. 2018;175(12):1243–54.PubMedPubMedCentralCrossRef Martinez A, Gaspar PA, Hillyard SA, Andersen SK, Lopez-Calderon J, Corcoran CM, et al. Impaired motion processing in schizophrenia and the attenuated psychosis syndrome: etiological and clinical implications. Am J Psychiatry. 2018;175(12):1243–54.PubMedPubMedCentralCrossRef
29.
go back to reference McDonald S, Bornhofen C, Shum D, Long E, Saunders C, Neulinger K. Reliability and validity of The Awareness of Social Inference Test (TASIT): a clinical test of social perception. Disabil Rehabil. 2006;28(24):1529–42.PubMedCrossRef McDonald S, Bornhofen C, Shum D, Long E, Saunders C, Neulinger K. Reliability and validity of The Awareness of Social Inference Test (TASIT): a clinical test of social perception. Disabil Rehabil. 2006;28(24):1529–42.PubMedCrossRef
30.
go back to reference Pinkham AE, Penn DL, Green MF, Harvey PD. Social cognition psychometric evaluation: results of the initial psychometric study. Schizophr Bull. 2016;42(2):494–504.PubMedCrossRef Pinkham AE, Penn DL, Green MF, Harvey PD. Social cognition psychometric evaluation: results of the initial psychometric study. Schizophr Bull. 2016;42(2):494–504.PubMedCrossRef
31.
go back to reference Pinkham AE, Harvey PD, Penn DL. Social cognition psychometric evaluation: results of the final validation study. Schizophr Bull. 2017;44:737.PubMedCentralCrossRef Pinkham AE, Harvey PD, Penn DL. Social cognition psychometric evaluation: results of the final validation study. Schizophr Bull. 2017;44:737.PubMedCentralCrossRef
32.
go back to reference Sehatpour P, Bassir Nia A, Adair D, Wang Z, DeBaun HM, Silipo G, et al. Multimodal computational modeling of visual object recognition deficits but intact repetition priming in schizophrenia. Front Psychiatry. 2020;11:547189.PubMedPubMedCentralCrossRef Sehatpour P, Bassir Nia A, Adair D, Wang Z, DeBaun HM, Silipo G, et al. Multimodal computational modeling of visual object recognition deficits but intact repetition priming in schizophrenia. Front Psychiatry. 2020;11:547189.PubMedPubMedCentralCrossRef
33.
go back to reference Martinez A, Revheim N, Butler PD, Guilfoyle DN, Dias EC, Javitt DC. Impaired magnocellular/dorsal stream activation predicts impaired reading ability in schizophrenia. NeuroImage Clinical. 2012;2:8–16.PubMedPubMedCentralCrossRef Martinez A, Revheim N, Butler PD, Guilfoyle DN, Dias EC, Javitt DC. Impaired magnocellular/dorsal stream activation predicts impaired reading ability in schizophrenia. NeuroImage Clinical. 2012;2:8–16.PubMedPubMedCentralCrossRef
34.
go back to reference Butler PD, Abeles IY, Weiskopf NG, Tambini A, Jalbrzikowski M, Legatt ME, et al. Sensory contributions to impaired emotion processing in schizophrenia. Schizophr Bull. 2009;35(6):1095–107.PubMedPubMedCentralCrossRef Butler PD, Abeles IY, Weiskopf NG, Tambini A, Jalbrzikowski M, Legatt ME, et al. Sensory contributions to impaired emotion processing in schizophrenia. Schizophr Bull. 2009;35(6):1095–107.PubMedPubMedCentralCrossRef
35.
go back to reference Patel GH, Arkin SC, Ruiz-Betancourt DR, DeBaun HM, Strauss NE, Bartel LP, et al. What you see is what you get: visual scanning failures of naturalistic social scenes in schizophrenia. Psychol Med. 2020:1–10. Patel GH, Arkin SC, Ruiz-Betancourt DR, DeBaun HM, Strauss NE, Bartel LP, et al. What you see is what you get: visual scanning failures of naturalistic social scenes in schizophrenia. Psychol Med. 2020:1–10.
36.
go back to reference Patel GH, Arkin SC, Ruiz-Betancourt DR, Plaza FI, Mirza SA, Vieira DJ, et al. Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia. Brain. 2021;144(6):1898–910.PubMedPubMedCentralCrossRef Patel GH, Arkin SC, Ruiz-Betancourt DR, Plaza FI, Mirza SA, Vieira DJ, et al. Failure to engage the temporoparietal junction/posterior superior temporal sulcus predicts impaired naturalistic social cognition in schizophrenia. Brain. 2021;144(6):1898–910.PubMedPubMedCentralCrossRef
37.
go back to reference Lavrencic LM, Kurylowicz L, Valenzuela MJ, Churches OF, Keage HA. Social cognition is not associated with cognitive reserve in older adults. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2016;23(1):61–77.PubMedCrossRef Lavrencic LM, Kurylowicz L, Valenzuela MJ, Churches OF, Keage HA. Social cognition is not associated with cognitive reserve in older adults. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2016;23(1):61–77.PubMedCrossRef
38.
go back to reference Martin AK, Ceslis A, Robinson GA. Social inference from middle to older adulthood. Arch Clin Neuropsychol. 2022;37(8):1653–61.PubMedCrossRef Martin AK, Ceslis A, Robinson GA. Social inference from middle to older adulthood. Arch Clin Neuropsychol. 2022;37(8):1653–61.PubMedCrossRef
39.
go back to reference Phillips LH, Allen R, Bull R, Hering A, Kliegel M, Channon S. Older adults have difficulty in decoding sarcasm. Dev Psychol. 2015;51(12):1840–52.PubMedCrossRef Phillips LH, Allen R, Bull R, Hering A, Kliegel M, Channon S. Older adults have difficulty in decoding sarcasm. Dev Psychol. 2015;51(12):1840–52.PubMedCrossRef
40.
go back to reference McDonald S, Honan C, Allen SK, El-Helou R, Kelly M, Kumfor F, et al. Normal adult and adolescent performance on TASIT-S, a short version of The Assessment of Social Inference Test. Clin Neuropsychol. 2018;32(4):700–19.PubMedCrossRef McDonald S, Honan C, Allen SK, El-Helou R, Kelly M, Kumfor F, et al. Normal adult and adolescent performance on TASIT-S, a short version of The Assessment of Social Inference Test. Clin Neuropsychol. 2018;32(4):700–19.PubMedCrossRef
41.
go back to reference Mattis S. Dementia Rating Scale (DRS). Odessa, FL: Psychological Assessment Resources; 1988. Mattis S. Dementia Rating Scale (DRS). Odessa, FL: Psychological Assessment Resources; 1988.
42.
go back to reference Buschke H, Fuld PA. Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology. 1974;24(11):1019–25.PubMedCrossRef Buschke H, Fuld PA. Evaluating storage, retention, and retrieval in disordered memory and learning. Neurology. 1974;24(11):1019–25.PubMedCrossRef
43.
go back to reference Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dementia. 2011;7(3):270–9.CrossRef Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dementia. 2011;7(3):270–9.CrossRef
44.
go back to reference Acharya JN, Hani AJ, Thirumala PD, Tsuchida TN. American Clinical Neurophysiology Society Guideline 3: A proposal for standard montages to be used in clinical EEG. J Clin Neurophysiol. 2016;33(4):312–6.PubMedCrossRef Acharya JN, Hani AJ, Thirumala PD, Tsuchida TN. American Clinical Neurophysiology Society Guideline 3: A proposal for standard montages to be used in clinical EEG. J Clin Neurophysiol. 2016;33(4):312–6.PubMedCrossRef
46.
go back to reference Knesaurek K, Warnock G, Kostakoglu L, Burger C, for Alzheimer’s Disease Neouroimaging I. Comparison of standardized uptake value ratio calculations in amyloid positron emission tomography brain imaging. World J Nucl Med. 2018;17(1):21–6. Knesaurek K, Warnock G, Kostakoglu L, Burger C, for Alzheimer’s Disease Neouroimaging I. Comparison of standardized uptake value ratio calculations in amyloid positron emission tomography brain imaging. World J Nucl Med. 2018;17(1):21–6.
47.
go back to reference Lao PJ, Boehme AK, Morales C, Laing KK, Chesebro A, Igwe KC, et al. Amyloid, cerebrovascular disease, and neurodegeneration biomarkers are associated with cognitive trajectories in a racially and ethnically diverse, community-based sample. Neurobiol Aging. 2022;117:83–96.PubMedCrossRef Lao PJ, Boehme AK, Morales C, Laing KK, Chesebro A, Igwe KC, et al. Amyloid, cerebrovascular disease, and neurodegeneration biomarkers are associated with cognitive trajectories in a racially and ethnically diverse, community-based sample. Neurobiol Aging. 2022;117:83–96.PubMedCrossRef
48.
go back to reference Martinez A, Tobe RH, Gaspar PA, Malinsky D, Dias EC, Sehatpour P, et al. Disease-specific contribution of pulvinar dysfunction to impaired emotion recognition in schizophrenia. Front Behav Neurosci. 2021;15: 787383.PubMedCrossRef Martinez A, Tobe RH, Gaspar PA, Malinsky D, Dias EC, Sehatpour P, et al. Disease-specific contribution of pulvinar dysfunction to impaired emotion recognition in schizophrenia. Front Behav Neurosci. 2021;15: 787383.PubMedCrossRef
49.
go back to reference Cohen J. Statistical power analysis for the behavioral sciences, 2nd edition. Hillsdale, NJ: Lawrence Erlbaum Assoc.; 1988. Cohen J. Statistical power analysis for the behavioral sciences, 2nd edition. Hillsdale, NJ: Lawrence Erlbaum Assoc.; 1988.
50.
go back to reference Yamasaki T, Horie S, Muranaka H, Kaseda Y, Mimori Y, Tobimatsu S. Relevance of in vivo neurophysiological biomarkers for mild cognitive impairment and Alzheimer’s disease. J Alzheimers Dis. 2012;31(Suppl 3):S137–54.PubMedCrossRef Yamasaki T, Horie S, Muranaka H, Kaseda Y, Mimori Y, Tobimatsu S. Relevance of in vivo neurophysiological biomarkers for mild cognitive impairment and Alzheimer’s disease. J Alzheimers Dis. 2012;31(Suppl 3):S137–54.PubMedCrossRef
51.
go back to reference Yoonessi A, Yoonessi A. Functional assessment of magno, parvo and konio-cellular pathways; current state and future clinical applications. J Ophthalmic Vis Res. 2011;6(2):119–26.PubMedPubMedCentral Yoonessi A, Yoonessi A. Functional assessment of magno, parvo and konio-cellular pathways; current state and future clinical applications. J Ophthalmic Vis Res. 2011;6(2):119–26.PubMedPubMedCentral
52.
go back to reference Sartucci F, Borghetti D, Bocci T, Murri L, Orsini P, Porciatti V, et al. Dysfunction of the magnocellular stream in Alzheimer’s disease evaluated by pattern electroretinograms and visual evoked potentials. Brain Res Bull. 2010;82(3–4):169–76.PubMedPubMedCentralCrossRef Sartucci F, Borghetti D, Bocci T, Murri L, Orsini P, Porciatti V, et al. Dysfunction of the magnocellular stream in Alzheimer’s disease evaluated by pattern electroretinograms and visual evoked potentials. Brain Res Bull. 2010;82(3–4):169–76.PubMedPubMedCentralCrossRef
53.
go back to reference Morrison C, Rabipour S, Taler V, Sheppard C, Knoefel F. Visual event-related potentials in mild cognitive impairment and Alzheimer’s disease: a literature review. Curr Alzheimer Res. 2019;16(1):67–89.PubMedCrossRef Morrison C, Rabipour S, Taler V, Sheppard C, Knoefel F. Visual event-related potentials in mild cognitive impairment and Alzheimer’s disease: a literature review. Curr Alzheimer Res. 2019;16(1):67–89.PubMedCrossRef
54.
go back to reference Yamasaki T. Use of VEPs as electrodiagnostic biomarkers of mild cognitive impairment. Neurol Clin Neurosci. 2021;9:3–9.CrossRef Yamasaki T. Use of VEPs as electrodiagnostic biomarkers of mild cognitive impairment. Neurol Clin Neurosci. 2021;9:3–9.CrossRef
55.
go back to reference Yener GG, Emek-Savas DD, Guntekin B, Basar E. The visual cognitive network, but not the visual sensory network, is affected in amnestic mild cognitive impairment: a study of brain oscillatory responses. Brain Res. 2014;1585:141–9.PubMedCrossRef Yener GG, Emek-Savas DD, Guntekin B, Basar E. The visual cognitive network, but not the visual sensory network, is affected in amnestic mild cognitive impairment: a study of brain oscillatory responses. Brain Res. 2014;1585:141–9.PubMedCrossRef
56.
go back to reference Trick GL, Silverman SE. Visual sensitivity to motion: age-related changes and deficits in senile dementia of the Alzheimer type. Neurology. 1991;41(9):1437–40.PubMedCrossRef Trick GL, Silverman SE. Visual sensitivity to motion: age-related changes and deficits in senile dementia of the Alzheimer type. Neurology. 1991;41(9):1437–40.PubMedCrossRef
57.
go back to reference O’Brien HL, Tetewsky SJ, Avery LM, Cushman LA, Makous W, Duffy CJ. Visual mechanisms of spatial disorientation in Alzheimer’s disease. Cereb Cortex. 2001;11(11):1083–92.PubMedCrossRef O’Brien HL, Tetewsky SJ, Avery LM, Cushman LA, Makous W, Duffy CJ. Visual mechanisms of spatial disorientation in Alzheimer’s disease. Cereb Cortex. 2001;11(11):1083–92.PubMedCrossRef
58.
go back to reference Yamasaki T, Goto Y, Ohyagi Y, Monji A, Munetsuna S, Minohara M, et al. Selective impairment of optic flow perception in amnestic mild cognitive impairment: evidence from event-related potentials. J Alzheimers Dis. 2012;28(3):695–708.PubMedCrossRef Yamasaki T, Goto Y, Ohyagi Y, Monji A, Munetsuna S, Minohara M, et al. Selective impairment of optic flow perception in amnestic mild cognitive impairment: evidence from event-related potentials. J Alzheimers Dis. 2012;28(3):695–708.PubMedCrossRef
59.
go back to reference Yamasaki T, Horie S, Ohyagi Y, Tanaka E, Nakamura N, Goto Y, et al. A potential VEP biomarker for mild cognitive impairment: evidence from selective visual deficit of higher-level dorsal pathway. J Alzheimers Dis. 2016;53(2):661–76.PubMedCrossRef Yamasaki T, Horie S, Ohyagi Y, Tanaka E, Nakamura N, Goto Y, et al. A potential VEP biomarker for mild cognitive impairment: evidence from selective visual deficit of higher-level dorsal pathway. J Alzheimers Dis. 2016;53(2):661–76.PubMedCrossRef
60.
go back to reference Fernandez R, Monacelli A, Duffy CJ. Visual motion event related potentials distinguish aging and Alzheimer’s disease. J Alzheimers Dis. 2013;36(1):177–83.PubMedPubMedCentralCrossRef Fernandez R, Monacelli A, Duffy CJ. Visual motion event related potentials distinguish aging and Alzheimer’s disease. J Alzheimers Dis. 2013;36(1):177–83.PubMedPubMedCentralCrossRef
61.
go back to reference Kubova Z, Kremlacek J, Valis M, Langrova J, Szanyi J, Vit F, et al. Visual evoked potentials to pattern, motion and cognitive stimuli in Alzheimer’s disease. Doc Ophthalmol. 2010;121(1):37–49.PubMedCrossRef Kubova Z, Kremlacek J, Valis M, Langrova J, Szanyi J, Vit F, et al. Visual evoked potentials to pattern, motion and cognitive stimuli in Alzheimer’s disease. Doc Ophthalmol. 2010;121(1):37–49.PubMedCrossRef
62.
go back to reference Yamasaki T, Aso T, Kaseda Y, Mimori Y, Doi H, Matsuoka N, et al. Decreased stimulus-driven connectivity of the primary visual cortex during visual motion stimulation in amnestic mild cognitive impairment: An fMRI study. Neurosci Lett. 2019;711: 134402.PubMedCrossRef Yamasaki T, Aso T, Kaseda Y, Mimori Y, Doi H, Matsuoka N, et al. Decreased stimulus-driven connectivity of the primary visual cortex during visual motion stimulation in amnestic mild cognitive impairment: An fMRI study. Neurosci Lett. 2019;711: 134402.PubMedCrossRef
63.
go back to reference Criscuolo C, Cerri E, Fabiani C, Capsoni S, Cattaneo A, Domenici L. The retina as a window to early dysfunctions of Alzheimer’s disease following studies with a 5xFAD mouse model. Neurobiol Aging. 2018;67:181–8.PubMedCrossRef Criscuolo C, Cerri E, Fabiani C, Capsoni S, Cattaneo A, Domenici L. The retina as a window to early dysfunctions of Alzheimer’s disease following studies with a 5xFAD mouse model. Neurobiol Aging. 2018;67:181–8.PubMedCrossRef
64.
go back to reference Guo L, Ravindran N, Shamsher E, Hill D, Cordeiro MF. Retinal changes in transgenic mouse models of Alzheimer’s disease. Curr Alzheimer Res. 2021;18(2):89–102.PubMedCrossRef Guo L, Ravindran N, Shamsher E, Hill D, Cordeiro MF. Retinal changes in transgenic mouse models of Alzheimer’s disease. Curr Alzheimer Res. 2021;18(2):89–102.PubMedCrossRef
65.
go back to reference Karaduman A, Karoglu-Eravsar ET, Kaya U, Aydin A, Adams MM, Kafaligonul H. The optomotor response of aging zebrafish reveals a complex relationship between visual motion characteristics and cholinergic system. Neurobiol Aging. 2021;98:21–32.PubMedCrossRef Karaduman A, Karoglu-Eravsar ET, Kaya U, Aydin A, Adams MM, Kafaligonul H. The optomotor response of aging zebrafish reveals a complex relationship between visual motion characteristics and cholinergic system. Neurobiol Aging. 2021;98:21–32.PubMedCrossRef
66.
go back to reference Duke Han S, Nguyen CP, Stricker NH, Nation DA. Detectable neuropsychological differences in early preclinical Alzheimer’s disease: a meta-analysis. Neuropsychol Rev. 2017;27(4):305–25.PubMedCrossRef Duke Han S, Nguyen CP, Stricker NH, Nation DA. Detectable neuropsychological differences in early preclinical Alzheimer’s disease: a meta-analysis. Neuropsychol Rev. 2017;27(4):305–25.PubMedCrossRef
67.
go back to reference Ranasinghe KG, Cha J, Iaccarino L, Hinkley LB, Beagle AJ, Pham J, et al. Neurophysiological signatures in Alzheimer’s disease are distinctly associated with TAU, amyloid-beta accumulation, and cognitive decline. Sci Transl Med. 2020;12(534):eaaz4069. Ranasinghe KG, Cha J, Iaccarino L, Hinkley LB, Beagle AJ, Pham J, et al. Neurophysiological signatures in Alzheimer’s disease are distinctly associated with TAU, amyloid-beta accumulation, and cognitive decline. Sci Transl Med. 2020;12(534):eaaz4069.
68.
go back to reference Kern RS, Green MF, Fiske AP, Kee KS, Lee J, Sergi MJ, et al. Theory of mind deficits for processing counterfactual information in persons with chronic schizophrenia. Psychol Med. 2009;39(4):645–54.PubMedCrossRef Kern RS, Green MF, Fiske AP, Kee KS, Lee J, Sergi MJ, et al. Theory of mind deficits for processing counterfactual information in persons with chronic schizophrenia. Psychol Med. 2009;39(4):645–54.PubMedCrossRef
69.
go back to reference Green MF, Horan WP, Lee J. Social cognition in schizophrenia. Nat Rev Neurosci. 2015;16(10):620–31.PubMedCrossRef Green MF, Horan WP, Lee J. Social cognition in schizophrenia. Nat Rev Neurosci. 2015;16(10):620–31.PubMedCrossRef
70.
71.
go back to reference Jansen WJ, Janssen O, Tijms BM, Vos SJB, Ossenkoppele R, Visser PJ, et al. Prevalence estimates of amyloid abnormality across the Alzheimer disease clinical spectrum. JAMA Neurol. 2022;79(3):228–43.PubMedCrossRef Jansen WJ, Janssen O, Tijms BM, Vos SJB, Ossenkoppele R, Visser PJ, et al. Prevalence estimates of amyloid abnormality across the Alzheimer disease clinical spectrum. JAMA Neurol. 2022;79(3):228–43.PubMedCrossRef
Metadata
Title
Disruption of early visual processing in amyloid-positive healthy individuals and mild cognitive impairment
Authors
Daniel C. Javitt
Antigona Martinez
Pejman Sehatpour
Anna Beloborodova
Christian Habeck
Yunglin Gazes
Dalton Bermudez
Qolamreza R. Razlighi
D. P. Devanand
Yaakov Stern
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2023
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-023-01189-7

Other articles of this Issue 1/2023

Alzheimer's Research & Therapy 1/2023 Go to the issue